1
Three-dimensional visualization of the tubular-lamellar transformation of the 1
internal plastid membrane network during runner bean chloroplast biogenesis 2
3
Łucja Kowalewska1 Radosław Mazur2 Szymon Suski3 Maciej Garstka2 and 4
Agnieszka Mostowska1 5 1Department of Plant Anatomy and Cytology 2Department of Metabolic Regulation 6
Faculty of Biology University of Warsaw Miecznikowa 1 02-096 Warsaw Poland 7 3Laboratory of Electron Microscopy Nencki Institute of Experimental Biology Polish 8
Academy of Sciences Pasteura 3 02-093 Warsaw Poland 9
10
Corresponding author e-mail mostowagbioluwedupl 11
12
Short title 3D models of chloroplast membrane biogenesis 13
14
The author responsible for distribution of materials integral to the findings presented 15
in this article in accordance with the policy described in the Instructions for Authors 16
(wwwplantcellorg) is Agnieszka Mostowska (mostowagbioluwedupl) 17
18
19
Synopsis Three-dimensional visualization of the internal plastid membrane network 20
using electron tomography revealed a dynamic tubular-parallel transformation and a 21
helical manner of grana formation during runner bean chloroplast biogenesis 22
23
Plant Cell Advance Publication Published on March 21 2016 doi101105tpc1501053
copy2016 American Society of Plant Biologists All Rights Reserved
2
ABSTRACT 24
25
Chloroplast biogenesis is a complex process that is integrated with plant 26
development leading to fully differentiated and functionally mature plastids In this 27
work we used electron tomography and confocal microscopy to reconstruct the 28
process of structural membrane transformation during the etioplast-to-chloroplast 29
transition in runner bean (Phaseolus coccineus L) During chloroplast development 30
the regular tubular network of paracrystalline prolamellar bodies (PLBs) and the 31
flattened porous membranes of prothylakoids (PTs) develop into the chloroplast 32
thylakoids Three-dimensional (3D) reconstruction is required to provide us with a 33
more complete understanding of this transformation We provide spatial models of 34
the bean chloroplast biogenesis that allow such reconstruction of the internal 35
membranes of the developing chloroplast and visualize the transformation from the 36
tubular arrangement to the linear system of parallel lamellae We prove that the 37
tubular structure of the PLB transforms directly to flat slats without dispersion to 38
vesicles We demonstrate that the granastroma thylakoid connections have a helical 39
character starting from the early stages of appressed membrane formation 40
Moreover we point out the importance of particular chlorophyll-protein (CP) complex 41
components in the membrane stacking during the biogenesis The main stages of 42
chloroplast internal membrane biogenesis are presented in a movie that shows the 43
time development of the chloroplast biogenesis as a dynamic model of this process 44
45
3
INTRODUCTION 46
47
Chloroplast biogenesis is a complex process that is essential for plant ontogenesis It 48
involves changes in gene expression together with the transcriptional and 49
translational control of both nuclear and plastid genes These genes can be regulated 50
by anterograde and retrograde signals the synthesis of necessary lipids and 51
pigments the import and routing of the nucleus-encoded proteins into plastids 52
protein-lipid interactions the insertion of proteins into the plastid membranes and the 53
assembly into functional complexes (eg Vothknecht and Westhoff 2001 Baena-54
Gonzaacutelez and Aro 2002 Kota et al 2002 Stern et al 2004 Loacutepez-Juez 2007 55
Waters and Langdale 2009 Solymosi and Schoefs 2010 Adam et al 2011 56
Pogson and Albrecht 2011 Ling et al 2012 Jarvis and Loacutepez-Juez 2013 Lyska et 57
al 2013 Belcher et al 2015 Boumlrner et al 2015 DallrsquoOsto et al 2015 Ling and 58
Jarvis 2015 Rast et al 2015 Sun and Zerges 2015 Yang et al 2015) Chloroplast 59
biogenesis is highly integrated with cell and plant development especially with 60
photomorphogenesis (Pogson et al 2015) and is controlled by cellular and 61
organismal regulatory mechanisms such as the ubiquitin-proteasome system (Jarvis 62
and Loacutepez-Juez 2013) Although biogenesis of chloroplasts has been a subject of 63
investigations for many years the correlation of simultaneous changes at the 64
structural biochemical and functional level was described only recently when time 65
dependent models of chloroplast biogenesis for bean (Phaseolus vulgaris L) and 66
pea (Pisum sativum L) were described (Rudowska et al 2012) 67
The development of chloroplasts up to the stage of etioplasts often takes place when 68
seedling growth proceeds without light Etioplasts contain characteristic structures 69
known as prolamellar bodies (PLBs) that have tubules joined together in a regular 70
network and have a special paracrystalline symmetry Together with prothylakoids 71
(PTs) mdash flattened porous membranes PLBs are precursors of the chloroplast 72
thylakoid membranes PLBs are observed under natural growing conditions when the 73
first stages of seed germination proceed under the ground and are not artificial 74
laboratory phenomena (Solymosi et al 2007 Solymosi and Schoefs 2010 Vitaacutenyi 75
et al 2013) The paracrystalline structure of PLBs can differ depending on the 76
species and the conditions of PLB crystallization All types of paracrystalline 77
arrangements have an exceptionally high surface-to-volume ratio (Gunning 2001) 78
4
Although the formation of etioplasts in darkness which have a characteristic 79
paracrystalline PLB and their transformation upon exposure to light has been 80
documented since the 1960rsquos (eg Gunning 1965 2001 Mostowska 1986a 1986b 81
Solymosi and Schoefs 2010) but the spatial arrangement of these changes is still not 82
known 83
Despite of 60 years of studies the true organization of the paracrystalline 84
membranes in three dimensions (3D) have remained unclear Cubic membranes 85
other than PLBs were described in different biological systems especially in stressed 86
conditions or virally infected cells (Almsherqi et al 2006 2009 Deng et al 2010) 87
However this widespread phenomenon is poorly understood due to having limited 88
tools available to depict periodic arrangements of cubic membranes having a lattice 89
constant in the range of 50-1000 nm (Chong and Deng 2012) This makes electron 90
tomography (ET) an extremely valuable tool to study the non-lamellar membrane 91
configurations in cells Complimentary investigation to mathematically describe the 92
spatial arrangement as a triply periodic minimal surface and compare the 2D TEM 93
images with the 2D projections of these theoretical models has been quite useful 94
(Deng and Mieczkowski 1998) However the ET technique is still required to confirm 95
any cubic membrane configuration predicted by the above direct template matching 96
technique (Chong and Deng 2012) The connections of the cubic structures with the 97
adjacent tubular or lamellar arrangements and thus the spatial changes of the local 98
topology within the paracrystalline structure are difficult to properly predict An 99
alternative method applied to precisely determine PLB tubule dimensions as well as 100
the unit cell size is small angle X-ray scattering Small angle X-ray scattering 101
performed on isolated maize (Zea mays L) PLBs confirmed their paracrystalline 102
structure with the diamond cubic lattice being the most abundant type The unit cell 103
size was 78 nm (Selstam et al 2007) However the dimensions of isolated structures 104
and those in sliced tissue ie in situ performed by ET technique are difficult to 105
compare In similar studies ET was used to determine the cubic structure of the inner 106
mitochondrial membrane morphology in amoeba (C carolinens) upon starvation 107
(Deng et al 1999) 108
The paracrystalline nature of PLBs is thought to be due to the aggregation of a 109
complex containing protochlorophyllide (Pchlide) light-dependent protochlorophyllide 110
oxidoreductase (LPOR) and NADPH (Pchlide-LPOR-NADPH) (Ryberg and 111
5
Sundqvist 1982) The spatial structure can be clarified by studying the mechanism of 112
aggregation of such complexes and their interactions with the membrane lipids 113
(Mysliwa-Kurdziel et al 2013) Although PLB tubules contain more 114
monogalactosyldiacylglycerol than PTs that facilitate cubic phase structure formation 115
both PLBs and PTs are composed from the same types of lipids 116
monogalactosyldiacylglycerol digalactosyldiacylglycerol 117
sulfoquinovosyldiacylglycerol and phosphatidylglycerol Thus it appears that the lipid 118
composition is not a critical factor and that proteins appear to play an important role 119
(Selstam 1998) It is known that integral membrane proteins have a stabilizing effect 120
on the bilayer membrane even in the presence of purified non-bilayer lipids (Rietveld 121
et al 1987) This is probably due to a strong interaction between the hydrophobic 122
region passing through the membrane and the hydrophobic tails of the lipid molecule 123
(Taraschi et al 1982) Proteins are also considered to be important in vitro for 124
transforming non-bilayer lipids into the lamellar structure (Simidjiev et al 2000) The 125
role of the large pigment-protein complex Pchlide-LPOR in the formation of PLB 126
membranes with a cubic phase structure is probably due to the ability of this pigment-127
protein complex to form an oligomer and to anchor the LPOR protein into the 128
membrane (Selstam 1998) Moreover the proper composition of carotenoids in the 129
PLB membrane can play an important role in the formation and maintenance of its 130
paracrystalline structure (Park et al 2002) 131
PLBs contain two spectral forms of the Pchlide-LPOR complexes with absorption 132
maxima at approximately 640 nm and 650 nm (Selstam et al 2002) These two 133
Pchlide forms are photoconvertible An analysis of low temperature fluorescence 134
(77K) spectra has revealed one more type of Pchlide the nonphotoconvertible form 135
Pchlide 628-633 (Boumlddi et al 1998) The longer-wavelength forms are bound to 136
PLBs while this shorter-wavelength form unbound to LPOR is mainly found in PTs 137
In addition to LPOR PLBs contain enzymes of the chlorophyll (Chl) and carotenoid 138
biosynthesis pathways enzymes of the Calvin cycle and proteins involved in 139
photosynthetic light reactions (subunits of ATP synthase the oxygen-evolving 140
complex cytochrome b6f plastocyanin and ferrodoxin-NADPH oxidoreductase) and 141
also other proteins necessary during photomorphogenesis with the exception of the 142
core subunits and the antenna complexes of the two photosystems (Blomqvist et al 143
2008 Kleffmann et al 2007 von Zychlinski et al 2005 Adam et al 2011) 144
6
Upon illumination the photomorphogenic process called greening or de-etiolation 145
takes place and etioplasts develop into chloroplasts (Ryberg and Sundqvist 1982 146
Mostowska 1986a Von Wettstein et al 1995) During this process PLBs begin to 147
both disperse and transform and Pchlide is phototransformed to chlorophyllide 148
(Chlide) In angiosperms LPOR the major protein of PLB membranes is responsible 149
for the NADPH-dependent reduction of Pchlide to Chlide during illumination (Selstam 150
et al 2002) Recently it was shown using isolated wheat PLBs that the 151
photoreduction was followed by the disruption of the PLB lattice and the formation of 152
vesicles around the PLBs Data on isolated PLBs obtained by TEM was correlated 153
with atomic force microscopy results (Grzyb et al 2013) The release of Chlide from 154
a Chlide-LPOR complex leads to the degradation of the paracrystalline PLB 155
structure (Selstam et al 2002) 156
In the case of meristematic tissues chloroplast development proceeds mainly from a 157
proplastid (Charuvi et al 2012) In this case the thylakoid membrane is formed by 158
invaginations of the inner chloroplast envelope In the differentiated chloroplast 159
however the vesicle-based transport system dominates (Rast et al 2015) If a 160
proplastid develops into an etioplast in darkness but later the PLB transformation 161
takes place upon illumination the structural changes differ from those in meristematic 162
tissues In this case the transfer system for the newly synthetized lipids and proteins 163
into the forming thylakoids can be similar to that occuring during the direct 164
development of a proplastid into a chloroplast (Rast et al 2015) However it is still 165
not clear whether the degrading PLB transforms into thylakoids continuously or 166
through the formation of vesicles (Rosinski and Rosen 1972 Adam et al 2011 167
Grzyb et al 2013 Pribil et al 2014) 168
Eventually the tubular system of PLBs transforms into a linear system of lamellae 169
arranged in parallel to each other and the first grana appear as overlapping 170
thylakoids Finally fully developed chloroplasts have the internal membrane system 171
differentiated into stacks of appressed thylakoids and nonappressed regions with 172
grana margins as well as stroma lamellae linking grana together The structure of 173
mature thylakoids is determined by the lipid composition and arrangement of 174
chlorophyll-protein (CP) complexes hierarchically organized in supercomplexes and 175
megacomplexes and spatially segregated (Dekker and Boekema 2005 Kouřil et al 176
2012 Rumak et al 2012) The main component of the appressed regions is 177
7
photosystem II (PSII) forming together with extrinsic antennae light-harvesting 178
complex II (LHCII) supercomplex LHCII-PSII while the light-harvesting complex I-179
photosystem I supercomplex (LHCI-PSI) is localized in nonappressed thylakoids 180
(Danielsson et al 2004 2006) The organization composition dynamics and 181
structural rearrangements of the developed photosynthetic apparatus of higher plants 182
under changing light conditions have been examined with high resolution microscopic 183
techniques and by spectroscopic and biochemical methods (Nevo et al 2012 Janik 184
et al 2013 Garab 2014 Jensen and Leister 2014 Pribil et al 2014) 185
Spatial models of the thylakoid membrane architecture were created with the help of 186
electron tomography in the case of fully mature higher plant chloroplasts (Shimoni et 187
al 2005 Daum et al 2010 Austin and Staehelin 2011) and Chlamydomonas 188
(Chlamydomonas reinhardtii) chloroplasts (Engel et al 2015) The most probable 189
model of thylakoid membrane organization is based on the pioneering results of 190
Paolillo (Paolillo 1970) This is a modified helical model of chloroplast membranes 191
that shows an imperfect regularity (Mustaacuterdy et al 2008 Daum et al 2010 Daum 192
and Kuumlhlbrandt 2011) and a large variability in size of the junctional connections 193
between the grana and stroma thylakoids (Austin and Staehelin 2011) 194
Although the 3D view of the overall structure of chloroplasts has been already 195
presented based on confocal laser scanning microscopy (CLSM) (Rumak et al 196
2010 2012) and on 3D models of the thylakoid membrane architecture of mature 197
chloroplasts using electron tomography (Shimoni et al 2005 Daum et al 2010 198
Austin and Staehelin 2011) a 3D membrane visualization during the etioplast-to-199
chloroplast transition can give important developmental information Without this full 200
3D information it is not possible to understand the process of the transformation of 201
the membrane structure during the chloroplast biogenesis 202
In this paper we establish the spatial 3D structure of successive stages of runner 203
bean (Phaseolus coccineus L) chloroplast biogenesis by electron tomography and 204
by confocal laser scanning microscopy We have reconstructed the paracrystalline 205
structure and the membrane connections within the PLB and the gradual 206
transformation from a tubular arrangement to the linear one during the greening 207
process Moreover we present the early stages of grana formation especially the 208
character of the grana-stroma thylakoid connections We reconstruct the spatial 209
structure of the internal plastid membrane using electron tomography with the aid of 210
8
confocal laser scanning microscopy in later stages This enables visualization and 211
thus an understanding of the membrane connections during the key stages of 212
chloroplast biogenesis We correlate the 3D structure of PLBs and of the developing 213
bean thylakoid network with the formation of CP complexes 214
The results of our studies show that the transformation of PLBs consists of the 215
untwining of tubules from the PLB structure in a continuous process The tubular 216
structure of the prolamellar body transforms directly without dispersion into vesicles 217
into flat slats that eventually in a continuous way form grana We demonstrate that 218
grana membranes from the beginning of their formation associate with stroma 219
thylakoids in a helical way 220
221
RESULTS 222
Spatial Model of Chloroplast Biogenesis 223
To determine the spatial structure of successive stages of bean chloroplast 224
biogenesis during 3 daynight cycles both CLSM and ET were used Previous results 225
from ultrastructural analysis indicated that starting from 8 d-old etiolated plants 226
chloroplast development proceeds synchronously in all plastids (Rudowska et al 227
2012) 228
To establish the sequence of structural changes of the thylakoid network during 229
chloroplast biogenesis we followed the process of biogenesis step by step from the 230
paracrystalline structure of PLB to the stacked membranes observed in the 231
ultrastructure of bean chloroplasts For the electron tomography analysis seven 232
stages of plastid internal membrane arrangements were selected during the 233
photomorphogenesis as described in Methods (Supplemental Figure 1) 234
We focused on one hand on areas of membrane connections within tightly 235
organized tubular PLB structure and grana thylakoids and on the other hand on 236
areas of loosely organized structure with transforming PLBs with newly formed 237
thylakoids 3D modeling was performed from the stage of paracrystalline structure of 238
PLB to the stage of reorganization into first appressed thylakoids and formation of 239
more developed grana 240
9
Reconstruction of the very early stages of chloroplast development by CLSM was not 241
reliable due to the small dimensions and lack of red Chl fluorescence in early 242
developmental stages Because of this the images of the etioplast internal 243
membranes obtained with CLSM were not comparable with relevant structures on 244
electron micrographs Moreover the lipophilic dye (DiOC18(3)) that was used in these 245
early stages did not incorporate uniformly into the tight paracrystalline and 246
transforming PLB membranes causing imaging artefacts Therefore spatial models 247
obtained from CLSM were used only in the two latest analyzed stages of biogenesis 248
when the Chl autofluorescence of PSII was sufficiently stable and the dimensions of 249
chloroplasts were large enough 250
251
(Stage 10) Paracrystalline prolamellar body (PLB) 252
8 d-old etiolated bean leaves have etioplasts with characteristic paracrystalline 253
prolamellar bodies as was already shown by us and other researchers (Rudowska et 254
al 2012) Based on Gunning and Steer (1975) bean etioplast PLB is of a closed 255
type with hexagonal symmetry of the tubule arrangement The tetrahedrally branched 256
basic tubular units form a typical wurtzite (a zinc iron sulfide mineral) lattice For a 257
better comparison between the PLB structure and the theoretical model of a 258
hexagonal lattice we chose perpendicular sections of the closed-type PLB for ET 259
analysis (Supplemental Figure 2) 260
We found that the structure of the PLB was a regular tetrahedral arrangement of 261
tubular connections within the PLB (Figure 1) Such a composite tomographic image 262
stack was obtained by superimposing reconstructed parallel slices such as the one 263
shown in Figure 1A The volume of the PLB (Figure 1B) and isosurface visualization 264
of the 3D reconstruction of paracrystalline PLB membranes was generated (Figure 265
1C) with the help of Imaris microscopy image processing and analysis software In 266
Figures 1C and 1D the PLB volume together with the first layer of the PLB is visible 267
For better visualization of the PLB network we highlight a single unit (orange) of the 268
PLB together with the rendered volume (Figure 1E) An enlargement of the 269
isosurface of one unit is shown (Figure 1F) together with its side view (Figure 1G) In 270
Figure 1H the theoretical model created with the help of 3ds max software showing 271
the arrangement of inner plastid membranes within the prolamellar body is displayed 272
10
273
(Stage 11) Irregular prolamellar body 274
After 1 h of illumination the regularity and the symmetry of the PLB was lost The 275
structure of the PLB became irregular and PLB membranes became rearranged 276
(Figure 2) The 3D array of branched tubes in the PLB became dissociated and the 277
characteristic tetrahedral network was no longer visible and all units lost regular 278
connections with each other A composite tomographic slice image was obtained by 279
superimposing reconstructed parallel slices representing the spatial structure of an 280
irregular PLB and this composite image is shown in Figure 2A The volume (Figure 281
2B) and isosurface (Figures 2C to 2H) of an irregular PLB was rendered with the help 282
of Imaris software Already at this stage PLB membranes both within the PLB 283
(Figures 2E to 2H) and in its marginal regions (Figure 2D) had given rise to flat 284
stromal slats at the periphery of the PLB that were seen as porous PTs PTs were 285
tightly connected with the degrading PLB that were radially spreading from the PLB 286
margins (Figure 2C) In Figures 2C and 2D the isosurface of the irregular PLB 287
together with the outer layer of the PLB is visible Upon magnification the PTs 288
emerging from the degrading PLB are seen as flat slats (Figure 2D) For better 289
visualization of the transformation from tubular elements to slats a single unit of a 290
degrading PLB net (lime green) is shown from various directions (Figures 2E to 2H) 291
We strongly emphasize that electron tomography enabled the visualization of slat 292
arrangements during transformation and untwining of PLB nodes This was not 293
possible in traditional electron microscopy 294
295
(Stage 12) Remnants of PLB and numerous prothylakoids 296
After 2 h of illumination only remnants of the PLB were observed (Figure 3) A 297
composite tomographic slice image was obtained by superimposing reconstructed 298
parallel slices of remnants of the PLB and porous PTs connected with them (Figure 299
3A) The area of interest was drawn on every slice with the help of 3DMOD software 300
(Figure 3B the middle slice in the stack) We reconstructed a particular area of 301
chloroplast membranes focusing on connections between the remnants of the PLB 302
and the PTs This model was superimposed on a TEM image for better visualization 303
of the region of interest (blue) (Figures 3C and 3D) In Figures 3E to 3G slat-like 304
11
images of PTs are presented from different angles From these models we could 305
observe that the membranes that were remnants of the PLB had a continuous 306
character as opposed to the porous PT membranes that were tightly connected with 307
the former (Figures 3E to 3G) Both types of membrane were slat-like and not tubule-308
like structures At this stage of chloroplast biogenesis the inner membranes were 309
arranged in parallel to the long chloroplast axis 310
311
(Stage 14) Parallel prothylakoids 312
After 4 h of illumination there were no more remnants of PLBs in the bean 313
chloroplasts (Figure 4) A composite tomographic slice image was obtained by 314
superimposing reconstructed parallel slices of chloroplasts at this stage of 315
development (Figure 4A) A selected area of membranes was drawn with the help of 316
3DMOD software (Figure 4B middle slice from the stack) A model of the area of 317
interest was superimposed on a TEM image for better visualization (purple) (Figures 318
4C and 4D) In Figures 4E to 4G slat-like models of porous PTs are shown after 319
rotation and presented from different angles Such models enabled the visualization 320
of the parallel arrangement of PTs and the local connections between them The PTs 321
had a slat-like and porous character and some of them had split in a dichotomous 322
manner (Figures 4E to 4G) 323
324
(Stage 18) First stacked membranes 325
After 8 h of illumination the first stacked membranes were observed (Figure 5) A 326
composite tomographic slice image was obtained in a similar way as before (Figure 327
5A) Interesting areas of thylakoid membranes especially of stacked membranes and 328
their connections to unstacked ones were drawn using 3DMOD software (Figure 5B 329
middle slice from the stack) A model of the area of interest was superimposed on the 330
TEM image (Figures 5C and 5D) In Figures 5E to 5H models of the first stacked 331
membranes are shown after magnification and presented from different angles 332
These models revealed that the appressed thylakoids (light yellow) were no longer 333
porous but had continuous membranes in the stacked region From our constructed 334
model we learned that the PTs (yellow) remained still porous although to a lesser 335
extent than at earlier stages In this model each stacked membrane was connected 336
12
to a single split PT This dichotomous splitting existed only locally where a PT joined 337
with both the upper and lower stacked membrane The PT membrane connected with 338
the stacked region not in parallel but at an angle in the range of 18 to 33deg 339
340
(Stage 20) Small grana 341
At the beginning of the second day of the experiment (Figure 6) small grana stacks 342
were observed (stage 20) A composite tomographic slice image was obtained in a 343
similar way as for the other stages of biogenesis (Figure 6A) Grana thylakoids (GTs) 344
and stroma thylakoids (STs) connected with them were drawn using the 3DMOD 345
software (Figure 6B middle slice from the stack) A small grana model was 346
superimposed on the TEM image for a better visualization of the region of interest 347
(Figures 6C and 6D) The model shows GTs (light green) arranged in parallel and no-348
longer-porous STs (green) connected with them (Figure 6E) In Figures 6F to 6I the 349
models of GTs and STs are shown from different angles Every modelled ST was 350
connected with two adjacent GTs (Figures 6F and 6G) The STs were connected with 351
the stacked region at an angle of approximately 20deg 352
As mentioned previously a CLSM study was performed for the two latest stages of 353
chloroplast biogenesis The density of the red Chl fluorescence spots in a CLSM 354
image showed the distribution of the appressed thylakoids (grana) in the chloroplast 355
(Supplemental Figure 3) There was no visible regularity of the appressed thylakoid 356
distribution (Supplemental Figure 3A) that correlated with the TEM pictures Also 3D 357
models of the computer generated isosurface of Chl fluorescence (Supplemental 358
Figures 3B to 3D) confirmed the lack of regularity of grana location within a 359
chloroplast The red fluorescence originated from the LHCII-PSII supercomplexes 360
dimers and monomers and also from LHCII trimers that were not bound and 361
localized in grana (Mehta et al 1999) Selective images of PSI and PSII in plant 362
chloroplasts in situ have shown that they are spatially separated from each other 363
however the majority of the fluorescence signals originating from PSI overlap with 364
those from PSII (Hasegawa et al 2010) Thus in the case of CLSM images of bean 365
chloroplasts the LHCI-PSI complexes can be located both in red and dark areas but 366
the LHCII-PSII and LHCII trimers are located in red fluorescence regions only 367
368
13
(Stage 33) More developed grana 369
During the third day (stage 33) chloroplasts with grana more developed than in the 370
previous stage containing numerous thylakoids were observed (Figure 7) A 371
composite tomographic slice image was obtained as in the previously analyzed 372
stages (Figure 7A) The region of interest was drawn using the 3DMOD software 373
(Figure 7B middle slice from the stack) A model of the granum (light navy) with 374
connected STs (navy) was superimposed on the TEM image (Figures 7C and 7D) In 375
Figures 7E to 7I the model is shown from different angles to visualize direct 376
connections of STs with GTs The complexity of these connections can be observed 377
Some STs were associated with two neighboring GTs as in the previous stage and 378
were connected at an angle of approximately 18deg (Fig 7E and 7F) ST can also split 379
in a dichotomous manner and connect with both the adjacent GT and the next GT in 380
the other slice (left bottom ST Figures 7F and 7H) Additionally we saw that the ST in 381
the area of our model could connect with only one GT as was observed at the top 382
and bottom of the granum (Figure 7G) This shows that the junctional slits created by 383
the connections between GTs and STs can be of different widths as was also 384
reported by Austin and Staehelin for the thylakoid network of well-developed 385
chloroplasts of mature plants (Austin and Staehelin 2011) 386
For this stage the CLSM analysis was also performed The distribution of Chl 387
autofluorescence (Supplemental Figure 4) visible in CLSM changed drastically in 388
comparison to the earlier stage of grana formation Red spots corresponding to grana 389
were uniformly distributed within the chloroplast (Supplemental Figure 4A) 3D 390
models of the computer generated isosurface of Chl fluorescence confirmed the 391
regular distribution of grana that is characteristic of a mature chloroplast (Rumak et 392
al 2010) (Figures 4B to 4D) However the size of chloroplast at this stage of 393
biogenesis was much smaller (approximately 3 μm) than the 6 μm chloroplasts found 394
in mature plants 395
Based on the TEM sections of numerous developmental stages and also on the 396
reconstruction of the membrane transformation in 3D during the 7 stages of 397
chloroplast biogenesis we proposed a 2D theoretical model (Figure 8) of the 398
membrane changes The proposed theoretical model of membrane rearrangements 399
taken together with the 3D models allow us to create a dynamic model of chloroplast 400
development which is presented as a movie (Supplemental Movie 1) 401
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
Parsed CitationsAbdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) High salt stress induces swollen prothylakoids indark-grown wheat and alters both prolamellar body transformation and reformation after irradiation J Exp Bot 58 2553-2564
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ Biophotonics International 11 36-42Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of thylakoid networks in angiosperms knowns andunknowns Plant Mol Biol 76 221-234
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend beyond the Flatland of cell membraneorganization J Cell Biol 173 839-844
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic membranes the missing dimension of cellmembrane organization Int Rev Cell Mol Biol 274 275-342
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the structure and function of photosystem II in higherplant thylakoid membranes the grana enigma Photosynth Res 98 575-587
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
2
ABSTRACT 24
25
Chloroplast biogenesis is a complex process that is integrated with plant 26
development leading to fully differentiated and functionally mature plastids In this 27
work we used electron tomography and confocal microscopy to reconstruct the 28
process of structural membrane transformation during the etioplast-to-chloroplast 29
transition in runner bean (Phaseolus coccineus L) During chloroplast development 30
the regular tubular network of paracrystalline prolamellar bodies (PLBs) and the 31
flattened porous membranes of prothylakoids (PTs) develop into the chloroplast 32
thylakoids Three-dimensional (3D) reconstruction is required to provide us with a 33
more complete understanding of this transformation We provide spatial models of 34
the bean chloroplast biogenesis that allow such reconstruction of the internal 35
membranes of the developing chloroplast and visualize the transformation from the 36
tubular arrangement to the linear system of parallel lamellae We prove that the 37
tubular structure of the PLB transforms directly to flat slats without dispersion to 38
vesicles We demonstrate that the granastroma thylakoid connections have a helical 39
character starting from the early stages of appressed membrane formation 40
Moreover we point out the importance of particular chlorophyll-protein (CP) complex 41
components in the membrane stacking during the biogenesis The main stages of 42
chloroplast internal membrane biogenesis are presented in a movie that shows the 43
time development of the chloroplast biogenesis as a dynamic model of this process 44
45
3
INTRODUCTION 46
47
Chloroplast biogenesis is a complex process that is essential for plant ontogenesis It 48
involves changes in gene expression together with the transcriptional and 49
translational control of both nuclear and plastid genes These genes can be regulated 50
by anterograde and retrograde signals the synthesis of necessary lipids and 51
pigments the import and routing of the nucleus-encoded proteins into plastids 52
protein-lipid interactions the insertion of proteins into the plastid membranes and the 53
assembly into functional complexes (eg Vothknecht and Westhoff 2001 Baena-54
Gonzaacutelez and Aro 2002 Kota et al 2002 Stern et al 2004 Loacutepez-Juez 2007 55
Waters and Langdale 2009 Solymosi and Schoefs 2010 Adam et al 2011 56
Pogson and Albrecht 2011 Ling et al 2012 Jarvis and Loacutepez-Juez 2013 Lyska et 57
al 2013 Belcher et al 2015 Boumlrner et al 2015 DallrsquoOsto et al 2015 Ling and 58
Jarvis 2015 Rast et al 2015 Sun and Zerges 2015 Yang et al 2015) Chloroplast 59
biogenesis is highly integrated with cell and plant development especially with 60
photomorphogenesis (Pogson et al 2015) and is controlled by cellular and 61
organismal regulatory mechanisms such as the ubiquitin-proteasome system (Jarvis 62
and Loacutepez-Juez 2013) Although biogenesis of chloroplasts has been a subject of 63
investigations for many years the correlation of simultaneous changes at the 64
structural biochemical and functional level was described only recently when time 65
dependent models of chloroplast biogenesis for bean (Phaseolus vulgaris L) and 66
pea (Pisum sativum L) were described (Rudowska et al 2012) 67
The development of chloroplasts up to the stage of etioplasts often takes place when 68
seedling growth proceeds without light Etioplasts contain characteristic structures 69
known as prolamellar bodies (PLBs) that have tubules joined together in a regular 70
network and have a special paracrystalline symmetry Together with prothylakoids 71
(PTs) mdash flattened porous membranes PLBs are precursors of the chloroplast 72
thylakoid membranes PLBs are observed under natural growing conditions when the 73
first stages of seed germination proceed under the ground and are not artificial 74
laboratory phenomena (Solymosi et al 2007 Solymosi and Schoefs 2010 Vitaacutenyi 75
et al 2013) The paracrystalline structure of PLBs can differ depending on the 76
species and the conditions of PLB crystallization All types of paracrystalline 77
arrangements have an exceptionally high surface-to-volume ratio (Gunning 2001) 78
4
Although the formation of etioplasts in darkness which have a characteristic 79
paracrystalline PLB and their transformation upon exposure to light has been 80
documented since the 1960rsquos (eg Gunning 1965 2001 Mostowska 1986a 1986b 81
Solymosi and Schoefs 2010) but the spatial arrangement of these changes is still not 82
known 83
Despite of 60 years of studies the true organization of the paracrystalline 84
membranes in three dimensions (3D) have remained unclear Cubic membranes 85
other than PLBs were described in different biological systems especially in stressed 86
conditions or virally infected cells (Almsherqi et al 2006 2009 Deng et al 2010) 87
However this widespread phenomenon is poorly understood due to having limited 88
tools available to depict periodic arrangements of cubic membranes having a lattice 89
constant in the range of 50-1000 nm (Chong and Deng 2012) This makes electron 90
tomography (ET) an extremely valuable tool to study the non-lamellar membrane 91
configurations in cells Complimentary investigation to mathematically describe the 92
spatial arrangement as a triply periodic minimal surface and compare the 2D TEM 93
images with the 2D projections of these theoretical models has been quite useful 94
(Deng and Mieczkowski 1998) However the ET technique is still required to confirm 95
any cubic membrane configuration predicted by the above direct template matching 96
technique (Chong and Deng 2012) The connections of the cubic structures with the 97
adjacent tubular or lamellar arrangements and thus the spatial changes of the local 98
topology within the paracrystalline structure are difficult to properly predict An 99
alternative method applied to precisely determine PLB tubule dimensions as well as 100
the unit cell size is small angle X-ray scattering Small angle X-ray scattering 101
performed on isolated maize (Zea mays L) PLBs confirmed their paracrystalline 102
structure with the diamond cubic lattice being the most abundant type The unit cell 103
size was 78 nm (Selstam et al 2007) However the dimensions of isolated structures 104
and those in sliced tissue ie in situ performed by ET technique are difficult to 105
compare In similar studies ET was used to determine the cubic structure of the inner 106
mitochondrial membrane morphology in amoeba (C carolinens) upon starvation 107
(Deng et al 1999) 108
The paracrystalline nature of PLBs is thought to be due to the aggregation of a 109
complex containing protochlorophyllide (Pchlide) light-dependent protochlorophyllide 110
oxidoreductase (LPOR) and NADPH (Pchlide-LPOR-NADPH) (Ryberg and 111
5
Sundqvist 1982) The spatial structure can be clarified by studying the mechanism of 112
aggregation of such complexes and their interactions with the membrane lipids 113
(Mysliwa-Kurdziel et al 2013) Although PLB tubules contain more 114
monogalactosyldiacylglycerol than PTs that facilitate cubic phase structure formation 115
both PLBs and PTs are composed from the same types of lipids 116
monogalactosyldiacylglycerol digalactosyldiacylglycerol 117
sulfoquinovosyldiacylglycerol and phosphatidylglycerol Thus it appears that the lipid 118
composition is not a critical factor and that proteins appear to play an important role 119
(Selstam 1998) It is known that integral membrane proteins have a stabilizing effect 120
on the bilayer membrane even in the presence of purified non-bilayer lipids (Rietveld 121
et al 1987) This is probably due to a strong interaction between the hydrophobic 122
region passing through the membrane and the hydrophobic tails of the lipid molecule 123
(Taraschi et al 1982) Proteins are also considered to be important in vitro for 124
transforming non-bilayer lipids into the lamellar structure (Simidjiev et al 2000) The 125
role of the large pigment-protein complex Pchlide-LPOR in the formation of PLB 126
membranes with a cubic phase structure is probably due to the ability of this pigment-127
protein complex to form an oligomer and to anchor the LPOR protein into the 128
membrane (Selstam 1998) Moreover the proper composition of carotenoids in the 129
PLB membrane can play an important role in the formation and maintenance of its 130
paracrystalline structure (Park et al 2002) 131
PLBs contain two spectral forms of the Pchlide-LPOR complexes with absorption 132
maxima at approximately 640 nm and 650 nm (Selstam et al 2002) These two 133
Pchlide forms are photoconvertible An analysis of low temperature fluorescence 134
(77K) spectra has revealed one more type of Pchlide the nonphotoconvertible form 135
Pchlide 628-633 (Boumlddi et al 1998) The longer-wavelength forms are bound to 136
PLBs while this shorter-wavelength form unbound to LPOR is mainly found in PTs 137
In addition to LPOR PLBs contain enzymes of the chlorophyll (Chl) and carotenoid 138
biosynthesis pathways enzymes of the Calvin cycle and proteins involved in 139
photosynthetic light reactions (subunits of ATP synthase the oxygen-evolving 140
complex cytochrome b6f plastocyanin and ferrodoxin-NADPH oxidoreductase) and 141
also other proteins necessary during photomorphogenesis with the exception of the 142
core subunits and the antenna complexes of the two photosystems (Blomqvist et al 143
2008 Kleffmann et al 2007 von Zychlinski et al 2005 Adam et al 2011) 144
6
Upon illumination the photomorphogenic process called greening or de-etiolation 145
takes place and etioplasts develop into chloroplasts (Ryberg and Sundqvist 1982 146
Mostowska 1986a Von Wettstein et al 1995) During this process PLBs begin to 147
both disperse and transform and Pchlide is phototransformed to chlorophyllide 148
(Chlide) In angiosperms LPOR the major protein of PLB membranes is responsible 149
for the NADPH-dependent reduction of Pchlide to Chlide during illumination (Selstam 150
et al 2002) Recently it was shown using isolated wheat PLBs that the 151
photoreduction was followed by the disruption of the PLB lattice and the formation of 152
vesicles around the PLBs Data on isolated PLBs obtained by TEM was correlated 153
with atomic force microscopy results (Grzyb et al 2013) The release of Chlide from 154
a Chlide-LPOR complex leads to the degradation of the paracrystalline PLB 155
structure (Selstam et al 2002) 156
In the case of meristematic tissues chloroplast development proceeds mainly from a 157
proplastid (Charuvi et al 2012) In this case the thylakoid membrane is formed by 158
invaginations of the inner chloroplast envelope In the differentiated chloroplast 159
however the vesicle-based transport system dominates (Rast et al 2015) If a 160
proplastid develops into an etioplast in darkness but later the PLB transformation 161
takes place upon illumination the structural changes differ from those in meristematic 162
tissues In this case the transfer system for the newly synthetized lipids and proteins 163
into the forming thylakoids can be similar to that occuring during the direct 164
development of a proplastid into a chloroplast (Rast et al 2015) However it is still 165
not clear whether the degrading PLB transforms into thylakoids continuously or 166
through the formation of vesicles (Rosinski and Rosen 1972 Adam et al 2011 167
Grzyb et al 2013 Pribil et al 2014) 168
Eventually the tubular system of PLBs transforms into a linear system of lamellae 169
arranged in parallel to each other and the first grana appear as overlapping 170
thylakoids Finally fully developed chloroplasts have the internal membrane system 171
differentiated into stacks of appressed thylakoids and nonappressed regions with 172
grana margins as well as stroma lamellae linking grana together The structure of 173
mature thylakoids is determined by the lipid composition and arrangement of 174
chlorophyll-protein (CP) complexes hierarchically organized in supercomplexes and 175
megacomplexes and spatially segregated (Dekker and Boekema 2005 Kouřil et al 176
2012 Rumak et al 2012) The main component of the appressed regions is 177
7
photosystem II (PSII) forming together with extrinsic antennae light-harvesting 178
complex II (LHCII) supercomplex LHCII-PSII while the light-harvesting complex I-179
photosystem I supercomplex (LHCI-PSI) is localized in nonappressed thylakoids 180
(Danielsson et al 2004 2006) The organization composition dynamics and 181
structural rearrangements of the developed photosynthetic apparatus of higher plants 182
under changing light conditions have been examined with high resolution microscopic 183
techniques and by spectroscopic and biochemical methods (Nevo et al 2012 Janik 184
et al 2013 Garab 2014 Jensen and Leister 2014 Pribil et al 2014) 185
Spatial models of the thylakoid membrane architecture were created with the help of 186
electron tomography in the case of fully mature higher plant chloroplasts (Shimoni et 187
al 2005 Daum et al 2010 Austin and Staehelin 2011) and Chlamydomonas 188
(Chlamydomonas reinhardtii) chloroplasts (Engel et al 2015) The most probable 189
model of thylakoid membrane organization is based on the pioneering results of 190
Paolillo (Paolillo 1970) This is a modified helical model of chloroplast membranes 191
that shows an imperfect regularity (Mustaacuterdy et al 2008 Daum et al 2010 Daum 192
and Kuumlhlbrandt 2011) and a large variability in size of the junctional connections 193
between the grana and stroma thylakoids (Austin and Staehelin 2011) 194
Although the 3D view of the overall structure of chloroplasts has been already 195
presented based on confocal laser scanning microscopy (CLSM) (Rumak et al 196
2010 2012) and on 3D models of the thylakoid membrane architecture of mature 197
chloroplasts using electron tomography (Shimoni et al 2005 Daum et al 2010 198
Austin and Staehelin 2011) a 3D membrane visualization during the etioplast-to-199
chloroplast transition can give important developmental information Without this full 200
3D information it is not possible to understand the process of the transformation of 201
the membrane structure during the chloroplast biogenesis 202
In this paper we establish the spatial 3D structure of successive stages of runner 203
bean (Phaseolus coccineus L) chloroplast biogenesis by electron tomography and 204
by confocal laser scanning microscopy We have reconstructed the paracrystalline 205
structure and the membrane connections within the PLB and the gradual 206
transformation from a tubular arrangement to the linear one during the greening 207
process Moreover we present the early stages of grana formation especially the 208
character of the grana-stroma thylakoid connections We reconstruct the spatial 209
structure of the internal plastid membrane using electron tomography with the aid of 210
8
confocal laser scanning microscopy in later stages This enables visualization and 211
thus an understanding of the membrane connections during the key stages of 212
chloroplast biogenesis We correlate the 3D structure of PLBs and of the developing 213
bean thylakoid network with the formation of CP complexes 214
The results of our studies show that the transformation of PLBs consists of the 215
untwining of tubules from the PLB structure in a continuous process The tubular 216
structure of the prolamellar body transforms directly without dispersion into vesicles 217
into flat slats that eventually in a continuous way form grana We demonstrate that 218
grana membranes from the beginning of their formation associate with stroma 219
thylakoids in a helical way 220
221
RESULTS 222
Spatial Model of Chloroplast Biogenesis 223
To determine the spatial structure of successive stages of bean chloroplast 224
biogenesis during 3 daynight cycles both CLSM and ET were used Previous results 225
from ultrastructural analysis indicated that starting from 8 d-old etiolated plants 226
chloroplast development proceeds synchronously in all plastids (Rudowska et al 227
2012) 228
To establish the sequence of structural changes of the thylakoid network during 229
chloroplast biogenesis we followed the process of biogenesis step by step from the 230
paracrystalline structure of PLB to the stacked membranes observed in the 231
ultrastructure of bean chloroplasts For the electron tomography analysis seven 232
stages of plastid internal membrane arrangements were selected during the 233
photomorphogenesis as described in Methods (Supplemental Figure 1) 234
We focused on one hand on areas of membrane connections within tightly 235
organized tubular PLB structure and grana thylakoids and on the other hand on 236
areas of loosely organized structure with transforming PLBs with newly formed 237
thylakoids 3D modeling was performed from the stage of paracrystalline structure of 238
PLB to the stage of reorganization into first appressed thylakoids and formation of 239
more developed grana 240
9
Reconstruction of the very early stages of chloroplast development by CLSM was not 241
reliable due to the small dimensions and lack of red Chl fluorescence in early 242
developmental stages Because of this the images of the etioplast internal 243
membranes obtained with CLSM were not comparable with relevant structures on 244
electron micrographs Moreover the lipophilic dye (DiOC18(3)) that was used in these 245
early stages did not incorporate uniformly into the tight paracrystalline and 246
transforming PLB membranes causing imaging artefacts Therefore spatial models 247
obtained from CLSM were used only in the two latest analyzed stages of biogenesis 248
when the Chl autofluorescence of PSII was sufficiently stable and the dimensions of 249
chloroplasts were large enough 250
251
(Stage 10) Paracrystalline prolamellar body (PLB) 252
8 d-old etiolated bean leaves have etioplasts with characteristic paracrystalline 253
prolamellar bodies as was already shown by us and other researchers (Rudowska et 254
al 2012) Based on Gunning and Steer (1975) bean etioplast PLB is of a closed 255
type with hexagonal symmetry of the tubule arrangement The tetrahedrally branched 256
basic tubular units form a typical wurtzite (a zinc iron sulfide mineral) lattice For a 257
better comparison between the PLB structure and the theoretical model of a 258
hexagonal lattice we chose perpendicular sections of the closed-type PLB for ET 259
analysis (Supplemental Figure 2) 260
We found that the structure of the PLB was a regular tetrahedral arrangement of 261
tubular connections within the PLB (Figure 1) Such a composite tomographic image 262
stack was obtained by superimposing reconstructed parallel slices such as the one 263
shown in Figure 1A The volume of the PLB (Figure 1B) and isosurface visualization 264
of the 3D reconstruction of paracrystalline PLB membranes was generated (Figure 265
1C) with the help of Imaris microscopy image processing and analysis software In 266
Figures 1C and 1D the PLB volume together with the first layer of the PLB is visible 267
For better visualization of the PLB network we highlight a single unit (orange) of the 268
PLB together with the rendered volume (Figure 1E) An enlargement of the 269
isosurface of one unit is shown (Figure 1F) together with its side view (Figure 1G) In 270
Figure 1H the theoretical model created with the help of 3ds max software showing 271
the arrangement of inner plastid membranes within the prolamellar body is displayed 272
10
273
(Stage 11) Irregular prolamellar body 274
After 1 h of illumination the regularity and the symmetry of the PLB was lost The 275
structure of the PLB became irregular and PLB membranes became rearranged 276
(Figure 2) The 3D array of branched tubes in the PLB became dissociated and the 277
characteristic tetrahedral network was no longer visible and all units lost regular 278
connections with each other A composite tomographic slice image was obtained by 279
superimposing reconstructed parallel slices representing the spatial structure of an 280
irregular PLB and this composite image is shown in Figure 2A The volume (Figure 281
2B) and isosurface (Figures 2C to 2H) of an irregular PLB was rendered with the help 282
of Imaris software Already at this stage PLB membranes both within the PLB 283
(Figures 2E to 2H) and in its marginal regions (Figure 2D) had given rise to flat 284
stromal slats at the periphery of the PLB that were seen as porous PTs PTs were 285
tightly connected with the degrading PLB that were radially spreading from the PLB 286
margins (Figure 2C) In Figures 2C and 2D the isosurface of the irregular PLB 287
together with the outer layer of the PLB is visible Upon magnification the PTs 288
emerging from the degrading PLB are seen as flat slats (Figure 2D) For better 289
visualization of the transformation from tubular elements to slats a single unit of a 290
degrading PLB net (lime green) is shown from various directions (Figures 2E to 2H) 291
We strongly emphasize that electron tomography enabled the visualization of slat 292
arrangements during transformation and untwining of PLB nodes This was not 293
possible in traditional electron microscopy 294
295
(Stage 12) Remnants of PLB and numerous prothylakoids 296
After 2 h of illumination only remnants of the PLB were observed (Figure 3) A 297
composite tomographic slice image was obtained by superimposing reconstructed 298
parallel slices of remnants of the PLB and porous PTs connected with them (Figure 299
3A) The area of interest was drawn on every slice with the help of 3DMOD software 300
(Figure 3B the middle slice in the stack) We reconstructed a particular area of 301
chloroplast membranes focusing on connections between the remnants of the PLB 302
and the PTs This model was superimposed on a TEM image for better visualization 303
of the region of interest (blue) (Figures 3C and 3D) In Figures 3E to 3G slat-like 304
11
images of PTs are presented from different angles From these models we could 305
observe that the membranes that were remnants of the PLB had a continuous 306
character as opposed to the porous PT membranes that were tightly connected with 307
the former (Figures 3E to 3G) Both types of membrane were slat-like and not tubule-308
like structures At this stage of chloroplast biogenesis the inner membranes were 309
arranged in parallel to the long chloroplast axis 310
311
(Stage 14) Parallel prothylakoids 312
After 4 h of illumination there were no more remnants of PLBs in the bean 313
chloroplasts (Figure 4) A composite tomographic slice image was obtained by 314
superimposing reconstructed parallel slices of chloroplasts at this stage of 315
development (Figure 4A) A selected area of membranes was drawn with the help of 316
3DMOD software (Figure 4B middle slice from the stack) A model of the area of 317
interest was superimposed on a TEM image for better visualization (purple) (Figures 318
4C and 4D) In Figures 4E to 4G slat-like models of porous PTs are shown after 319
rotation and presented from different angles Such models enabled the visualization 320
of the parallel arrangement of PTs and the local connections between them The PTs 321
had a slat-like and porous character and some of them had split in a dichotomous 322
manner (Figures 4E to 4G) 323
324
(Stage 18) First stacked membranes 325
After 8 h of illumination the first stacked membranes were observed (Figure 5) A 326
composite tomographic slice image was obtained in a similar way as before (Figure 327
5A) Interesting areas of thylakoid membranes especially of stacked membranes and 328
their connections to unstacked ones were drawn using 3DMOD software (Figure 5B 329
middle slice from the stack) A model of the area of interest was superimposed on the 330
TEM image (Figures 5C and 5D) In Figures 5E to 5H models of the first stacked 331
membranes are shown after magnification and presented from different angles 332
These models revealed that the appressed thylakoids (light yellow) were no longer 333
porous but had continuous membranes in the stacked region From our constructed 334
model we learned that the PTs (yellow) remained still porous although to a lesser 335
extent than at earlier stages In this model each stacked membrane was connected 336
12
to a single split PT This dichotomous splitting existed only locally where a PT joined 337
with both the upper and lower stacked membrane The PT membrane connected with 338
the stacked region not in parallel but at an angle in the range of 18 to 33deg 339
340
(Stage 20) Small grana 341
At the beginning of the second day of the experiment (Figure 6) small grana stacks 342
were observed (stage 20) A composite tomographic slice image was obtained in a 343
similar way as for the other stages of biogenesis (Figure 6A) Grana thylakoids (GTs) 344
and stroma thylakoids (STs) connected with them were drawn using the 3DMOD 345
software (Figure 6B middle slice from the stack) A small grana model was 346
superimposed on the TEM image for a better visualization of the region of interest 347
(Figures 6C and 6D) The model shows GTs (light green) arranged in parallel and no-348
longer-porous STs (green) connected with them (Figure 6E) In Figures 6F to 6I the 349
models of GTs and STs are shown from different angles Every modelled ST was 350
connected with two adjacent GTs (Figures 6F and 6G) The STs were connected with 351
the stacked region at an angle of approximately 20deg 352
As mentioned previously a CLSM study was performed for the two latest stages of 353
chloroplast biogenesis The density of the red Chl fluorescence spots in a CLSM 354
image showed the distribution of the appressed thylakoids (grana) in the chloroplast 355
(Supplemental Figure 3) There was no visible regularity of the appressed thylakoid 356
distribution (Supplemental Figure 3A) that correlated with the TEM pictures Also 3D 357
models of the computer generated isosurface of Chl fluorescence (Supplemental 358
Figures 3B to 3D) confirmed the lack of regularity of grana location within a 359
chloroplast The red fluorescence originated from the LHCII-PSII supercomplexes 360
dimers and monomers and also from LHCII trimers that were not bound and 361
localized in grana (Mehta et al 1999) Selective images of PSI and PSII in plant 362
chloroplasts in situ have shown that they are spatially separated from each other 363
however the majority of the fluorescence signals originating from PSI overlap with 364
those from PSII (Hasegawa et al 2010) Thus in the case of CLSM images of bean 365
chloroplasts the LHCI-PSI complexes can be located both in red and dark areas but 366
the LHCII-PSII and LHCII trimers are located in red fluorescence regions only 367
368
13
(Stage 33) More developed grana 369
During the third day (stage 33) chloroplasts with grana more developed than in the 370
previous stage containing numerous thylakoids were observed (Figure 7) A 371
composite tomographic slice image was obtained as in the previously analyzed 372
stages (Figure 7A) The region of interest was drawn using the 3DMOD software 373
(Figure 7B middle slice from the stack) A model of the granum (light navy) with 374
connected STs (navy) was superimposed on the TEM image (Figures 7C and 7D) In 375
Figures 7E to 7I the model is shown from different angles to visualize direct 376
connections of STs with GTs The complexity of these connections can be observed 377
Some STs were associated with two neighboring GTs as in the previous stage and 378
were connected at an angle of approximately 18deg (Fig 7E and 7F) ST can also split 379
in a dichotomous manner and connect with both the adjacent GT and the next GT in 380
the other slice (left bottom ST Figures 7F and 7H) Additionally we saw that the ST in 381
the area of our model could connect with only one GT as was observed at the top 382
and bottom of the granum (Figure 7G) This shows that the junctional slits created by 383
the connections between GTs and STs can be of different widths as was also 384
reported by Austin and Staehelin for the thylakoid network of well-developed 385
chloroplasts of mature plants (Austin and Staehelin 2011) 386
For this stage the CLSM analysis was also performed The distribution of Chl 387
autofluorescence (Supplemental Figure 4) visible in CLSM changed drastically in 388
comparison to the earlier stage of grana formation Red spots corresponding to grana 389
were uniformly distributed within the chloroplast (Supplemental Figure 4A) 3D 390
models of the computer generated isosurface of Chl fluorescence confirmed the 391
regular distribution of grana that is characteristic of a mature chloroplast (Rumak et 392
al 2010) (Figures 4B to 4D) However the size of chloroplast at this stage of 393
biogenesis was much smaller (approximately 3 μm) than the 6 μm chloroplasts found 394
in mature plants 395
Based on the TEM sections of numerous developmental stages and also on the 396
reconstruction of the membrane transformation in 3D during the 7 stages of 397
chloroplast biogenesis we proposed a 2D theoretical model (Figure 8) of the 398
membrane changes The proposed theoretical model of membrane rearrangements 399
taken together with the 3D models allow us to create a dynamic model of chloroplast 400
development which is presented as a movie (Supplemental Movie 1) 401
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
Parsed CitationsAbdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) High salt stress induces swollen prothylakoids indark-grown wheat and alters both prolamellar body transformation and reformation after irradiation J Exp Bot 58 2553-2564
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ Biophotonics International 11 36-42Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of thylakoid networks in angiosperms knowns andunknowns Plant Mol Biol 76 221-234
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend beyond the Flatland of cell membraneorganization J Cell Biol 173 839-844
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic membranes the missing dimension of cellmembrane organization Int Rev Cell Mol Biol 274 275-342
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the structure and function of photosystem II in higherplant thylakoid membranes the grana enigma Photosynth Res 98 575-587
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R and Dekker JP (2005) Origin of the F685 andF695 fluorescence in photosystem II Photosynth Res 84 173-180
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants asdetermined by electron tomography Plant Physiol 155 1601-1611
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of photosystem II units Philos Trans R Soc LondB Biol Sci 357 1451-1459 discussion 1459-1460
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale genetic analysis of chloroplast biogenesis in maizeBiochim Biophys Acta 1847 1004-1016
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals theirsignificance in chloroplast development Photosynth Res 96 37-50
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The two spectroscopically different short wavelengthprotochlorophyllide forms in pea epicotyls are both monomeric Biochim Biophys Acta 1365 531-540
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast RNA polymerases Role in chloroplast biogenesisBiochim Biophys Acta 1847 761-769
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR (2010) Energy transfer processes in the isolated
core antenna complexes CP43 and CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606-1616Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain and loss of photosynthetic membranes duringplastid differentiation in the shoot apex of Arabidopsis Plant Cell 24 1143-1157
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar to cubic membrane transition as investigatedby electron microscopy Methods Cell Biol 108 319-343
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of thylakoid membranes in higher plant chloroplaststhe physicochemical forces at work and the functional consequences that ensue Photochem Photobiol Sci Off J EurPhotochem Assoc Eur Soc Photobiol 4 1081-1090
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
DallOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting proteins Biochim Biophys Acta 1847 861-871Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) Quantification of photosystem I and II in different parts of thethylakoid membrane from spinach Biochim Biophys Acta 1608 53-61
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-M and Mamedov F (2006) Dimeric andmonomeric organization of photosystem II Distribution of five distinct complexes in the different domains of the thylakoidmembrane J Biol Chem 281 14241-14249
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid membranes J Exp Bot 62 2393-2402Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) Arrangement of photosystem II and ATP synthase inchloroplast membranes of spinach and pea Plant Cell 22 1299-1312
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants BiochimBiophys Acta 1706 12-39
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses subvert cholesterol homeostasis to induce host cubicmembranes Trends Cell Biol 20 371-379
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane structure in the mitochondria of amoebaeChaos carolinensis Protoplasma 20316-25
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA (1999) Cubic membrane structure in amoeba(Chaos carolinensis) mitochondria determined by electron microscopic tomography J Struct Biol 127 231-239
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister W (2015) Native architecture of theChlamydomonas chloroplast revealed by in situ cryo-electron tomography eLife 4
Pubmed Author and Title
CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gabruk M Stecka A Strzalka W Kruk J Strzalka K and Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzymecomplexes reconstituted with PORA PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS One 10e0116990
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes Biochim Biophys Acta 1837 481-494Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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3
INTRODUCTION 46
47
Chloroplast biogenesis is a complex process that is essential for plant ontogenesis It 48
involves changes in gene expression together with the transcriptional and 49
translational control of both nuclear and plastid genes These genes can be regulated 50
by anterograde and retrograde signals the synthesis of necessary lipids and 51
pigments the import and routing of the nucleus-encoded proteins into plastids 52
protein-lipid interactions the insertion of proteins into the plastid membranes and the 53
assembly into functional complexes (eg Vothknecht and Westhoff 2001 Baena-54
Gonzaacutelez and Aro 2002 Kota et al 2002 Stern et al 2004 Loacutepez-Juez 2007 55
Waters and Langdale 2009 Solymosi and Schoefs 2010 Adam et al 2011 56
Pogson and Albrecht 2011 Ling et al 2012 Jarvis and Loacutepez-Juez 2013 Lyska et 57
al 2013 Belcher et al 2015 Boumlrner et al 2015 DallrsquoOsto et al 2015 Ling and 58
Jarvis 2015 Rast et al 2015 Sun and Zerges 2015 Yang et al 2015) Chloroplast 59
biogenesis is highly integrated with cell and plant development especially with 60
photomorphogenesis (Pogson et al 2015) and is controlled by cellular and 61
organismal regulatory mechanisms such as the ubiquitin-proteasome system (Jarvis 62
and Loacutepez-Juez 2013) Although biogenesis of chloroplasts has been a subject of 63
investigations for many years the correlation of simultaneous changes at the 64
structural biochemical and functional level was described only recently when time 65
dependent models of chloroplast biogenesis for bean (Phaseolus vulgaris L) and 66
pea (Pisum sativum L) were described (Rudowska et al 2012) 67
The development of chloroplasts up to the stage of etioplasts often takes place when 68
seedling growth proceeds without light Etioplasts contain characteristic structures 69
known as prolamellar bodies (PLBs) that have tubules joined together in a regular 70
network and have a special paracrystalline symmetry Together with prothylakoids 71
(PTs) mdash flattened porous membranes PLBs are precursors of the chloroplast 72
thylakoid membranes PLBs are observed under natural growing conditions when the 73
first stages of seed germination proceed under the ground and are not artificial 74
laboratory phenomena (Solymosi et al 2007 Solymosi and Schoefs 2010 Vitaacutenyi 75
et al 2013) The paracrystalline structure of PLBs can differ depending on the 76
species and the conditions of PLB crystallization All types of paracrystalline 77
arrangements have an exceptionally high surface-to-volume ratio (Gunning 2001) 78
4
Although the formation of etioplasts in darkness which have a characteristic 79
paracrystalline PLB and their transformation upon exposure to light has been 80
documented since the 1960rsquos (eg Gunning 1965 2001 Mostowska 1986a 1986b 81
Solymosi and Schoefs 2010) but the spatial arrangement of these changes is still not 82
known 83
Despite of 60 years of studies the true organization of the paracrystalline 84
membranes in three dimensions (3D) have remained unclear Cubic membranes 85
other than PLBs were described in different biological systems especially in stressed 86
conditions or virally infected cells (Almsherqi et al 2006 2009 Deng et al 2010) 87
However this widespread phenomenon is poorly understood due to having limited 88
tools available to depict periodic arrangements of cubic membranes having a lattice 89
constant in the range of 50-1000 nm (Chong and Deng 2012) This makes electron 90
tomography (ET) an extremely valuable tool to study the non-lamellar membrane 91
configurations in cells Complimentary investigation to mathematically describe the 92
spatial arrangement as a triply periodic minimal surface and compare the 2D TEM 93
images with the 2D projections of these theoretical models has been quite useful 94
(Deng and Mieczkowski 1998) However the ET technique is still required to confirm 95
any cubic membrane configuration predicted by the above direct template matching 96
technique (Chong and Deng 2012) The connections of the cubic structures with the 97
adjacent tubular or lamellar arrangements and thus the spatial changes of the local 98
topology within the paracrystalline structure are difficult to properly predict An 99
alternative method applied to precisely determine PLB tubule dimensions as well as 100
the unit cell size is small angle X-ray scattering Small angle X-ray scattering 101
performed on isolated maize (Zea mays L) PLBs confirmed their paracrystalline 102
structure with the diamond cubic lattice being the most abundant type The unit cell 103
size was 78 nm (Selstam et al 2007) However the dimensions of isolated structures 104
and those in sliced tissue ie in situ performed by ET technique are difficult to 105
compare In similar studies ET was used to determine the cubic structure of the inner 106
mitochondrial membrane morphology in amoeba (C carolinens) upon starvation 107
(Deng et al 1999) 108
The paracrystalline nature of PLBs is thought to be due to the aggregation of a 109
complex containing protochlorophyllide (Pchlide) light-dependent protochlorophyllide 110
oxidoreductase (LPOR) and NADPH (Pchlide-LPOR-NADPH) (Ryberg and 111
5
Sundqvist 1982) The spatial structure can be clarified by studying the mechanism of 112
aggregation of such complexes and their interactions with the membrane lipids 113
(Mysliwa-Kurdziel et al 2013) Although PLB tubules contain more 114
monogalactosyldiacylglycerol than PTs that facilitate cubic phase structure formation 115
both PLBs and PTs are composed from the same types of lipids 116
monogalactosyldiacylglycerol digalactosyldiacylglycerol 117
sulfoquinovosyldiacylglycerol and phosphatidylglycerol Thus it appears that the lipid 118
composition is not a critical factor and that proteins appear to play an important role 119
(Selstam 1998) It is known that integral membrane proteins have a stabilizing effect 120
on the bilayer membrane even in the presence of purified non-bilayer lipids (Rietveld 121
et al 1987) This is probably due to a strong interaction between the hydrophobic 122
region passing through the membrane and the hydrophobic tails of the lipid molecule 123
(Taraschi et al 1982) Proteins are also considered to be important in vitro for 124
transforming non-bilayer lipids into the lamellar structure (Simidjiev et al 2000) The 125
role of the large pigment-protein complex Pchlide-LPOR in the formation of PLB 126
membranes with a cubic phase structure is probably due to the ability of this pigment-127
protein complex to form an oligomer and to anchor the LPOR protein into the 128
membrane (Selstam 1998) Moreover the proper composition of carotenoids in the 129
PLB membrane can play an important role in the formation and maintenance of its 130
paracrystalline structure (Park et al 2002) 131
PLBs contain two spectral forms of the Pchlide-LPOR complexes with absorption 132
maxima at approximately 640 nm and 650 nm (Selstam et al 2002) These two 133
Pchlide forms are photoconvertible An analysis of low temperature fluorescence 134
(77K) spectra has revealed one more type of Pchlide the nonphotoconvertible form 135
Pchlide 628-633 (Boumlddi et al 1998) The longer-wavelength forms are bound to 136
PLBs while this shorter-wavelength form unbound to LPOR is mainly found in PTs 137
In addition to LPOR PLBs contain enzymes of the chlorophyll (Chl) and carotenoid 138
biosynthesis pathways enzymes of the Calvin cycle and proteins involved in 139
photosynthetic light reactions (subunits of ATP synthase the oxygen-evolving 140
complex cytochrome b6f plastocyanin and ferrodoxin-NADPH oxidoreductase) and 141
also other proteins necessary during photomorphogenesis with the exception of the 142
core subunits and the antenna complexes of the two photosystems (Blomqvist et al 143
2008 Kleffmann et al 2007 von Zychlinski et al 2005 Adam et al 2011) 144
6
Upon illumination the photomorphogenic process called greening or de-etiolation 145
takes place and etioplasts develop into chloroplasts (Ryberg and Sundqvist 1982 146
Mostowska 1986a Von Wettstein et al 1995) During this process PLBs begin to 147
both disperse and transform and Pchlide is phototransformed to chlorophyllide 148
(Chlide) In angiosperms LPOR the major protein of PLB membranes is responsible 149
for the NADPH-dependent reduction of Pchlide to Chlide during illumination (Selstam 150
et al 2002) Recently it was shown using isolated wheat PLBs that the 151
photoreduction was followed by the disruption of the PLB lattice and the formation of 152
vesicles around the PLBs Data on isolated PLBs obtained by TEM was correlated 153
with atomic force microscopy results (Grzyb et al 2013) The release of Chlide from 154
a Chlide-LPOR complex leads to the degradation of the paracrystalline PLB 155
structure (Selstam et al 2002) 156
In the case of meristematic tissues chloroplast development proceeds mainly from a 157
proplastid (Charuvi et al 2012) In this case the thylakoid membrane is formed by 158
invaginations of the inner chloroplast envelope In the differentiated chloroplast 159
however the vesicle-based transport system dominates (Rast et al 2015) If a 160
proplastid develops into an etioplast in darkness but later the PLB transformation 161
takes place upon illumination the structural changes differ from those in meristematic 162
tissues In this case the transfer system for the newly synthetized lipids and proteins 163
into the forming thylakoids can be similar to that occuring during the direct 164
development of a proplastid into a chloroplast (Rast et al 2015) However it is still 165
not clear whether the degrading PLB transforms into thylakoids continuously or 166
through the formation of vesicles (Rosinski and Rosen 1972 Adam et al 2011 167
Grzyb et al 2013 Pribil et al 2014) 168
Eventually the tubular system of PLBs transforms into a linear system of lamellae 169
arranged in parallel to each other and the first grana appear as overlapping 170
thylakoids Finally fully developed chloroplasts have the internal membrane system 171
differentiated into stacks of appressed thylakoids and nonappressed regions with 172
grana margins as well as stroma lamellae linking grana together The structure of 173
mature thylakoids is determined by the lipid composition and arrangement of 174
chlorophyll-protein (CP) complexes hierarchically organized in supercomplexes and 175
megacomplexes and spatially segregated (Dekker and Boekema 2005 Kouřil et al 176
2012 Rumak et al 2012) The main component of the appressed regions is 177
7
photosystem II (PSII) forming together with extrinsic antennae light-harvesting 178
complex II (LHCII) supercomplex LHCII-PSII while the light-harvesting complex I-179
photosystem I supercomplex (LHCI-PSI) is localized in nonappressed thylakoids 180
(Danielsson et al 2004 2006) The organization composition dynamics and 181
structural rearrangements of the developed photosynthetic apparatus of higher plants 182
under changing light conditions have been examined with high resolution microscopic 183
techniques and by spectroscopic and biochemical methods (Nevo et al 2012 Janik 184
et al 2013 Garab 2014 Jensen and Leister 2014 Pribil et al 2014) 185
Spatial models of the thylakoid membrane architecture were created with the help of 186
electron tomography in the case of fully mature higher plant chloroplasts (Shimoni et 187
al 2005 Daum et al 2010 Austin and Staehelin 2011) and Chlamydomonas 188
(Chlamydomonas reinhardtii) chloroplasts (Engel et al 2015) The most probable 189
model of thylakoid membrane organization is based on the pioneering results of 190
Paolillo (Paolillo 1970) This is a modified helical model of chloroplast membranes 191
that shows an imperfect regularity (Mustaacuterdy et al 2008 Daum et al 2010 Daum 192
and Kuumlhlbrandt 2011) and a large variability in size of the junctional connections 193
between the grana and stroma thylakoids (Austin and Staehelin 2011) 194
Although the 3D view of the overall structure of chloroplasts has been already 195
presented based on confocal laser scanning microscopy (CLSM) (Rumak et al 196
2010 2012) and on 3D models of the thylakoid membrane architecture of mature 197
chloroplasts using electron tomography (Shimoni et al 2005 Daum et al 2010 198
Austin and Staehelin 2011) a 3D membrane visualization during the etioplast-to-199
chloroplast transition can give important developmental information Without this full 200
3D information it is not possible to understand the process of the transformation of 201
the membrane structure during the chloroplast biogenesis 202
In this paper we establish the spatial 3D structure of successive stages of runner 203
bean (Phaseolus coccineus L) chloroplast biogenesis by electron tomography and 204
by confocal laser scanning microscopy We have reconstructed the paracrystalline 205
structure and the membrane connections within the PLB and the gradual 206
transformation from a tubular arrangement to the linear one during the greening 207
process Moreover we present the early stages of grana formation especially the 208
character of the grana-stroma thylakoid connections We reconstruct the spatial 209
structure of the internal plastid membrane using electron tomography with the aid of 210
8
confocal laser scanning microscopy in later stages This enables visualization and 211
thus an understanding of the membrane connections during the key stages of 212
chloroplast biogenesis We correlate the 3D structure of PLBs and of the developing 213
bean thylakoid network with the formation of CP complexes 214
The results of our studies show that the transformation of PLBs consists of the 215
untwining of tubules from the PLB structure in a continuous process The tubular 216
structure of the prolamellar body transforms directly without dispersion into vesicles 217
into flat slats that eventually in a continuous way form grana We demonstrate that 218
grana membranes from the beginning of their formation associate with stroma 219
thylakoids in a helical way 220
221
RESULTS 222
Spatial Model of Chloroplast Biogenesis 223
To determine the spatial structure of successive stages of bean chloroplast 224
biogenesis during 3 daynight cycles both CLSM and ET were used Previous results 225
from ultrastructural analysis indicated that starting from 8 d-old etiolated plants 226
chloroplast development proceeds synchronously in all plastids (Rudowska et al 227
2012) 228
To establish the sequence of structural changes of the thylakoid network during 229
chloroplast biogenesis we followed the process of biogenesis step by step from the 230
paracrystalline structure of PLB to the stacked membranes observed in the 231
ultrastructure of bean chloroplasts For the electron tomography analysis seven 232
stages of plastid internal membrane arrangements were selected during the 233
photomorphogenesis as described in Methods (Supplemental Figure 1) 234
We focused on one hand on areas of membrane connections within tightly 235
organized tubular PLB structure and grana thylakoids and on the other hand on 236
areas of loosely organized structure with transforming PLBs with newly formed 237
thylakoids 3D modeling was performed from the stage of paracrystalline structure of 238
PLB to the stage of reorganization into first appressed thylakoids and formation of 239
more developed grana 240
9
Reconstruction of the very early stages of chloroplast development by CLSM was not 241
reliable due to the small dimensions and lack of red Chl fluorescence in early 242
developmental stages Because of this the images of the etioplast internal 243
membranes obtained with CLSM were not comparable with relevant structures on 244
electron micrographs Moreover the lipophilic dye (DiOC18(3)) that was used in these 245
early stages did not incorporate uniformly into the tight paracrystalline and 246
transforming PLB membranes causing imaging artefacts Therefore spatial models 247
obtained from CLSM were used only in the two latest analyzed stages of biogenesis 248
when the Chl autofluorescence of PSII was sufficiently stable and the dimensions of 249
chloroplasts were large enough 250
251
(Stage 10) Paracrystalline prolamellar body (PLB) 252
8 d-old etiolated bean leaves have etioplasts with characteristic paracrystalline 253
prolamellar bodies as was already shown by us and other researchers (Rudowska et 254
al 2012) Based on Gunning and Steer (1975) bean etioplast PLB is of a closed 255
type with hexagonal symmetry of the tubule arrangement The tetrahedrally branched 256
basic tubular units form a typical wurtzite (a zinc iron sulfide mineral) lattice For a 257
better comparison between the PLB structure and the theoretical model of a 258
hexagonal lattice we chose perpendicular sections of the closed-type PLB for ET 259
analysis (Supplemental Figure 2) 260
We found that the structure of the PLB was a regular tetrahedral arrangement of 261
tubular connections within the PLB (Figure 1) Such a composite tomographic image 262
stack was obtained by superimposing reconstructed parallel slices such as the one 263
shown in Figure 1A The volume of the PLB (Figure 1B) and isosurface visualization 264
of the 3D reconstruction of paracrystalline PLB membranes was generated (Figure 265
1C) with the help of Imaris microscopy image processing and analysis software In 266
Figures 1C and 1D the PLB volume together with the first layer of the PLB is visible 267
For better visualization of the PLB network we highlight a single unit (orange) of the 268
PLB together with the rendered volume (Figure 1E) An enlargement of the 269
isosurface of one unit is shown (Figure 1F) together with its side view (Figure 1G) In 270
Figure 1H the theoretical model created with the help of 3ds max software showing 271
the arrangement of inner plastid membranes within the prolamellar body is displayed 272
10
273
(Stage 11) Irregular prolamellar body 274
After 1 h of illumination the regularity and the symmetry of the PLB was lost The 275
structure of the PLB became irregular and PLB membranes became rearranged 276
(Figure 2) The 3D array of branched tubes in the PLB became dissociated and the 277
characteristic tetrahedral network was no longer visible and all units lost regular 278
connections with each other A composite tomographic slice image was obtained by 279
superimposing reconstructed parallel slices representing the spatial structure of an 280
irregular PLB and this composite image is shown in Figure 2A The volume (Figure 281
2B) and isosurface (Figures 2C to 2H) of an irregular PLB was rendered with the help 282
of Imaris software Already at this stage PLB membranes both within the PLB 283
(Figures 2E to 2H) and in its marginal regions (Figure 2D) had given rise to flat 284
stromal slats at the periphery of the PLB that were seen as porous PTs PTs were 285
tightly connected with the degrading PLB that were radially spreading from the PLB 286
margins (Figure 2C) In Figures 2C and 2D the isosurface of the irregular PLB 287
together with the outer layer of the PLB is visible Upon magnification the PTs 288
emerging from the degrading PLB are seen as flat slats (Figure 2D) For better 289
visualization of the transformation from tubular elements to slats a single unit of a 290
degrading PLB net (lime green) is shown from various directions (Figures 2E to 2H) 291
We strongly emphasize that electron tomography enabled the visualization of slat 292
arrangements during transformation and untwining of PLB nodes This was not 293
possible in traditional electron microscopy 294
295
(Stage 12) Remnants of PLB and numerous prothylakoids 296
After 2 h of illumination only remnants of the PLB were observed (Figure 3) A 297
composite tomographic slice image was obtained by superimposing reconstructed 298
parallel slices of remnants of the PLB and porous PTs connected with them (Figure 299
3A) The area of interest was drawn on every slice with the help of 3DMOD software 300
(Figure 3B the middle slice in the stack) We reconstructed a particular area of 301
chloroplast membranes focusing on connections between the remnants of the PLB 302
and the PTs This model was superimposed on a TEM image for better visualization 303
of the region of interest (blue) (Figures 3C and 3D) In Figures 3E to 3G slat-like 304
11
images of PTs are presented from different angles From these models we could 305
observe that the membranes that were remnants of the PLB had a continuous 306
character as opposed to the porous PT membranes that were tightly connected with 307
the former (Figures 3E to 3G) Both types of membrane were slat-like and not tubule-308
like structures At this stage of chloroplast biogenesis the inner membranes were 309
arranged in parallel to the long chloroplast axis 310
311
(Stage 14) Parallel prothylakoids 312
After 4 h of illumination there were no more remnants of PLBs in the bean 313
chloroplasts (Figure 4) A composite tomographic slice image was obtained by 314
superimposing reconstructed parallel slices of chloroplasts at this stage of 315
development (Figure 4A) A selected area of membranes was drawn with the help of 316
3DMOD software (Figure 4B middle slice from the stack) A model of the area of 317
interest was superimposed on a TEM image for better visualization (purple) (Figures 318
4C and 4D) In Figures 4E to 4G slat-like models of porous PTs are shown after 319
rotation and presented from different angles Such models enabled the visualization 320
of the parallel arrangement of PTs and the local connections between them The PTs 321
had a slat-like and porous character and some of them had split in a dichotomous 322
manner (Figures 4E to 4G) 323
324
(Stage 18) First stacked membranes 325
After 8 h of illumination the first stacked membranes were observed (Figure 5) A 326
composite tomographic slice image was obtained in a similar way as before (Figure 327
5A) Interesting areas of thylakoid membranes especially of stacked membranes and 328
their connections to unstacked ones were drawn using 3DMOD software (Figure 5B 329
middle slice from the stack) A model of the area of interest was superimposed on the 330
TEM image (Figures 5C and 5D) In Figures 5E to 5H models of the first stacked 331
membranes are shown after magnification and presented from different angles 332
These models revealed that the appressed thylakoids (light yellow) were no longer 333
porous but had continuous membranes in the stacked region From our constructed 334
model we learned that the PTs (yellow) remained still porous although to a lesser 335
extent than at earlier stages In this model each stacked membrane was connected 336
12
to a single split PT This dichotomous splitting existed only locally where a PT joined 337
with both the upper and lower stacked membrane The PT membrane connected with 338
the stacked region not in parallel but at an angle in the range of 18 to 33deg 339
340
(Stage 20) Small grana 341
At the beginning of the second day of the experiment (Figure 6) small grana stacks 342
were observed (stage 20) A composite tomographic slice image was obtained in a 343
similar way as for the other stages of biogenesis (Figure 6A) Grana thylakoids (GTs) 344
and stroma thylakoids (STs) connected with them were drawn using the 3DMOD 345
software (Figure 6B middle slice from the stack) A small grana model was 346
superimposed on the TEM image for a better visualization of the region of interest 347
(Figures 6C and 6D) The model shows GTs (light green) arranged in parallel and no-348
longer-porous STs (green) connected with them (Figure 6E) In Figures 6F to 6I the 349
models of GTs and STs are shown from different angles Every modelled ST was 350
connected with two adjacent GTs (Figures 6F and 6G) The STs were connected with 351
the stacked region at an angle of approximately 20deg 352
As mentioned previously a CLSM study was performed for the two latest stages of 353
chloroplast biogenesis The density of the red Chl fluorescence spots in a CLSM 354
image showed the distribution of the appressed thylakoids (grana) in the chloroplast 355
(Supplemental Figure 3) There was no visible regularity of the appressed thylakoid 356
distribution (Supplemental Figure 3A) that correlated with the TEM pictures Also 3D 357
models of the computer generated isosurface of Chl fluorescence (Supplemental 358
Figures 3B to 3D) confirmed the lack of regularity of grana location within a 359
chloroplast The red fluorescence originated from the LHCII-PSII supercomplexes 360
dimers and monomers and also from LHCII trimers that were not bound and 361
localized in grana (Mehta et al 1999) Selective images of PSI and PSII in plant 362
chloroplasts in situ have shown that they are spatially separated from each other 363
however the majority of the fluorescence signals originating from PSI overlap with 364
those from PSII (Hasegawa et al 2010) Thus in the case of CLSM images of bean 365
chloroplasts the LHCI-PSI complexes can be located both in red and dark areas but 366
the LHCII-PSII and LHCII trimers are located in red fluorescence regions only 367
368
13
(Stage 33) More developed grana 369
During the third day (stage 33) chloroplasts with grana more developed than in the 370
previous stage containing numerous thylakoids were observed (Figure 7) A 371
composite tomographic slice image was obtained as in the previously analyzed 372
stages (Figure 7A) The region of interest was drawn using the 3DMOD software 373
(Figure 7B middle slice from the stack) A model of the granum (light navy) with 374
connected STs (navy) was superimposed on the TEM image (Figures 7C and 7D) In 375
Figures 7E to 7I the model is shown from different angles to visualize direct 376
connections of STs with GTs The complexity of these connections can be observed 377
Some STs were associated with two neighboring GTs as in the previous stage and 378
were connected at an angle of approximately 18deg (Fig 7E and 7F) ST can also split 379
in a dichotomous manner and connect with both the adjacent GT and the next GT in 380
the other slice (left bottom ST Figures 7F and 7H) Additionally we saw that the ST in 381
the area of our model could connect with only one GT as was observed at the top 382
and bottom of the granum (Figure 7G) This shows that the junctional slits created by 383
the connections between GTs and STs can be of different widths as was also 384
reported by Austin and Staehelin for the thylakoid network of well-developed 385
chloroplasts of mature plants (Austin and Staehelin 2011) 386
For this stage the CLSM analysis was also performed The distribution of Chl 387
autofluorescence (Supplemental Figure 4) visible in CLSM changed drastically in 388
comparison to the earlier stage of grana formation Red spots corresponding to grana 389
were uniformly distributed within the chloroplast (Supplemental Figure 4A) 3D 390
models of the computer generated isosurface of Chl fluorescence confirmed the 391
regular distribution of grana that is characteristic of a mature chloroplast (Rumak et 392
al 2010) (Figures 4B to 4D) However the size of chloroplast at this stage of 393
biogenesis was much smaller (approximately 3 μm) than the 6 μm chloroplasts found 394
in mature plants 395
Based on the TEM sections of numerous developmental stages and also on the 396
reconstruction of the membrane transformation in 3D during the 7 stages of 397
chloroplast biogenesis we proposed a 2D theoretical model (Figure 8) of the 398
membrane changes The proposed theoretical model of membrane rearrangements 399
taken together with the 3D models allow us to create a dynamic model of chloroplast 400
development which is presented as a movie (Supplemental Movie 1) 401
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
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Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
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Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
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Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
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Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
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Grzyb JM Solymosi K Strzalka K and Mysliwa-Kurdziel B (2013) Visualization and characterization of prolamellar bodieswith atomic force microscopy J Plant Physiol 170 1217-1227
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Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA FOLLOWING ALDEHYDE OSMIUM-TETROXIDEFIXATION J Cell Biol 24 79-93
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Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell (Edward Arnold London)
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective excitation of photosystems in chloroplasts inside plantleaves observed by near-infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225-238
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur R Garstka M Maksymiec W Kulik ADietler G and Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions astudy of lipid-light-harvesting complex II model membranes Plant Cell 25 2155-2170
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Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids Nat Rev Mol Cell Biol 14787-802
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Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems experimentally-investigated entropy-driven stackingof plant photosynthetic membranes Sci Rep 4 4142
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes BiochimBiophys Acta 1708 187-195
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P Gruissem W and Baginsky S (2007)Proteome dynamics during plastid differentiation in rice Plant Physiol 143 912-923
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED ANDFAR-RED LIGHT J Cell Biol 22 433-442
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV Dekker JP and Jansson S (2005) Structureof the higher plant light harvesting complex I in vivo characterization and structural interdependence of the Lhca proteinsBiochemistry (Mosc) 44 3065-3073
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) Protein assembly and heat stability in developingthylakoid membranes during greening Proc Natl Acad Sci U S A 99 12149-12154
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kouril R Dekker JP and Boekema EJ (2012) Supramolecular organization of photosystem II in green plants BiochimBiophys Acta 1817 2-12
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization of Three-Dimensional Image Data Using IMODJ Struct Biol 116 71-76
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 655-659
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-proteasome system in plastid developmentBiochim Biophys Acta 1847 939-948
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 58 11-26Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid membranes from plastid transcription to proteincomplex assembly Planta 237 413-428
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology Second Edition (CRC Press)
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography software for three-dimensional reconstructionin transmission electron microscopy BMC Bioinformatics 8 288
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings by white red and blue low intensity lightProtoplasma 131 166-173
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986b) Thylakoid and grana formation during the development of pea chloroplasts illuminated by white red andblue low intensity light Protoplasma 134 88-94
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mysliwa-Kurdziel B Kruk J and Strzalka K (2013) Protochlorophyllide in model systems--an approach to in vivo conditionsBiophys Chem 175-176 28-38
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture and dynamics of the photosynthetic apparatus inhigher plants Plant J Cell Mol Biol 70 157-176
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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4
Although the formation of etioplasts in darkness which have a characteristic 79
paracrystalline PLB and their transformation upon exposure to light has been 80
documented since the 1960rsquos (eg Gunning 1965 2001 Mostowska 1986a 1986b 81
Solymosi and Schoefs 2010) but the spatial arrangement of these changes is still not 82
known 83
Despite of 60 years of studies the true organization of the paracrystalline 84
membranes in three dimensions (3D) have remained unclear Cubic membranes 85
other than PLBs were described in different biological systems especially in stressed 86
conditions or virally infected cells (Almsherqi et al 2006 2009 Deng et al 2010) 87
However this widespread phenomenon is poorly understood due to having limited 88
tools available to depict periodic arrangements of cubic membranes having a lattice 89
constant in the range of 50-1000 nm (Chong and Deng 2012) This makes electron 90
tomography (ET) an extremely valuable tool to study the non-lamellar membrane 91
configurations in cells Complimentary investigation to mathematically describe the 92
spatial arrangement as a triply periodic minimal surface and compare the 2D TEM 93
images with the 2D projections of these theoretical models has been quite useful 94
(Deng and Mieczkowski 1998) However the ET technique is still required to confirm 95
any cubic membrane configuration predicted by the above direct template matching 96
technique (Chong and Deng 2012) The connections of the cubic structures with the 97
adjacent tubular or lamellar arrangements and thus the spatial changes of the local 98
topology within the paracrystalline structure are difficult to properly predict An 99
alternative method applied to precisely determine PLB tubule dimensions as well as 100
the unit cell size is small angle X-ray scattering Small angle X-ray scattering 101
performed on isolated maize (Zea mays L) PLBs confirmed their paracrystalline 102
structure with the diamond cubic lattice being the most abundant type The unit cell 103
size was 78 nm (Selstam et al 2007) However the dimensions of isolated structures 104
and those in sliced tissue ie in situ performed by ET technique are difficult to 105
compare In similar studies ET was used to determine the cubic structure of the inner 106
mitochondrial membrane morphology in amoeba (C carolinens) upon starvation 107
(Deng et al 1999) 108
The paracrystalline nature of PLBs is thought to be due to the aggregation of a 109
complex containing protochlorophyllide (Pchlide) light-dependent protochlorophyllide 110
oxidoreductase (LPOR) and NADPH (Pchlide-LPOR-NADPH) (Ryberg and 111
5
Sundqvist 1982) The spatial structure can be clarified by studying the mechanism of 112
aggregation of such complexes and their interactions with the membrane lipids 113
(Mysliwa-Kurdziel et al 2013) Although PLB tubules contain more 114
monogalactosyldiacylglycerol than PTs that facilitate cubic phase structure formation 115
both PLBs and PTs are composed from the same types of lipids 116
monogalactosyldiacylglycerol digalactosyldiacylglycerol 117
sulfoquinovosyldiacylglycerol and phosphatidylglycerol Thus it appears that the lipid 118
composition is not a critical factor and that proteins appear to play an important role 119
(Selstam 1998) It is known that integral membrane proteins have a stabilizing effect 120
on the bilayer membrane even in the presence of purified non-bilayer lipids (Rietveld 121
et al 1987) This is probably due to a strong interaction between the hydrophobic 122
region passing through the membrane and the hydrophobic tails of the lipid molecule 123
(Taraschi et al 1982) Proteins are also considered to be important in vitro for 124
transforming non-bilayer lipids into the lamellar structure (Simidjiev et al 2000) The 125
role of the large pigment-protein complex Pchlide-LPOR in the formation of PLB 126
membranes with a cubic phase structure is probably due to the ability of this pigment-127
protein complex to form an oligomer and to anchor the LPOR protein into the 128
membrane (Selstam 1998) Moreover the proper composition of carotenoids in the 129
PLB membrane can play an important role in the formation and maintenance of its 130
paracrystalline structure (Park et al 2002) 131
PLBs contain two spectral forms of the Pchlide-LPOR complexes with absorption 132
maxima at approximately 640 nm and 650 nm (Selstam et al 2002) These two 133
Pchlide forms are photoconvertible An analysis of low temperature fluorescence 134
(77K) spectra has revealed one more type of Pchlide the nonphotoconvertible form 135
Pchlide 628-633 (Boumlddi et al 1998) The longer-wavelength forms are bound to 136
PLBs while this shorter-wavelength form unbound to LPOR is mainly found in PTs 137
In addition to LPOR PLBs contain enzymes of the chlorophyll (Chl) and carotenoid 138
biosynthesis pathways enzymes of the Calvin cycle and proteins involved in 139
photosynthetic light reactions (subunits of ATP synthase the oxygen-evolving 140
complex cytochrome b6f plastocyanin and ferrodoxin-NADPH oxidoreductase) and 141
also other proteins necessary during photomorphogenesis with the exception of the 142
core subunits and the antenna complexes of the two photosystems (Blomqvist et al 143
2008 Kleffmann et al 2007 von Zychlinski et al 2005 Adam et al 2011) 144
6
Upon illumination the photomorphogenic process called greening or de-etiolation 145
takes place and etioplasts develop into chloroplasts (Ryberg and Sundqvist 1982 146
Mostowska 1986a Von Wettstein et al 1995) During this process PLBs begin to 147
both disperse and transform and Pchlide is phototransformed to chlorophyllide 148
(Chlide) In angiosperms LPOR the major protein of PLB membranes is responsible 149
for the NADPH-dependent reduction of Pchlide to Chlide during illumination (Selstam 150
et al 2002) Recently it was shown using isolated wheat PLBs that the 151
photoreduction was followed by the disruption of the PLB lattice and the formation of 152
vesicles around the PLBs Data on isolated PLBs obtained by TEM was correlated 153
with atomic force microscopy results (Grzyb et al 2013) The release of Chlide from 154
a Chlide-LPOR complex leads to the degradation of the paracrystalline PLB 155
structure (Selstam et al 2002) 156
In the case of meristematic tissues chloroplast development proceeds mainly from a 157
proplastid (Charuvi et al 2012) In this case the thylakoid membrane is formed by 158
invaginations of the inner chloroplast envelope In the differentiated chloroplast 159
however the vesicle-based transport system dominates (Rast et al 2015) If a 160
proplastid develops into an etioplast in darkness but later the PLB transformation 161
takes place upon illumination the structural changes differ from those in meristematic 162
tissues In this case the transfer system for the newly synthetized lipids and proteins 163
into the forming thylakoids can be similar to that occuring during the direct 164
development of a proplastid into a chloroplast (Rast et al 2015) However it is still 165
not clear whether the degrading PLB transforms into thylakoids continuously or 166
through the formation of vesicles (Rosinski and Rosen 1972 Adam et al 2011 167
Grzyb et al 2013 Pribil et al 2014) 168
Eventually the tubular system of PLBs transforms into a linear system of lamellae 169
arranged in parallel to each other and the first grana appear as overlapping 170
thylakoids Finally fully developed chloroplasts have the internal membrane system 171
differentiated into stacks of appressed thylakoids and nonappressed regions with 172
grana margins as well as stroma lamellae linking grana together The structure of 173
mature thylakoids is determined by the lipid composition and arrangement of 174
chlorophyll-protein (CP) complexes hierarchically organized in supercomplexes and 175
megacomplexes and spatially segregated (Dekker and Boekema 2005 Kouřil et al 176
2012 Rumak et al 2012) The main component of the appressed regions is 177
7
photosystem II (PSII) forming together with extrinsic antennae light-harvesting 178
complex II (LHCII) supercomplex LHCII-PSII while the light-harvesting complex I-179
photosystem I supercomplex (LHCI-PSI) is localized in nonappressed thylakoids 180
(Danielsson et al 2004 2006) The organization composition dynamics and 181
structural rearrangements of the developed photosynthetic apparatus of higher plants 182
under changing light conditions have been examined with high resolution microscopic 183
techniques and by spectroscopic and biochemical methods (Nevo et al 2012 Janik 184
et al 2013 Garab 2014 Jensen and Leister 2014 Pribil et al 2014) 185
Spatial models of the thylakoid membrane architecture were created with the help of 186
electron tomography in the case of fully mature higher plant chloroplasts (Shimoni et 187
al 2005 Daum et al 2010 Austin and Staehelin 2011) and Chlamydomonas 188
(Chlamydomonas reinhardtii) chloroplasts (Engel et al 2015) The most probable 189
model of thylakoid membrane organization is based on the pioneering results of 190
Paolillo (Paolillo 1970) This is a modified helical model of chloroplast membranes 191
that shows an imperfect regularity (Mustaacuterdy et al 2008 Daum et al 2010 Daum 192
and Kuumlhlbrandt 2011) and a large variability in size of the junctional connections 193
between the grana and stroma thylakoids (Austin and Staehelin 2011) 194
Although the 3D view of the overall structure of chloroplasts has been already 195
presented based on confocal laser scanning microscopy (CLSM) (Rumak et al 196
2010 2012) and on 3D models of the thylakoid membrane architecture of mature 197
chloroplasts using electron tomography (Shimoni et al 2005 Daum et al 2010 198
Austin and Staehelin 2011) a 3D membrane visualization during the etioplast-to-199
chloroplast transition can give important developmental information Without this full 200
3D information it is not possible to understand the process of the transformation of 201
the membrane structure during the chloroplast biogenesis 202
In this paper we establish the spatial 3D structure of successive stages of runner 203
bean (Phaseolus coccineus L) chloroplast biogenesis by electron tomography and 204
by confocal laser scanning microscopy We have reconstructed the paracrystalline 205
structure and the membrane connections within the PLB and the gradual 206
transformation from a tubular arrangement to the linear one during the greening 207
process Moreover we present the early stages of grana formation especially the 208
character of the grana-stroma thylakoid connections We reconstruct the spatial 209
structure of the internal plastid membrane using electron tomography with the aid of 210
8
confocal laser scanning microscopy in later stages This enables visualization and 211
thus an understanding of the membrane connections during the key stages of 212
chloroplast biogenesis We correlate the 3D structure of PLBs and of the developing 213
bean thylakoid network with the formation of CP complexes 214
The results of our studies show that the transformation of PLBs consists of the 215
untwining of tubules from the PLB structure in a continuous process The tubular 216
structure of the prolamellar body transforms directly without dispersion into vesicles 217
into flat slats that eventually in a continuous way form grana We demonstrate that 218
grana membranes from the beginning of their formation associate with stroma 219
thylakoids in a helical way 220
221
RESULTS 222
Spatial Model of Chloroplast Biogenesis 223
To determine the spatial structure of successive stages of bean chloroplast 224
biogenesis during 3 daynight cycles both CLSM and ET were used Previous results 225
from ultrastructural analysis indicated that starting from 8 d-old etiolated plants 226
chloroplast development proceeds synchronously in all plastids (Rudowska et al 227
2012) 228
To establish the sequence of structural changes of the thylakoid network during 229
chloroplast biogenesis we followed the process of biogenesis step by step from the 230
paracrystalline structure of PLB to the stacked membranes observed in the 231
ultrastructure of bean chloroplasts For the electron tomography analysis seven 232
stages of plastid internal membrane arrangements were selected during the 233
photomorphogenesis as described in Methods (Supplemental Figure 1) 234
We focused on one hand on areas of membrane connections within tightly 235
organized tubular PLB structure and grana thylakoids and on the other hand on 236
areas of loosely organized structure with transforming PLBs with newly formed 237
thylakoids 3D modeling was performed from the stage of paracrystalline structure of 238
PLB to the stage of reorganization into first appressed thylakoids and formation of 239
more developed grana 240
9
Reconstruction of the very early stages of chloroplast development by CLSM was not 241
reliable due to the small dimensions and lack of red Chl fluorescence in early 242
developmental stages Because of this the images of the etioplast internal 243
membranes obtained with CLSM were not comparable with relevant structures on 244
electron micrographs Moreover the lipophilic dye (DiOC18(3)) that was used in these 245
early stages did not incorporate uniformly into the tight paracrystalline and 246
transforming PLB membranes causing imaging artefacts Therefore spatial models 247
obtained from CLSM were used only in the two latest analyzed stages of biogenesis 248
when the Chl autofluorescence of PSII was sufficiently stable and the dimensions of 249
chloroplasts were large enough 250
251
(Stage 10) Paracrystalline prolamellar body (PLB) 252
8 d-old etiolated bean leaves have etioplasts with characteristic paracrystalline 253
prolamellar bodies as was already shown by us and other researchers (Rudowska et 254
al 2012) Based on Gunning and Steer (1975) bean etioplast PLB is of a closed 255
type with hexagonal symmetry of the tubule arrangement The tetrahedrally branched 256
basic tubular units form a typical wurtzite (a zinc iron sulfide mineral) lattice For a 257
better comparison between the PLB structure and the theoretical model of a 258
hexagonal lattice we chose perpendicular sections of the closed-type PLB for ET 259
analysis (Supplemental Figure 2) 260
We found that the structure of the PLB was a regular tetrahedral arrangement of 261
tubular connections within the PLB (Figure 1) Such a composite tomographic image 262
stack was obtained by superimposing reconstructed parallel slices such as the one 263
shown in Figure 1A The volume of the PLB (Figure 1B) and isosurface visualization 264
of the 3D reconstruction of paracrystalline PLB membranes was generated (Figure 265
1C) with the help of Imaris microscopy image processing and analysis software In 266
Figures 1C and 1D the PLB volume together with the first layer of the PLB is visible 267
For better visualization of the PLB network we highlight a single unit (orange) of the 268
PLB together with the rendered volume (Figure 1E) An enlargement of the 269
isosurface of one unit is shown (Figure 1F) together with its side view (Figure 1G) In 270
Figure 1H the theoretical model created with the help of 3ds max software showing 271
the arrangement of inner plastid membranes within the prolamellar body is displayed 272
10
273
(Stage 11) Irregular prolamellar body 274
After 1 h of illumination the regularity and the symmetry of the PLB was lost The 275
structure of the PLB became irregular and PLB membranes became rearranged 276
(Figure 2) The 3D array of branched tubes in the PLB became dissociated and the 277
characteristic tetrahedral network was no longer visible and all units lost regular 278
connections with each other A composite tomographic slice image was obtained by 279
superimposing reconstructed parallel slices representing the spatial structure of an 280
irregular PLB and this composite image is shown in Figure 2A The volume (Figure 281
2B) and isosurface (Figures 2C to 2H) of an irregular PLB was rendered with the help 282
of Imaris software Already at this stage PLB membranes both within the PLB 283
(Figures 2E to 2H) and in its marginal regions (Figure 2D) had given rise to flat 284
stromal slats at the periphery of the PLB that were seen as porous PTs PTs were 285
tightly connected with the degrading PLB that were radially spreading from the PLB 286
margins (Figure 2C) In Figures 2C and 2D the isosurface of the irregular PLB 287
together with the outer layer of the PLB is visible Upon magnification the PTs 288
emerging from the degrading PLB are seen as flat slats (Figure 2D) For better 289
visualization of the transformation from tubular elements to slats a single unit of a 290
degrading PLB net (lime green) is shown from various directions (Figures 2E to 2H) 291
We strongly emphasize that electron tomography enabled the visualization of slat 292
arrangements during transformation and untwining of PLB nodes This was not 293
possible in traditional electron microscopy 294
295
(Stage 12) Remnants of PLB and numerous prothylakoids 296
After 2 h of illumination only remnants of the PLB were observed (Figure 3) A 297
composite tomographic slice image was obtained by superimposing reconstructed 298
parallel slices of remnants of the PLB and porous PTs connected with them (Figure 299
3A) The area of interest was drawn on every slice with the help of 3DMOD software 300
(Figure 3B the middle slice in the stack) We reconstructed a particular area of 301
chloroplast membranes focusing on connections between the remnants of the PLB 302
and the PTs This model was superimposed on a TEM image for better visualization 303
of the region of interest (blue) (Figures 3C and 3D) In Figures 3E to 3G slat-like 304
11
images of PTs are presented from different angles From these models we could 305
observe that the membranes that were remnants of the PLB had a continuous 306
character as opposed to the porous PT membranes that were tightly connected with 307
the former (Figures 3E to 3G) Both types of membrane were slat-like and not tubule-308
like structures At this stage of chloroplast biogenesis the inner membranes were 309
arranged in parallel to the long chloroplast axis 310
311
(Stage 14) Parallel prothylakoids 312
After 4 h of illumination there were no more remnants of PLBs in the bean 313
chloroplasts (Figure 4) A composite tomographic slice image was obtained by 314
superimposing reconstructed parallel slices of chloroplasts at this stage of 315
development (Figure 4A) A selected area of membranes was drawn with the help of 316
3DMOD software (Figure 4B middle slice from the stack) A model of the area of 317
interest was superimposed on a TEM image for better visualization (purple) (Figures 318
4C and 4D) In Figures 4E to 4G slat-like models of porous PTs are shown after 319
rotation and presented from different angles Such models enabled the visualization 320
of the parallel arrangement of PTs and the local connections between them The PTs 321
had a slat-like and porous character and some of them had split in a dichotomous 322
manner (Figures 4E to 4G) 323
324
(Stage 18) First stacked membranes 325
After 8 h of illumination the first stacked membranes were observed (Figure 5) A 326
composite tomographic slice image was obtained in a similar way as before (Figure 327
5A) Interesting areas of thylakoid membranes especially of stacked membranes and 328
their connections to unstacked ones were drawn using 3DMOD software (Figure 5B 329
middle slice from the stack) A model of the area of interest was superimposed on the 330
TEM image (Figures 5C and 5D) In Figures 5E to 5H models of the first stacked 331
membranes are shown after magnification and presented from different angles 332
These models revealed that the appressed thylakoids (light yellow) were no longer 333
porous but had continuous membranes in the stacked region From our constructed 334
model we learned that the PTs (yellow) remained still porous although to a lesser 335
extent than at earlier stages In this model each stacked membrane was connected 336
12
to a single split PT This dichotomous splitting existed only locally where a PT joined 337
with both the upper and lower stacked membrane The PT membrane connected with 338
the stacked region not in parallel but at an angle in the range of 18 to 33deg 339
340
(Stage 20) Small grana 341
At the beginning of the second day of the experiment (Figure 6) small grana stacks 342
were observed (stage 20) A composite tomographic slice image was obtained in a 343
similar way as for the other stages of biogenesis (Figure 6A) Grana thylakoids (GTs) 344
and stroma thylakoids (STs) connected with them were drawn using the 3DMOD 345
software (Figure 6B middle slice from the stack) A small grana model was 346
superimposed on the TEM image for a better visualization of the region of interest 347
(Figures 6C and 6D) The model shows GTs (light green) arranged in parallel and no-348
longer-porous STs (green) connected with them (Figure 6E) In Figures 6F to 6I the 349
models of GTs and STs are shown from different angles Every modelled ST was 350
connected with two adjacent GTs (Figures 6F and 6G) The STs were connected with 351
the stacked region at an angle of approximately 20deg 352
As mentioned previously a CLSM study was performed for the two latest stages of 353
chloroplast biogenesis The density of the red Chl fluorescence spots in a CLSM 354
image showed the distribution of the appressed thylakoids (grana) in the chloroplast 355
(Supplemental Figure 3) There was no visible regularity of the appressed thylakoid 356
distribution (Supplemental Figure 3A) that correlated with the TEM pictures Also 3D 357
models of the computer generated isosurface of Chl fluorescence (Supplemental 358
Figures 3B to 3D) confirmed the lack of regularity of grana location within a 359
chloroplast The red fluorescence originated from the LHCII-PSII supercomplexes 360
dimers and monomers and also from LHCII trimers that were not bound and 361
localized in grana (Mehta et al 1999) Selective images of PSI and PSII in plant 362
chloroplasts in situ have shown that they are spatially separated from each other 363
however the majority of the fluorescence signals originating from PSI overlap with 364
those from PSII (Hasegawa et al 2010) Thus in the case of CLSM images of bean 365
chloroplasts the LHCI-PSI complexes can be located both in red and dark areas but 366
the LHCII-PSII and LHCII trimers are located in red fluorescence regions only 367
368
13
(Stage 33) More developed grana 369
During the third day (stage 33) chloroplasts with grana more developed than in the 370
previous stage containing numerous thylakoids were observed (Figure 7) A 371
composite tomographic slice image was obtained as in the previously analyzed 372
stages (Figure 7A) The region of interest was drawn using the 3DMOD software 373
(Figure 7B middle slice from the stack) A model of the granum (light navy) with 374
connected STs (navy) was superimposed on the TEM image (Figures 7C and 7D) In 375
Figures 7E to 7I the model is shown from different angles to visualize direct 376
connections of STs with GTs The complexity of these connections can be observed 377
Some STs were associated with two neighboring GTs as in the previous stage and 378
were connected at an angle of approximately 18deg (Fig 7E and 7F) ST can also split 379
in a dichotomous manner and connect with both the adjacent GT and the next GT in 380
the other slice (left bottom ST Figures 7F and 7H) Additionally we saw that the ST in 381
the area of our model could connect with only one GT as was observed at the top 382
and bottom of the granum (Figure 7G) This shows that the junctional slits created by 383
the connections between GTs and STs can be of different widths as was also 384
reported by Austin and Staehelin for the thylakoid network of well-developed 385
chloroplasts of mature plants (Austin and Staehelin 2011) 386
For this stage the CLSM analysis was also performed The distribution of Chl 387
autofluorescence (Supplemental Figure 4) visible in CLSM changed drastically in 388
comparison to the earlier stage of grana formation Red spots corresponding to grana 389
were uniformly distributed within the chloroplast (Supplemental Figure 4A) 3D 390
models of the computer generated isosurface of Chl fluorescence confirmed the 391
regular distribution of grana that is characteristic of a mature chloroplast (Rumak et 392
al 2010) (Figures 4B to 4D) However the size of chloroplast at this stage of 393
biogenesis was much smaller (approximately 3 μm) than the 6 μm chloroplasts found 394
in mature plants 395
Based on the TEM sections of numerous developmental stages and also on the 396
reconstruction of the membrane transformation in 3D during the 7 stages of 397
chloroplast biogenesis we proposed a 2D theoretical model (Figure 8) of the 398
membrane changes The proposed theoretical model of membrane rearrangements 399
taken together with the 3D models allow us to create a dynamic model of chloroplast 400
development which is presented as a movie (Supplemental Movie 1) 401
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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5
Sundqvist 1982) The spatial structure can be clarified by studying the mechanism of 112
aggregation of such complexes and their interactions with the membrane lipids 113
(Mysliwa-Kurdziel et al 2013) Although PLB tubules contain more 114
monogalactosyldiacylglycerol than PTs that facilitate cubic phase structure formation 115
both PLBs and PTs are composed from the same types of lipids 116
monogalactosyldiacylglycerol digalactosyldiacylglycerol 117
sulfoquinovosyldiacylglycerol and phosphatidylglycerol Thus it appears that the lipid 118
composition is not a critical factor and that proteins appear to play an important role 119
(Selstam 1998) It is known that integral membrane proteins have a stabilizing effect 120
on the bilayer membrane even in the presence of purified non-bilayer lipids (Rietveld 121
et al 1987) This is probably due to a strong interaction between the hydrophobic 122
region passing through the membrane and the hydrophobic tails of the lipid molecule 123
(Taraschi et al 1982) Proteins are also considered to be important in vitro for 124
transforming non-bilayer lipids into the lamellar structure (Simidjiev et al 2000) The 125
role of the large pigment-protein complex Pchlide-LPOR in the formation of PLB 126
membranes with a cubic phase structure is probably due to the ability of this pigment-127
protein complex to form an oligomer and to anchor the LPOR protein into the 128
membrane (Selstam 1998) Moreover the proper composition of carotenoids in the 129
PLB membrane can play an important role in the formation and maintenance of its 130
paracrystalline structure (Park et al 2002) 131
PLBs contain two spectral forms of the Pchlide-LPOR complexes with absorption 132
maxima at approximately 640 nm and 650 nm (Selstam et al 2002) These two 133
Pchlide forms are photoconvertible An analysis of low temperature fluorescence 134
(77K) spectra has revealed one more type of Pchlide the nonphotoconvertible form 135
Pchlide 628-633 (Boumlddi et al 1998) The longer-wavelength forms are bound to 136
PLBs while this shorter-wavelength form unbound to LPOR is mainly found in PTs 137
In addition to LPOR PLBs contain enzymes of the chlorophyll (Chl) and carotenoid 138
biosynthesis pathways enzymes of the Calvin cycle and proteins involved in 139
photosynthetic light reactions (subunits of ATP synthase the oxygen-evolving 140
complex cytochrome b6f plastocyanin and ferrodoxin-NADPH oxidoreductase) and 141
also other proteins necessary during photomorphogenesis with the exception of the 142
core subunits and the antenna complexes of the two photosystems (Blomqvist et al 143
2008 Kleffmann et al 2007 von Zychlinski et al 2005 Adam et al 2011) 144
6
Upon illumination the photomorphogenic process called greening or de-etiolation 145
takes place and etioplasts develop into chloroplasts (Ryberg and Sundqvist 1982 146
Mostowska 1986a Von Wettstein et al 1995) During this process PLBs begin to 147
both disperse and transform and Pchlide is phototransformed to chlorophyllide 148
(Chlide) In angiosperms LPOR the major protein of PLB membranes is responsible 149
for the NADPH-dependent reduction of Pchlide to Chlide during illumination (Selstam 150
et al 2002) Recently it was shown using isolated wheat PLBs that the 151
photoreduction was followed by the disruption of the PLB lattice and the formation of 152
vesicles around the PLBs Data on isolated PLBs obtained by TEM was correlated 153
with atomic force microscopy results (Grzyb et al 2013) The release of Chlide from 154
a Chlide-LPOR complex leads to the degradation of the paracrystalline PLB 155
structure (Selstam et al 2002) 156
In the case of meristematic tissues chloroplast development proceeds mainly from a 157
proplastid (Charuvi et al 2012) In this case the thylakoid membrane is formed by 158
invaginations of the inner chloroplast envelope In the differentiated chloroplast 159
however the vesicle-based transport system dominates (Rast et al 2015) If a 160
proplastid develops into an etioplast in darkness but later the PLB transformation 161
takes place upon illumination the structural changes differ from those in meristematic 162
tissues In this case the transfer system for the newly synthetized lipids and proteins 163
into the forming thylakoids can be similar to that occuring during the direct 164
development of a proplastid into a chloroplast (Rast et al 2015) However it is still 165
not clear whether the degrading PLB transforms into thylakoids continuously or 166
through the formation of vesicles (Rosinski and Rosen 1972 Adam et al 2011 167
Grzyb et al 2013 Pribil et al 2014) 168
Eventually the tubular system of PLBs transforms into a linear system of lamellae 169
arranged in parallel to each other and the first grana appear as overlapping 170
thylakoids Finally fully developed chloroplasts have the internal membrane system 171
differentiated into stacks of appressed thylakoids and nonappressed regions with 172
grana margins as well as stroma lamellae linking grana together The structure of 173
mature thylakoids is determined by the lipid composition and arrangement of 174
chlorophyll-protein (CP) complexes hierarchically organized in supercomplexes and 175
megacomplexes and spatially segregated (Dekker and Boekema 2005 Kouřil et al 176
2012 Rumak et al 2012) The main component of the appressed regions is 177
7
photosystem II (PSII) forming together with extrinsic antennae light-harvesting 178
complex II (LHCII) supercomplex LHCII-PSII while the light-harvesting complex I-179
photosystem I supercomplex (LHCI-PSI) is localized in nonappressed thylakoids 180
(Danielsson et al 2004 2006) The organization composition dynamics and 181
structural rearrangements of the developed photosynthetic apparatus of higher plants 182
under changing light conditions have been examined with high resolution microscopic 183
techniques and by spectroscopic and biochemical methods (Nevo et al 2012 Janik 184
et al 2013 Garab 2014 Jensen and Leister 2014 Pribil et al 2014) 185
Spatial models of the thylakoid membrane architecture were created with the help of 186
electron tomography in the case of fully mature higher plant chloroplasts (Shimoni et 187
al 2005 Daum et al 2010 Austin and Staehelin 2011) and Chlamydomonas 188
(Chlamydomonas reinhardtii) chloroplasts (Engel et al 2015) The most probable 189
model of thylakoid membrane organization is based on the pioneering results of 190
Paolillo (Paolillo 1970) This is a modified helical model of chloroplast membranes 191
that shows an imperfect regularity (Mustaacuterdy et al 2008 Daum et al 2010 Daum 192
and Kuumlhlbrandt 2011) and a large variability in size of the junctional connections 193
between the grana and stroma thylakoids (Austin and Staehelin 2011) 194
Although the 3D view of the overall structure of chloroplasts has been already 195
presented based on confocal laser scanning microscopy (CLSM) (Rumak et al 196
2010 2012) and on 3D models of the thylakoid membrane architecture of mature 197
chloroplasts using electron tomography (Shimoni et al 2005 Daum et al 2010 198
Austin and Staehelin 2011) a 3D membrane visualization during the etioplast-to-199
chloroplast transition can give important developmental information Without this full 200
3D information it is not possible to understand the process of the transformation of 201
the membrane structure during the chloroplast biogenesis 202
In this paper we establish the spatial 3D structure of successive stages of runner 203
bean (Phaseolus coccineus L) chloroplast biogenesis by electron tomography and 204
by confocal laser scanning microscopy We have reconstructed the paracrystalline 205
structure and the membrane connections within the PLB and the gradual 206
transformation from a tubular arrangement to the linear one during the greening 207
process Moreover we present the early stages of grana formation especially the 208
character of the grana-stroma thylakoid connections We reconstruct the spatial 209
structure of the internal plastid membrane using electron tomography with the aid of 210
8
confocal laser scanning microscopy in later stages This enables visualization and 211
thus an understanding of the membrane connections during the key stages of 212
chloroplast biogenesis We correlate the 3D structure of PLBs and of the developing 213
bean thylakoid network with the formation of CP complexes 214
The results of our studies show that the transformation of PLBs consists of the 215
untwining of tubules from the PLB structure in a continuous process The tubular 216
structure of the prolamellar body transforms directly without dispersion into vesicles 217
into flat slats that eventually in a continuous way form grana We demonstrate that 218
grana membranes from the beginning of their formation associate with stroma 219
thylakoids in a helical way 220
221
RESULTS 222
Spatial Model of Chloroplast Biogenesis 223
To determine the spatial structure of successive stages of bean chloroplast 224
biogenesis during 3 daynight cycles both CLSM and ET were used Previous results 225
from ultrastructural analysis indicated that starting from 8 d-old etiolated plants 226
chloroplast development proceeds synchronously in all plastids (Rudowska et al 227
2012) 228
To establish the sequence of structural changes of the thylakoid network during 229
chloroplast biogenesis we followed the process of biogenesis step by step from the 230
paracrystalline structure of PLB to the stacked membranes observed in the 231
ultrastructure of bean chloroplasts For the electron tomography analysis seven 232
stages of plastid internal membrane arrangements were selected during the 233
photomorphogenesis as described in Methods (Supplemental Figure 1) 234
We focused on one hand on areas of membrane connections within tightly 235
organized tubular PLB structure and grana thylakoids and on the other hand on 236
areas of loosely organized structure with transforming PLBs with newly formed 237
thylakoids 3D modeling was performed from the stage of paracrystalline structure of 238
PLB to the stage of reorganization into first appressed thylakoids and formation of 239
more developed grana 240
9
Reconstruction of the very early stages of chloroplast development by CLSM was not 241
reliable due to the small dimensions and lack of red Chl fluorescence in early 242
developmental stages Because of this the images of the etioplast internal 243
membranes obtained with CLSM were not comparable with relevant structures on 244
electron micrographs Moreover the lipophilic dye (DiOC18(3)) that was used in these 245
early stages did not incorporate uniformly into the tight paracrystalline and 246
transforming PLB membranes causing imaging artefacts Therefore spatial models 247
obtained from CLSM were used only in the two latest analyzed stages of biogenesis 248
when the Chl autofluorescence of PSII was sufficiently stable and the dimensions of 249
chloroplasts were large enough 250
251
(Stage 10) Paracrystalline prolamellar body (PLB) 252
8 d-old etiolated bean leaves have etioplasts with characteristic paracrystalline 253
prolamellar bodies as was already shown by us and other researchers (Rudowska et 254
al 2012) Based on Gunning and Steer (1975) bean etioplast PLB is of a closed 255
type with hexagonal symmetry of the tubule arrangement The tetrahedrally branched 256
basic tubular units form a typical wurtzite (a zinc iron sulfide mineral) lattice For a 257
better comparison between the PLB structure and the theoretical model of a 258
hexagonal lattice we chose perpendicular sections of the closed-type PLB for ET 259
analysis (Supplemental Figure 2) 260
We found that the structure of the PLB was a regular tetrahedral arrangement of 261
tubular connections within the PLB (Figure 1) Such a composite tomographic image 262
stack was obtained by superimposing reconstructed parallel slices such as the one 263
shown in Figure 1A The volume of the PLB (Figure 1B) and isosurface visualization 264
of the 3D reconstruction of paracrystalline PLB membranes was generated (Figure 265
1C) with the help of Imaris microscopy image processing and analysis software In 266
Figures 1C and 1D the PLB volume together with the first layer of the PLB is visible 267
For better visualization of the PLB network we highlight a single unit (orange) of the 268
PLB together with the rendered volume (Figure 1E) An enlargement of the 269
isosurface of one unit is shown (Figure 1F) together with its side view (Figure 1G) In 270
Figure 1H the theoretical model created with the help of 3ds max software showing 271
the arrangement of inner plastid membranes within the prolamellar body is displayed 272
10
273
(Stage 11) Irregular prolamellar body 274
After 1 h of illumination the regularity and the symmetry of the PLB was lost The 275
structure of the PLB became irregular and PLB membranes became rearranged 276
(Figure 2) The 3D array of branched tubes in the PLB became dissociated and the 277
characteristic tetrahedral network was no longer visible and all units lost regular 278
connections with each other A composite tomographic slice image was obtained by 279
superimposing reconstructed parallel slices representing the spatial structure of an 280
irregular PLB and this composite image is shown in Figure 2A The volume (Figure 281
2B) and isosurface (Figures 2C to 2H) of an irregular PLB was rendered with the help 282
of Imaris software Already at this stage PLB membranes both within the PLB 283
(Figures 2E to 2H) and in its marginal regions (Figure 2D) had given rise to flat 284
stromal slats at the periphery of the PLB that were seen as porous PTs PTs were 285
tightly connected with the degrading PLB that were radially spreading from the PLB 286
margins (Figure 2C) In Figures 2C and 2D the isosurface of the irregular PLB 287
together with the outer layer of the PLB is visible Upon magnification the PTs 288
emerging from the degrading PLB are seen as flat slats (Figure 2D) For better 289
visualization of the transformation from tubular elements to slats a single unit of a 290
degrading PLB net (lime green) is shown from various directions (Figures 2E to 2H) 291
We strongly emphasize that electron tomography enabled the visualization of slat 292
arrangements during transformation and untwining of PLB nodes This was not 293
possible in traditional electron microscopy 294
295
(Stage 12) Remnants of PLB and numerous prothylakoids 296
After 2 h of illumination only remnants of the PLB were observed (Figure 3) A 297
composite tomographic slice image was obtained by superimposing reconstructed 298
parallel slices of remnants of the PLB and porous PTs connected with them (Figure 299
3A) The area of interest was drawn on every slice with the help of 3DMOD software 300
(Figure 3B the middle slice in the stack) We reconstructed a particular area of 301
chloroplast membranes focusing on connections between the remnants of the PLB 302
and the PTs This model was superimposed on a TEM image for better visualization 303
of the region of interest (blue) (Figures 3C and 3D) In Figures 3E to 3G slat-like 304
11
images of PTs are presented from different angles From these models we could 305
observe that the membranes that were remnants of the PLB had a continuous 306
character as opposed to the porous PT membranes that were tightly connected with 307
the former (Figures 3E to 3G) Both types of membrane were slat-like and not tubule-308
like structures At this stage of chloroplast biogenesis the inner membranes were 309
arranged in parallel to the long chloroplast axis 310
311
(Stage 14) Parallel prothylakoids 312
After 4 h of illumination there were no more remnants of PLBs in the bean 313
chloroplasts (Figure 4) A composite tomographic slice image was obtained by 314
superimposing reconstructed parallel slices of chloroplasts at this stage of 315
development (Figure 4A) A selected area of membranes was drawn with the help of 316
3DMOD software (Figure 4B middle slice from the stack) A model of the area of 317
interest was superimposed on a TEM image for better visualization (purple) (Figures 318
4C and 4D) In Figures 4E to 4G slat-like models of porous PTs are shown after 319
rotation and presented from different angles Such models enabled the visualization 320
of the parallel arrangement of PTs and the local connections between them The PTs 321
had a slat-like and porous character and some of them had split in a dichotomous 322
manner (Figures 4E to 4G) 323
324
(Stage 18) First stacked membranes 325
After 8 h of illumination the first stacked membranes were observed (Figure 5) A 326
composite tomographic slice image was obtained in a similar way as before (Figure 327
5A) Interesting areas of thylakoid membranes especially of stacked membranes and 328
their connections to unstacked ones were drawn using 3DMOD software (Figure 5B 329
middle slice from the stack) A model of the area of interest was superimposed on the 330
TEM image (Figures 5C and 5D) In Figures 5E to 5H models of the first stacked 331
membranes are shown after magnification and presented from different angles 332
These models revealed that the appressed thylakoids (light yellow) were no longer 333
porous but had continuous membranes in the stacked region From our constructed 334
model we learned that the PTs (yellow) remained still porous although to a lesser 335
extent than at earlier stages In this model each stacked membrane was connected 336
12
to a single split PT This dichotomous splitting existed only locally where a PT joined 337
with both the upper and lower stacked membrane The PT membrane connected with 338
the stacked region not in parallel but at an angle in the range of 18 to 33deg 339
340
(Stage 20) Small grana 341
At the beginning of the second day of the experiment (Figure 6) small grana stacks 342
were observed (stage 20) A composite tomographic slice image was obtained in a 343
similar way as for the other stages of biogenesis (Figure 6A) Grana thylakoids (GTs) 344
and stroma thylakoids (STs) connected with them were drawn using the 3DMOD 345
software (Figure 6B middle slice from the stack) A small grana model was 346
superimposed on the TEM image for a better visualization of the region of interest 347
(Figures 6C and 6D) The model shows GTs (light green) arranged in parallel and no-348
longer-porous STs (green) connected with them (Figure 6E) In Figures 6F to 6I the 349
models of GTs and STs are shown from different angles Every modelled ST was 350
connected with two adjacent GTs (Figures 6F and 6G) The STs were connected with 351
the stacked region at an angle of approximately 20deg 352
As mentioned previously a CLSM study was performed for the two latest stages of 353
chloroplast biogenesis The density of the red Chl fluorescence spots in a CLSM 354
image showed the distribution of the appressed thylakoids (grana) in the chloroplast 355
(Supplemental Figure 3) There was no visible regularity of the appressed thylakoid 356
distribution (Supplemental Figure 3A) that correlated with the TEM pictures Also 3D 357
models of the computer generated isosurface of Chl fluorescence (Supplemental 358
Figures 3B to 3D) confirmed the lack of regularity of grana location within a 359
chloroplast The red fluorescence originated from the LHCII-PSII supercomplexes 360
dimers and monomers and also from LHCII trimers that were not bound and 361
localized in grana (Mehta et al 1999) Selective images of PSI and PSII in plant 362
chloroplasts in situ have shown that they are spatially separated from each other 363
however the majority of the fluorescence signals originating from PSI overlap with 364
those from PSII (Hasegawa et al 2010) Thus in the case of CLSM images of bean 365
chloroplasts the LHCI-PSI complexes can be located both in red and dark areas but 366
the LHCII-PSII and LHCII trimers are located in red fluorescence regions only 367
368
13
(Stage 33) More developed grana 369
During the third day (stage 33) chloroplasts with grana more developed than in the 370
previous stage containing numerous thylakoids were observed (Figure 7) A 371
composite tomographic slice image was obtained as in the previously analyzed 372
stages (Figure 7A) The region of interest was drawn using the 3DMOD software 373
(Figure 7B middle slice from the stack) A model of the granum (light navy) with 374
connected STs (navy) was superimposed on the TEM image (Figures 7C and 7D) In 375
Figures 7E to 7I the model is shown from different angles to visualize direct 376
connections of STs with GTs The complexity of these connections can be observed 377
Some STs were associated with two neighboring GTs as in the previous stage and 378
were connected at an angle of approximately 18deg (Fig 7E and 7F) ST can also split 379
in a dichotomous manner and connect with both the adjacent GT and the next GT in 380
the other slice (left bottom ST Figures 7F and 7H) Additionally we saw that the ST in 381
the area of our model could connect with only one GT as was observed at the top 382
and bottom of the granum (Figure 7G) This shows that the junctional slits created by 383
the connections between GTs and STs can be of different widths as was also 384
reported by Austin and Staehelin for the thylakoid network of well-developed 385
chloroplasts of mature plants (Austin and Staehelin 2011) 386
For this stage the CLSM analysis was also performed The distribution of Chl 387
autofluorescence (Supplemental Figure 4) visible in CLSM changed drastically in 388
comparison to the earlier stage of grana formation Red spots corresponding to grana 389
were uniformly distributed within the chloroplast (Supplemental Figure 4A) 3D 390
models of the computer generated isosurface of Chl fluorescence confirmed the 391
regular distribution of grana that is characteristic of a mature chloroplast (Rumak et 392
al 2010) (Figures 4B to 4D) However the size of chloroplast at this stage of 393
biogenesis was much smaller (approximately 3 μm) than the 6 μm chloroplasts found 394
in mature plants 395
Based on the TEM sections of numerous developmental stages and also on the 396
reconstruction of the membrane transformation in 3D during the 7 stages of 397
chloroplast biogenesis we proposed a 2D theoretical model (Figure 8) of the 398
membrane changes The proposed theoretical model of membrane rearrangements 399
taken together with the 3D models allow us to create a dynamic model of chloroplast 400
development which is presented as a movie (Supplemental Movie 1) 401
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
Parsed CitationsAbdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) High salt stress induces swollen prothylakoids indark-grown wheat and alters both prolamellar body transformation and reformation after irradiation J Exp Bot 58 2553-2564
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ Biophotonics International 11 36-42Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of thylakoid networks in angiosperms knowns andunknowns Plant Mol Biol 76 221-234
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend beyond the Flatland of cell membraneorganization J Cell Biol 173 839-844
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic membranes the missing dimension of cellmembrane organization Int Rev Cell Mol Biol 274 275-342
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the structure and function of photosystem II in higherplant thylakoid membranes the grana enigma Photosynth Res 98 575-587
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R and Dekker JP (2005) Origin of the F685 andF695 fluorescence in photosystem II Photosynth Res 84 173-180
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants asdetermined by electron tomography Plant Physiol 155 1601-1611
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of photosystem II units Philos Trans R Soc LondB Biol Sci 357 1451-1459 discussion 1459-1460
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale genetic analysis of chloroplast biogenesis in maizeBiochim Biophys Acta 1847 1004-1016
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals theirsignificance in chloroplast development Photosynth Res 96 37-50
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The two spectroscopically different short wavelengthprotochlorophyllide forms in pea epicotyls are both monomeric Biochim Biophys Acta 1365 531-540
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast RNA polymerases Role in chloroplast biogenesisBiochim Biophys Acta 1847 761-769
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR (2010) Energy transfer processes in the isolated
core antenna complexes CP43 and CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606-1616Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain and loss of photosynthetic membranes duringplastid differentiation in the shoot apex of Arabidopsis Plant Cell 24 1143-1157
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar to cubic membrane transition as investigatedby electron microscopy Methods Cell Biol 108 319-343
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of thylakoid membranes in higher plant chloroplaststhe physicochemical forces at work and the functional consequences that ensue Photochem Photobiol Sci Off J EurPhotochem Assoc Eur Soc Photobiol 4 1081-1090
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
DallOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting proteins Biochim Biophys Acta 1847 861-871Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) Quantification of photosystem I and II in different parts of thethylakoid membrane from spinach Biochim Biophys Acta 1608 53-61
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-M and Mamedov F (2006) Dimeric andmonomeric organization of photosystem II Distribution of five distinct complexes in the different domains of the thylakoidmembrane J Biol Chem 281 14241-14249
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid membranes J Exp Bot 62 2393-2402Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) Arrangement of photosystem II and ATP synthase inchloroplast membranes of spinach and pea Plant Cell 22 1299-1312
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants BiochimBiophys Acta 1706 12-39
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses subvert cholesterol homeostasis to induce host cubicmembranes Trends Cell Biol 20 371-379
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane structure in the mitochondria of amoebaeChaos carolinensis Protoplasma 20316-25
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA (1999) Cubic membrane structure in amoeba(Chaos carolinensis) mitochondria determined by electron microscopic tomography J Struct Biol 127 231-239
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister W (2015) Native architecture of theChlamydomonas chloroplast revealed by in situ cryo-electron tomography eLife 4
Pubmed Author and Title
CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gabruk M Stecka A Strzalka W Kruk J Strzalka K and Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzymecomplexes reconstituted with PORA PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS One 10e0116990
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes Biochim Biophys Acta 1837 481-494Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Grzyb JM Solymosi K Strzalka K and Mysliwa-Kurdziel B (2013) Visualization and characterization of prolamellar bodieswith atomic force microscopy J Plant Physiol 170 1217-1227
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (2001) Membrane geometry of open prolamellar bodies Protoplasma 215 4-15Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA FOLLOWING ALDEHYDE OSMIUM-TETROXIDEFIXATION J Cell Biol 24 79-93
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell (Edward Arnold London)
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective excitation of photosystems in chloroplasts inside plantleaves observed by near-infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225-238
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur R Garstka M Maksymiec W Kulik ADietler G and Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions astudy of lipid-light-harvesting complex II model membranes Plant Cell 25 2155-2170
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
6
Upon illumination the photomorphogenic process called greening or de-etiolation 145
takes place and etioplasts develop into chloroplasts (Ryberg and Sundqvist 1982 146
Mostowska 1986a Von Wettstein et al 1995) During this process PLBs begin to 147
both disperse and transform and Pchlide is phototransformed to chlorophyllide 148
(Chlide) In angiosperms LPOR the major protein of PLB membranes is responsible 149
for the NADPH-dependent reduction of Pchlide to Chlide during illumination (Selstam 150
et al 2002) Recently it was shown using isolated wheat PLBs that the 151
photoreduction was followed by the disruption of the PLB lattice and the formation of 152
vesicles around the PLBs Data on isolated PLBs obtained by TEM was correlated 153
with atomic force microscopy results (Grzyb et al 2013) The release of Chlide from 154
a Chlide-LPOR complex leads to the degradation of the paracrystalline PLB 155
structure (Selstam et al 2002) 156
In the case of meristematic tissues chloroplast development proceeds mainly from a 157
proplastid (Charuvi et al 2012) In this case the thylakoid membrane is formed by 158
invaginations of the inner chloroplast envelope In the differentiated chloroplast 159
however the vesicle-based transport system dominates (Rast et al 2015) If a 160
proplastid develops into an etioplast in darkness but later the PLB transformation 161
takes place upon illumination the structural changes differ from those in meristematic 162
tissues In this case the transfer system for the newly synthetized lipids and proteins 163
into the forming thylakoids can be similar to that occuring during the direct 164
development of a proplastid into a chloroplast (Rast et al 2015) However it is still 165
not clear whether the degrading PLB transforms into thylakoids continuously or 166
through the formation of vesicles (Rosinski and Rosen 1972 Adam et al 2011 167
Grzyb et al 2013 Pribil et al 2014) 168
Eventually the tubular system of PLBs transforms into a linear system of lamellae 169
arranged in parallel to each other and the first grana appear as overlapping 170
thylakoids Finally fully developed chloroplasts have the internal membrane system 171
differentiated into stacks of appressed thylakoids and nonappressed regions with 172
grana margins as well as stroma lamellae linking grana together The structure of 173
mature thylakoids is determined by the lipid composition and arrangement of 174
chlorophyll-protein (CP) complexes hierarchically organized in supercomplexes and 175
megacomplexes and spatially segregated (Dekker and Boekema 2005 Kouřil et al 176
2012 Rumak et al 2012) The main component of the appressed regions is 177
7
photosystem II (PSII) forming together with extrinsic antennae light-harvesting 178
complex II (LHCII) supercomplex LHCII-PSII while the light-harvesting complex I-179
photosystem I supercomplex (LHCI-PSI) is localized in nonappressed thylakoids 180
(Danielsson et al 2004 2006) The organization composition dynamics and 181
structural rearrangements of the developed photosynthetic apparatus of higher plants 182
under changing light conditions have been examined with high resolution microscopic 183
techniques and by spectroscopic and biochemical methods (Nevo et al 2012 Janik 184
et al 2013 Garab 2014 Jensen and Leister 2014 Pribil et al 2014) 185
Spatial models of the thylakoid membrane architecture were created with the help of 186
electron tomography in the case of fully mature higher plant chloroplasts (Shimoni et 187
al 2005 Daum et al 2010 Austin and Staehelin 2011) and Chlamydomonas 188
(Chlamydomonas reinhardtii) chloroplasts (Engel et al 2015) The most probable 189
model of thylakoid membrane organization is based on the pioneering results of 190
Paolillo (Paolillo 1970) This is a modified helical model of chloroplast membranes 191
that shows an imperfect regularity (Mustaacuterdy et al 2008 Daum et al 2010 Daum 192
and Kuumlhlbrandt 2011) and a large variability in size of the junctional connections 193
between the grana and stroma thylakoids (Austin and Staehelin 2011) 194
Although the 3D view of the overall structure of chloroplasts has been already 195
presented based on confocal laser scanning microscopy (CLSM) (Rumak et al 196
2010 2012) and on 3D models of the thylakoid membrane architecture of mature 197
chloroplasts using electron tomography (Shimoni et al 2005 Daum et al 2010 198
Austin and Staehelin 2011) a 3D membrane visualization during the etioplast-to-199
chloroplast transition can give important developmental information Without this full 200
3D information it is not possible to understand the process of the transformation of 201
the membrane structure during the chloroplast biogenesis 202
In this paper we establish the spatial 3D structure of successive stages of runner 203
bean (Phaseolus coccineus L) chloroplast biogenesis by electron tomography and 204
by confocal laser scanning microscopy We have reconstructed the paracrystalline 205
structure and the membrane connections within the PLB and the gradual 206
transformation from a tubular arrangement to the linear one during the greening 207
process Moreover we present the early stages of grana formation especially the 208
character of the grana-stroma thylakoid connections We reconstruct the spatial 209
structure of the internal plastid membrane using electron tomography with the aid of 210
8
confocal laser scanning microscopy in later stages This enables visualization and 211
thus an understanding of the membrane connections during the key stages of 212
chloroplast biogenesis We correlate the 3D structure of PLBs and of the developing 213
bean thylakoid network with the formation of CP complexes 214
The results of our studies show that the transformation of PLBs consists of the 215
untwining of tubules from the PLB structure in a continuous process The tubular 216
structure of the prolamellar body transforms directly without dispersion into vesicles 217
into flat slats that eventually in a continuous way form grana We demonstrate that 218
grana membranes from the beginning of their formation associate with stroma 219
thylakoids in a helical way 220
221
RESULTS 222
Spatial Model of Chloroplast Biogenesis 223
To determine the spatial structure of successive stages of bean chloroplast 224
biogenesis during 3 daynight cycles both CLSM and ET were used Previous results 225
from ultrastructural analysis indicated that starting from 8 d-old etiolated plants 226
chloroplast development proceeds synchronously in all plastids (Rudowska et al 227
2012) 228
To establish the sequence of structural changes of the thylakoid network during 229
chloroplast biogenesis we followed the process of biogenesis step by step from the 230
paracrystalline structure of PLB to the stacked membranes observed in the 231
ultrastructure of bean chloroplasts For the electron tomography analysis seven 232
stages of plastid internal membrane arrangements were selected during the 233
photomorphogenesis as described in Methods (Supplemental Figure 1) 234
We focused on one hand on areas of membrane connections within tightly 235
organized tubular PLB structure and grana thylakoids and on the other hand on 236
areas of loosely organized structure with transforming PLBs with newly formed 237
thylakoids 3D modeling was performed from the stage of paracrystalline structure of 238
PLB to the stage of reorganization into first appressed thylakoids and formation of 239
more developed grana 240
9
Reconstruction of the very early stages of chloroplast development by CLSM was not 241
reliable due to the small dimensions and lack of red Chl fluorescence in early 242
developmental stages Because of this the images of the etioplast internal 243
membranes obtained with CLSM were not comparable with relevant structures on 244
electron micrographs Moreover the lipophilic dye (DiOC18(3)) that was used in these 245
early stages did not incorporate uniformly into the tight paracrystalline and 246
transforming PLB membranes causing imaging artefacts Therefore spatial models 247
obtained from CLSM were used only in the two latest analyzed stages of biogenesis 248
when the Chl autofluorescence of PSII was sufficiently stable and the dimensions of 249
chloroplasts were large enough 250
251
(Stage 10) Paracrystalline prolamellar body (PLB) 252
8 d-old etiolated bean leaves have etioplasts with characteristic paracrystalline 253
prolamellar bodies as was already shown by us and other researchers (Rudowska et 254
al 2012) Based on Gunning and Steer (1975) bean etioplast PLB is of a closed 255
type with hexagonal symmetry of the tubule arrangement The tetrahedrally branched 256
basic tubular units form a typical wurtzite (a zinc iron sulfide mineral) lattice For a 257
better comparison between the PLB structure and the theoretical model of a 258
hexagonal lattice we chose perpendicular sections of the closed-type PLB for ET 259
analysis (Supplemental Figure 2) 260
We found that the structure of the PLB was a regular tetrahedral arrangement of 261
tubular connections within the PLB (Figure 1) Such a composite tomographic image 262
stack was obtained by superimposing reconstructed parallel slices such as the one 263
shown in Figure 1A The volume of the PLB (Figure 1B) and isosurface visualization 264
of the 3D reconstruction of paracrystalline PLB membranes was generated (Figure 265
1C) with the help of Imaris microscopy image processing and analysis software In 266
Figures 1C and 1D the PLB volume together with the first layer of the PLB is visible 267
For better visualization of the PLB network we highlight a single unit (orange) of the 268
PLB together with the rendered volume (Figure 1E) An enlargement of the 269
isosurface of one unit is shown (Figure 1F) together with its side view (Figure 1G) In 270
Figure 1H the theoretical model created with the help of 3ds max software showing 271
the arrangement of inner plastid membranes within the prolamellar body is displayed 272
10
273
(Stage 11) Irregular prolamellar body 274
After 1 h of illumination the regularity and the symmetry of the PLB was lost The 275
structure of the PLB became irregular and PLB membranes became rearranged 276
(Figure 2) The 3D array of branched tubes in the PLB became dissociated and the 277
characteristic tetrahedral network was no longer visible and all units lost regular 278
connections with each other A composite tomographic slice image was obtained by 279
superimposing reconstructed parallel slices representing the spatial structure of an 280
irregular PLB and this composite image is shown in Figure 2A The volume (Figure 281
2B) and isosurface (Figures 2C to 2H) of an irregular PLB was rendered with the help 282
of Imaris software Already at this stage PLB membranes both within the PLB 283
(Figures 2E to 2H) and in its marginal regions (Figure 2D) had given rise to flat 284
stromal slats at the periphery of the PLB that were seen as porous PTs PTs were 285
tightly connected with the degrading PLB that were radially spreading from the PLB 286
margins (Figure 2C) In Figures 2C and 2D the isosurface of the irregular PLB 287
together with the outer layer of the PLB is visible Upon magnification the PTs 288
emerging from the degrading PLB are seen as flat slats (Figure 2D) For better 289
visualization of the transformation from tubular elements to slats a single unit of a 290
degrading PLB net (lime green) is shown from various directions (Figures 2E to 2H) 291
We strongly emphasize that electron tomography enabled the visualization of slat 292
arrangements during transformation and untwining of PLB nodes This was not 293
possible in traditional electron microscopy 294
295
(Stage 12) Remnants of PLB and numerous prothylakoids 296
After 2 h of illumination only remnants of the PLB were observed (Figure 3) A 297
composite tomographic slice image was obtained by superimposing reconstructed 298
parallel slices of remnants of the PLB and porous PTs connected with them (Figure 299
3A) The area of interest was drawn on every slice with the help of 3DMOD software 300
(Figure 3B the middle slice in the stack) We reconstructed a particular area of 301
chloroplast membranes focusing on connections between the remnants of the PLB 302
and the PTs This model was superimposed on a TEM image for better visualization 303
of the region of interest (blue) (Figures 3C and 3D) In Figures 3E to 3G slat-like 304
11
images of PTs are presented from different angles From these models we could 305
observe that the membranes that were remnants of the PLB had a continuous 306
character as opposed to the porous PT membranes that were tightly connected with 307
the former (Figures 3E to 3G) Both types of membrane were slat-like and not tubule-308
like structures At this stage of chloroplast biogenesis the inner membranes were 309
arranged in parallel to the long chloroplast axis 310
311
(Stage 14) Parallel prothylakoids 312
After 4 h of illumination there were no more remnants of PLBs in the bean 313
chloroplasts (Figure 4) A composite tomographic slice image was obtained by 314
superimposing reconstructed parallel slices of chloroplasts at this stage of 315
development (Figure 4A) A selected area of membranes was drawn with the help of 316
3DMOD software (Figure 4B middle slice from the stack) A model of the area of 317
interest was superimposed on a TEM image for better visualization (purple) (Figures 318
4C and 4D) In Figures 4E to 4G slat-like models of porous PTs are shown after 319
rotation and presented from different angles Such models enabled the visualization 320
of the parallel arrangement of PTs and the local connections between them The PTs 321
had a slat-like and porous character and some of them had split in a dichotomous 322
manner (Figures 4E to 4G) 323
324
(Stage 18) First stacked membranes 325
After 8 h of illumination the first stacked membranes were observed (Figure 5) A 326
composite tomographic slice image was obtained in a similar way as before (Figure 327
5A) Interesting areas of thylakoid membranes especially of stacked membranes and 328
their connections to unstacked ones were drawn using 3DMOD software (Figure 5B 329
middle slice from the stack) A model of the area of interest was superimposed on the 330
TEM image (Figures 5C and 5D) In Figures 5E to 5H models of the first stacked 331
membranes are shown after magnification and presented from different angles 332
These models revealed that the appressed thylakoids (light yellow) were no longer 333
porous but had continuous membranes in the stacked region From our constructed 334
model we learned that the PTs (yellow) remained still porous although to a lesser 335
extent than at earlier stages In this model each stacked membrane was connected 336
12
to a single split PT This dichotomous splitting existed only locally where a PT joined 337
with both the upper and lower stacked membrane The PT membrane connected with 338
the stacked region not in parallel but at an angle in the range of 18 to 33deg 339
340
(Stage 20) Small grana 341
At the beginning of the second day of the experiment (Figure 6) small grana stacks 342
were observed (stage 20) A composite tomographic slice image was obtained in a 343
similar way as for the other stages of biogenesis (Figure 6A) Grana thylakoids (GTs) 344
and stroma thylakoids (STs) connected with them were drawn using the 3DMOD 345
software (Figure 6B middle slice from the stack) A small grana model was 346
superimposed on the TEM image for a better visualization of the region of interest 347
(Figures 6C and 6D) The model shows GTs (light green) arranged in parallel and no-348
longer-porous STs (green) connected with them (Figure 6E) In Figures 6F to 6I the 349
models of GTs and STs are shown from different angles Every modelled ST was 350
connected with two adjacent GTs (Figures 6F and 6G) The STs were connected with 351
the stacked region at an angle of approximately 20deg 352
As mentioned previously a CLSM study was performed for the two latest stages of 353
chloroplast biogenesis The density of the red Chl fluorescence spots in a CLSM 354
image showed the distribution of the appressed thylakoids (grana) in the chloroplast 355
(Supplemental Figure 3) There was no visible regularity of the appressed thylakoid 356
distribution (Supplemental Figure 3A) that correlated with the TEM pictures Also 3D 357
models of the computer generated isosurface of Chl fluorescence (Supplemental 358
Figures 3B to 3D) confirmed the lack of regularity of grana location within a 359
chloroplast The red fluorescence originated from the LHCII-PSII supercomplexes 360
dimers and monomers and also from LHCII trimers that were not bound and 361
localized in grana (Mehta et al 1999) Selective images of PSI and PSII in plant 362
chloroplasts in situ have shown that they are spatially separated from each other 363
however the majority of the fluorescence signals originating from PSI overlap with 364
those from PSII (Hasegawa et al 2010) Thus in the case of CLSM images of bean 365
chloroplasts the LHCI-PSI complexes can be located both in red and dark areas but 366
the LHCII-PSII and LHCII trimers are located in red fluorescence regions only 367
368
13
(Stage 33) More developed grana 369
During the third day (stage 33) chloroplasts with grana more developed than in the 370
previous stage containing numerous thylakoids were observed (Figure 7) A 371
composite tomographic slice image was obtained as in the previously analyzed 372
stages (Figure 7A) The region of interest was drawn using the 3DMOD software 373
(Figure 7B middle slice from the stack) A model of the granum (light navy) with 374
connected STs (navy) was superimposed on the TEM image (Figures 7C and 7D) In 375
Figures 7E to 7I the model is shown from different angles to visualize direct 376
connections of STs with GTs The complexity of these connections can be observed 377
Some STs were associated with two neighboring GTs as in the previous stage and 378
were connected at an angle of approximately 18deg (Fig 7E and 7F) ST can also split 379
in a dichotomous manner and connect with both the adjacent GT and the next GT in 380
the other slice (left bottom ST Figures 7F and 7H) Additionally we saw that the ST in 381
the area of our model could connect with only one GT as was observed at the top 382
and bottom of the granum (Figure 7G) This shows that the junctional slits created by 383
the connections between GTs and STs can be of different widths as was also 384
reported by Austin and Staehelin for the thylakoid network of well-developed 385
chloroplasts of mature plants (Austin and Staehelin 2011) 386
For this stage the CLSM analysis was also performed The distribution of Chl 387
autofluorescence (Supplemental Figure 4) visible in CLSM changed drastically in 388
comparison to the earlier stage of grana formation Red spots corresponding to grana 389
were uniformly distributed within the chloroplast (Supplemental Figure 4A) 3D 390
models of the computer generated isosurface of Chl fluorescence confirmed the 391
regular distribution of grana that is characteristic of a mature chloroplast (Rumak et 392
al 2010) (Figures 4B to 4D) However the size of chloroplast at this stage of 393
biogenesis was much smaller (approximately 3 μm) than the 6 μm chloroplasts found 394
in mature plants 395
Based on the TEM sections of numerous developmental stages and also on the 396
reconstruction of the membrane transformation in 3D during the 7 stages of 397
chloroplast biogenesis we proposed a 2D theoretical model (Figure 8) of the 398
membrane changes The proposed theoretical model of membrane rearrangements 399
taken together with the 3D models allow us to create a dynamic model of chloroplast 400
development which is presented as a movie (Supplemental Movie 1) 401
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
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Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
7
photosystem II (PSII) forming together with extrinsic antennae light-harvesting 178
complex II (LHCII) supercomplex LHCII-PSII while the light-harvesting complex I-179
photosystem I supercomplex (LHCI-PSI) is localized in nonappressed thylakoids 180
(Danielsson et al 2004 2006) The organization composition dynamics and 181
structural rearrangements of the developed photosynthetic apparatus of higher plants 182
under changing light conditions have been examined with high resolution microscopic 183
techniques and by spectroscopic and biochemical methods (Nevo et al 2012 Janik 184
et al 2013 Garab 2014 Jensen and Leister 2014 Pribil et al 2014) 185
Spatial models of the thylakoid membrane architecture were created with the help of 186
electron tomography in the case of fully mature higher plant chloroplasts (Shimoni et 187
al 2005 Daum et al 2010 Austin and Staehelin 2011) and Chlamydomonas 188
(Chlamydomonas reinhardtii) chloroplasts (Engel et al 2015) The most probable 189
model of thylakoid membrane organization is based on the pioneering results of 190
Paolillo (Paolillo 1970) This is a modified helical model of chloroplast membranes 191
that shows an imperfect regularity (Mustaacuterdy et al 2008 Daum et al 2010 Daum 192
and Kuumlhlbrandt 2011) and a large variability in size of the junctional connections 193
between the grana and stroma thylakoids (Austin and Staehelin 2011) 194
Although the 3D view of the overall structure of chloroplasts has been already 195
presented based on confocal laser scanning microscopy (CLSM) (Rumak et al 196
2010 2012) and on 3D models of the thylakoid membrane architecture of mature 197
chloroplasts using electron tomography (Shimoni et al 2005 Daum et al 2010 198
Austin and Staehelin 2011) a 3D membrane visualization during the etioplast-to-199
chloroplast transition can give important developmental information Without this full 200
3D information it is not possible to understand the process of the transformation of 201
the membrane structure during the chloroplast biogenesis 202
In this paper we establish the spatial 3D structure of successive stages of runner 203
bean (Phaseolus coccineus L) chloroplast biogenesis by electron tomography and 204
by confocal laser scanning microscopy We have reconstructed the paracrystalline 205
structure and the membrane connections within the PLB and the gradual 206
transformation from a tubular arrangement to the linear one during the greening 207
process Moreover we present the early stages of grana formation especially the 208
character of the grana-stroma thylakoid connections We reconstruct the spatial 209
structure of the internal plastid membrane using electron tomography with the aid of 210
8
confocal laser scanning microscopy in later stages This enables visualization and 211
thus an understanding of the membrane connections during the key stages of 212
chloroplast biogenesis We correlate the 3D structure of PLBs and of the developing 213
bean thylakoid network with the formation of CP complexes 214
The results of our studies show that the transformation of PLBs consists of the 215
untwining of tubules from the PLB structure in a continuous process The tubular 216
structure of the prolamellar body transforms directly without dispersion into vesicles 217
into flat slats that eventually in a continuous way form grana We demonstrate that 218
grana membranes from the beginning of their formation associate with stroma 219
thylakoids in a helical way 220
221
RESULTS 222
Spatial Model of Chloroplast Biogenesis 223
To determine the spatial structure of successive stages of bean chloroplast 224
biogenesis during 3 daynight cycles both CLSM and ET were used Previous results 225
from ultrastructural analysis indicated that starting from 8 d-old etiolated plants 226
chloroplast development proceeds synchronously in all plastids (Rudowska et al 227
2012) 228
To establish the sequence of structural changes of the thylakoid network during 229
chloroplast biogenesis we followed the process of biogenesis step by step from the 230
paracrystalline structure of PLB to the stacked membranes observed in the 231
ultrastructure of bean chloroplasts For the electron tomography analysis seven 232
stages of plastid internal membrane arrangements were selected during the 233
photomorphogenesis as described in Methods (Supplemental Figure 1) 234
We focused on one hand on areas of membrane connections within tightly 235
organized tubular PLB structure and grana thylakoids and on the other hand on 236
areas of loosely organized structure with transforming PLBs with newly formed 237
thylakoids 3D modeling was performed from the stage of paracrystalline structure of 238
PLB to the stage of reorganization into first appressed thylakoids and formation of 239
more developed grana 240
9
Reconstruction of the very early stages of chloroplast development by CLSM was not 241
reliable due to the small dimensions and lack of red Chl fluorescence in early 242
developmental stages Because of this the images of the etioplast internal 243
membranes obtained with CLSM were not comparable with relevant structures on 244
electron micrographs Moreover the lipophilic dye (DiOC18(3)) that was used in these 245
early stages did not incorporate uniformly into the tight paracrystalline and 246
transforming PLB membranes causing imaging artefacts Therefore spatial models 247
obtained from CLSM were used only in the two latest analyzed stages of biogenesis 248
when the Chl autofluorescence of PSII was sufficiently stable and the dimensions of 249
chloroplasts were large enough 250
251
(Stage 10) Paracrystalline prolamellar body (PLB) 252
8 d-old etiolated bean leaves have etioplasts with characteristic paracrystalline 253
prolamellar bodies as was already shown by us and other researchers (Rudowska et 254
al 2012) Based on Gunning and Steer (1975) bean etioplast PLB is of a closed 255
type with hexagonal symmetry of the tubule arrangement The tetrahedrally branched 256
basic tubular units form a typical wurtzite (a zinc iron sulfide mineral) lattice For a 257
better comparison between the PLB structure and the theoretical model of a 258
hexagonal lattice we chose perpendicular sections of the closed-type PLB for ET 259
analysis (Supplemental Figure 2) 260
We found that the structure of the PLB was a regular tetrahedral arrangement of 261
tubular connections within the PLB (Figure 1) Such a composite tomographic image 262
stack was obtained by superimposing reconstructed parallel slices such as the one 263
shown in Figure 1A The volume of the PLB (Figure 1B) and isosurface visualization 264
of the 3D reconstruction of paracrystalline PLB membranes was generated (Figure 265
1C) with the help of Imaris microscopy image processing and analysis software In 266
Figures 1C and 1D the PLB volume together with the first layer of the PLB is visible 267
For better visualization of the PLB network we highlight a single unit (orange) of the 268
PLB together with the rendered volume (Figure 1E) An enlargement of the 269
isosurface of one unit is shown (Figure 1F) together with its side view (Figure 1G) In 270
Figure 1H the theoretical model created with the help of 3ds max software showing 271
the arrangement of inner plastid membranes within the prolamellar body is displayed 272
10
273
(Stage 11) Irregular prolamellar body 274
After 1 h of illumination the regularity and the symmetry of the PLB was lost The 275
structure of the PLB became irregular and PLB membranes became rearranged 276
(Figure 2) The 3D array of branched tubes in the PLB became dissociated and the 277
characteristic tetrahedral network was no longer visible and all units lost regular 278
connections with each other A composite tomographic slice image was obtained by 279
superimposing reconstructed parallel slices representing the spatial structure of an 280
irregular PLB and this composite image is shown in Figure 2A The volume (Figure 281
2B) and isosurface (Figures 2C to 2H) of an irregular PLB was rendered with the help 282
of Imaris software Already at this stage PLB membranes both within the PLB 283
(Figures 2E to 2H) and in its marginal regions (Figure 2D) had given rise to flat 284
stromal slats at the periphery of the PLB that were seen as porous PTs PTs were 285
tightly connected with the degrading PLB that were radially spreading from the PLB 286
margins (Figure 2C) In Figures 2C and 2D the isosurface of the irregular PLB 287
together with the outer layer of the PLB is visible Upon magnification the PTs 288
emerging from the degrading PLB are seen as flat slats (Figure 2D) For better 289
visualization of the transformation from tubular elements to slats a single unit of a 290
degrading PLB net (lime green) is shown from various directions (Figures 2E to 2H) 291
We strongly emphasize that electron tomography enabled the visualization of slat 292
arrangements during transformation and untwining of PLB nodes This was not 293
possible in traditional electron microscopy 294
295
(Stage 12) Remnants of PLB and numerous prothylakoids 296
After 2 h of illumination only remnants of the PLB were observed (Figure 3) A 297
composite tomographic slice image was obtained by superimposing reconstructed 298
parallel slices of remnants of the PLB and porous PTs connected with them (Figure 299
3A) The area of interest was drawn on every slice with the help of 3DMOD software 300
(Figure 3B the middle slice in the stack) We reconstructed a particular area of 301
chloroplast membranes focusing on connections between the remnants of the PLB 302
and the PTs This model was superimposed on a TEM image for better visualization 303
of the region of interest (blue) (Figures 3C and 3D) In Figures 3E to 3G slat-like 304
11
images of PTs are presented from different angles From these models we could 305
observe that the membranes that were remnants of the PLB had a continuous 306
character as opposed to the porous PT membranes that were tightly connected with 307
the former (Figures 3E to 3G) Both types of membrane were slat-like and not tubule-308
like structures At this stage of chloroplast biogenesis the inner membranes were 309
arranged in parallel to the long chloroplast axis 310
311
(Stage 14) Parallel prothylakoids 312
After 4 h of illumination there were no more remnants of PLBs in the bean 313
chloroplasts (Figure 4) A composite tomographic slice image was obtained by 314
superimposing reconstructed parallel slices of chloroplasts at this stage of 315
development (Figure 4A) A selected area of membranes was drawn with the help of 316
3DMOD software (Figure 4B middle slice from the stack) A model of the area of 317
interest was superimposed on a TEM image for better visualization (purple) (Figures 318
4C and 4D) In Figures 4E to 4G slat-like models of porous PTs are shown after 319
rotation and presented from different angles Such models enabled the visualization 320
of the parallel arrangement of PTs and the local connections between them The PTs 321
had a slat-like and porous character and some of them had split in a dichotomous 322
manner (Figures 4E to 4G) 323
324
(Stage 18) First stacked membranes 325
After 8 h of illumination the first stacked membranes were observed (Figure 5) A 326
composite tomographic slice image was obtained in a similar way as before (Figure 327
5A) Interesting areas of thylakoid membranes especially of stacked membranes and 328
their connections to unstacked ones were drawn using 3DMOD software (Figure 5B 329
middle slice from the stack) A model of the area of interest was superimposed on the 330
TEM image (Figures 5C and 5D) In Figures 5E to 5H models of the first stacked 331
membranes are shown after magnification and presented from different angles 332
These models revealed that the appressed thylakoids (light yellow) were no longer 333
porous but had continuous membranes in the stacked region From our constructed 334
model we learned that the PTs (yellow) remained still porous although to a lesser 335
extent than at earlier stages In this model each stacked membrane was connected 336
12
to a single split PT This dichotomous splitting existed only locally where a PT joined 337
with both the upper and lower stacked membrane The PT membrane connected with 338
the stacked region not in parallel but at an angle in the range of 18 to 33deg 339
340
(Stage 20) Small grana 341
At the beginning of the second day of the experiment (Figure 6) small grana stacks 342
were observed (stage 20) A composite tomographic slice image was obtained in a 343
similar way as for the other stages of biogenesis (Figure 6A) Grana thylakoids (GTs) 344
and stroma thylakoids (STs) connected with them were drawn using the 3DMOD 345
software (Figure 6B middle slice from the stack) A small grana model was 346
superimposed on the TEM image for a better visualization of the region of interest 347
(Figures 6C and 6D) The model shows GTs (light green) arranged in parallel and no-348
longer-porous STs (green) connected with them (Figure 6E) In Figures 6F to 6I the 349
models of GTs and STs are shown from different angles Every modelled ST was 350
connected with two adjacent GTs (Figures 6F and 6G) The STs were connected with 351
the stacked region at an angle of approximately 20deg 352
As mentioned previously a CLSM study was performed for the two latest stages of 353
chloroplast biogenesis The density of the red Chl fluorescence spots in a CLSM 354
image showed the distribution of the appressed thylakoids (grana) in the chloroplast 355
(Supplemental Figure 3) There was no visible regularity of the appressed thylakoid 356
distribution (Supplemental Figure 3A) that correlated with the TEM pictures Also 3D 357
models of the computer generated isosurface of Chl fluorescence (Supplemental 358
Figures 3B to 3D) confirmed the lack of regularity of grana location within a 359
chloroplast The red fluorescence originated from the LHCII-PSII supercomplexes 360
dimers and monomers and also from LHCII trimers that were not bound and 361
localized in grana (Mehta et al 1999) Selective images of PSI and PSII in plant 362
chloroplasts in situ have shown that they are spatially separated from each other 363
however the majority of the fluorescence signals originating from PSI overlap with 364
those from PSII (Hasegawa et al 2010) Thus in the case of CLSM images of bean 365
chloroplasts the LHCI-PSI complexes can be located both in red and dark areas but 366
the LHCII-PSII and LHCII trimers are located in red fluorescence regions only 367
368
13
(Stage 33) More developed grana 369
During the third day (stage 33) chloroplasts with grana more developed than in the 370
previous stage containing numerous thylakoids were observed (Figure 7) A 371
composite tomographic slice image was obtained as in the previously analyzed 372
stages (Figure 7A) The region of interest was drawn using the 3DMOD software 373
(Figure 7B middle slice from the stack) A model of the granum (light navy) with 374
connected STs (navy) was superimposed on the TEM image (Figures 7C and 7D) In 375
Figures 7E to 7I the model is shown from different angles to visualize direct 376
connections of STs with GTs The complexity of these connections can be observed 377
Some STs were associated with two neighboring GTs as in the previous stage and 378
were connected at an angle of approximately 18deg (Fig 7E and 7F) ST can also split 379
in a dichotomous manner and connect with both the adjacent GT and the next GT in 380
the other slice (left bottom ST Figures 7F and 7H) Additionally we saw that the ST in 381
the area of our model could connect with only one GT as was observed at the top 382
and bottom of the granum (Figure 7G) This shows that the junctional slits created by 383
the connections between GTs and STs can be of different widths as was also 384
reported by Austin and Staehelin for the thylakoid network of well-developed 385
chloroplasts of mature plants (Austin and Staehelin 2011) 386
For this stage the CLSM analysis was also performed The distribution of Chl 387
autofluorescence (Supplemental Figure 4) visible in CLSM changed drastically in 388
comparison to the earlier stage of grana formation Red spots corresponding to grana 389
were uniformly distributed within the chloroplast (Supplemental Figure 4A) 3D 390
models of the computer generated isosurface of Chl fluorescence confirmed the 391
regular distribution of grana that is characteristic of a mature chloroplast (Rumak et 392
al 2010) (Figures 4B to 4D) However the size of chloroplast at this stage of 393
biogenesis was much smaller (approximately 3 μm) than the 6 μm chloroplasts found 394
in mature plants 395
Based on the TEM sections of numerous developmental stages and also on the 396
reconstruction of the membrane transformation in 3D during the 7 stages of 397
chloroplast biogenesis we proposed a 2D theoretical model (Figure 8) of the 398
membrane changes The proposed theoretical model of membrane rearrangements 399
taken together with the 3D models allow us to create a dynamic model of chloroplast 400
development which is presented as a movie (Supplemental Movie 1) 401
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
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Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale genetic analysis of chloroplast biogenesis in maizeBiochim Biophys Acta 1847 1004-1016
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Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals theirsignificance in chloroplast development Photosynth Res 96 37-50
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The two spectroscopically different short wavelengthprotochlorophyllide forms in pea epicotyls are both monomeric Biochim Biophys Acta 1365 531-540
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast RNA polymerases Role in chloroplast biogenesisBiochim Biophys Acta 1847 761-769
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR (2010) Energy transfer processes in the isolated
core antenna complexes CP43 and CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606-1616Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain and loss of photosynthetic membranes duringplastid differentiation in the shoot apex of Arabidopsis Plant Cell 24 1143-1157
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar to cubic membrane transition as investigatedby electron microscopy Methods Cell Biol 108 319-343
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of thylakoid membranes in higher plant chloroplaststhe physicochemical forces at work and the functional consequences that ensue Photochem Photobiol Sci Off J EurPhotochem Assoc Eur Soc Photobiol 4 1081-1090
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DallOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting proteins Biochim Biophys Acta 1847 861-871Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) Quantification of photosystem I and II in different parts of thethylakoid membrane from spinach Biochim Biophys Acta 1608 53-61
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-M and Mamedov F (2006) Dimeric andmonomeric organization of photosystem II Distribution of five distinct complexes in the different domains of the thylakoidmembrane J Biol Chem 281 14241-14249
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid membranes J Exp Bot 62 2393-2402Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) Arrangement of photosystem II and ATP synthase inchloroplast membranes of spinach and pea Plant Cell 22 1299-1312
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants BiochimBiophys Acta 1706 12-39
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses subvert cholesterol homeostasis to induce host cubicmembranes Trends Cell Biol 20 371-379
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane structure in the mitochondria of amoebaeChaos carolinensis Protoplasma 20316-25
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA (1999) Cubic membrane structure in amoeba(Chaos carolinensis) mitochondria determined by electron microscopic tomography J Struct Biol 127 231-239
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister W (2015) Native architecture of theChlamydomonas chloroplast revealed by in situ cryo-electron tomography eLife 4
Pubmed Author and Title
CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gabruk M Stecka A Strzalka W Kruk J Strzalka K and Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzymecomplexes reconstituted with PORA PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS One 10e0116990
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes Biochim Biophys Acta 1837 481-494Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Grzyb JM Solymosi K Strzalka K and Mysliwa-Kurdziel B (2013) Visualization and characterization of prolamellar bodieswith atomic force microscopy J Plant Physiol 170 1217-1227
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (2001) Membrane geometry of open prolamellar bodies Protoplasma 215 4-15Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA FOLLOWING ALDEHYDE OSMIUM-TETROXIDEFIXATION J Cell Biol 24 79-93
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell (Edward Arnold London)
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective excitation of photosystems in chloroplasts inside plantleaves observed by near-infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225-238
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur R Garstka M Maksymiec W Kulik ADietler G and Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions astudy of lipid-light-harvesting complex II model membranes Plant Cell 25 2155-2170
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids Nat Rev Mol Cell Biol 14787-802
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems experimentally-investigated entropy-driven stackingof plant photosynthetic membranes Sci Rep 4 4142
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes BiochimBiophys Acta 1708 187-195
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
8
confocal laser scanning microscopy in later stages This enables visualization and 211
thus an understanding of the membrane connections during the key stages of 212
chloroplast biogenesis We correlate the 3D structure of PLBs and of the developing 213
bean thylakoid network with the formation of CP complexes 214
The results of our studies show that the transformation of PLBs consists of the 215
untwining of tubules from the PLB structure in a continuous process The tubular 216
structure of the prolamellar body transforms directly without dispersion into vesicles 217
into flat slats that eventually in a continuous way form grana We demonstrate that 218
grana membranes from the beginning of their formation associate with stroma 219
thylakoids in a helical way 220
221
RESULTS 222
Spatial Model of Chloroplast Biogenesis 223
To determine the spatial structure of successive stages of bean chloroplast 224
biogenesis during 3 daynight cycles both CLSM and ET were used Previous results 225
from ultrastructural analysis indicated that starting from 8 d-old etiolated plants 226
chloroplast development proceeds synchronously in all plastids (Rudowska et al 227
2012) 228
To establish the sequence of structural changes of the thylakoid network during 229
chloroplast biogenesis we followed the process of biogenesis step by step from the 230
paracrystalline structure of PLB to the stacked membranes observed in the 231
ultrastructure of bean chloroplasts For the electron tomography analysis seven 232
stages of plastid internal membrane arrangements were selected during the 233
photomorphogenesis as described in Methods (Supplemental Figure 1) 234
We focused on one hand on areas of membrane connections within tightly 235
organized tubular PLB structure and grana thylakoids and on the other hand on 236
areas of loosely organized structure with transforming PLBs with newly formed 237
thylakoids 3D modeling was performed from the stage of paracrystalline structure of 238
PLB to the stage of reorganization into first appressed thylakoids and formation of 239
more developed grana 240
9
Reconstruction of the very early stages of chloroplast development by CLSM was not 241
reliable due to the small dimensions and lack of red Chl fluorescence in early 242
developmental stages Because of this the images of the etioplast internal 243
membranes obtained with CLSM were not comparable with relevant structures on 244
electron micrographs Moreover the lipophilic dye (DiOC18(3)) that was used in these 245
early stages did not incorporate uniformly into the tight paracrystalline and 246
transforming PLB membranes causing imaging artefacts Therefore spatial models 247
obtained from CLSM were used only in the two latest analyzed stages of biogenesis 248
when the Chl autofluorescence of PSII was sufficiently stable and the dimensions of 249
chloroplasts were large enough 250
251
(Stage 10) Paracrystalline prolamellar body (PLB) 252
8 d-old etiolated bean leaves have etioplasts with characteristic paracrystalline 253
prolamellar bodies as was already shown by us and other researchers (Rudowska et 254
al 2012) Based on Gunning and Steer (1975) bean etioplast PLB is of a closed 255
type with hexagonal symmetry of the tubule arrangement The tetrahedrally branched 256
basic tubular units form a typical wurtzite (a zinc iron sulfide mineral) lattice For a 257
better comparison between the PLB structure and the theoretical model of a 258
hexagonal lattice we chose perpendicular sections of the closed-type PLB for ET 259
analysis (Supplemental Figure 2) 260
We found that the structure of the PLB was a regular tetrahedral arrangement of 261
tubular connections within the PLB (Figure 1) Such a composite tomographic image 262
stack was obtained by superimposing reconstructed parallel slices such as the one 263
shown in Figure 1A The volume of the PLB (Figure 1B) and isosurface visualization 264
of the 3D reconstruction of paracrystalline PLB membranes was generated (Figure 265
1C) with the help of Imaris microscopy image processing and analysis software In 266
Figures 1C and 1D the PLB volume together with the first layer of the PLB is visible 267
For better visualization of the PLB network we highlight a single unit (orange) of the 268
PLB together with the rendered volume (Figure 1E) An enlargement of the 269
isosurface of one unit is shown (Figure 1F) together with its side view (Figure 1G) In 270
Figure 1H the theoretical model created with the help of 3ds max software showing 271
the arrangement of inner plastid membranes within the prolamellar body is displayed 272
10
273
(Stage 11) Irregular prolamellar body 274
After 1 h of illumination the regularity and the symmetry of the PLB was lost The 275
structure of the PLB became irregular and PLB membranes became rearranged 276
(Figure 2) The 3D array of branched tubes in the PLB became dissociated and the 277
characteristic tetrahedral network was no longer visible and all units lost regular 278
connections with each other A composite tomographic slice image was obtained by 279
superimposing reconstructed parallel slices representing the spatial structure of an 280
irregular PLB and this composite image is shown in Figure 2A The volume (Figure 281
2B) and isosurface (Figures 2C to 2H) of an irregular PLB was rendered with the help 282
of Imaris software Already at this stage PLB membranes both within the PLB 283
(Figures 2E to 2H) and in its marginal regions (Figure 2D) had given rise to flat 284
stromal slats at the periphery of the PLB that were seen as porous PTs PTs were 285
tightly connected with the degrading PLB that were radially spreading from the PLB 286
margins (Figure 2C) In Figures 2C and 2D the isosurface of the irregular PLB 287
together with the outer layer of the PLB is visible Upon magnification the PTs 288
emerging from the degrading PLB are seen as flat slats (Figure 2D) For better 289
visualization of the transformation from tubular elements to slats a single unit of a 290
degrading PLB net (lime green) is shown from various directions (Figures 2E to 2H) 291
We strongly emphasize that electron tomography enabled the visualization of slat 292
arrangements during transformation and untwining of PLB nodes This was not 293
possible in traditional electron microscopy 294
295
(Stage 12) Remnants of PLB and numerous prothylakoids 296
After 2 h of illumination only remnants of the PLB were observed (Figure 3) A 297
composite tomographic slice image was obtained by superimposing reconstructed 298
parallel slices of remnants of the PLB and porous PTs connected with them (Figure 299
3A) The area of interest was drawn on every slice with the help of 3DMOD software 300
(Figure 3B the middle slice in the stack) We reconstructed a particular area of 301
chloroplast membranes focusing on connections between the remnants of the PLB 302
and the PTs This model was superimposed on a TEM image for better visualization 303
of the region of interest (blue) (Figures 3C and 3D) In Figures 3E to 3G slat-like 304
11
images of PTs are presented from different angles From these models we could 305
observe that the membranes that were remnants of the PLB had a continuous 306
character as opposed to the porous PT membranes that were tightly connected with 307
the former (Figures 3E to 3G) Both types of membrane were slat-like and not tubule-308
like structures At this stage of chloroplast biogenesis the inner membranes were 309
arranged in parallel to the long chloroplast axis 310
311
(Stage 14) Parallel prothylakoids 312
After 4 h of illumination there were no more remnants of PLBs in the bean 313
chloroplasts (Figure 4) A composite tomographic slice image was obtained by 314
superimposing reconstructed parallel slices of chloroplasts at this stage of 315
development (Figure 4A) A selected area of membranes was drawn with the help of 316
3DMOD software (Figure 4B middle slice from the stack) A model of the area of 317
interest was superimposed on a TEM image for better visualization (purple) (Figures 318
4C and 4D) In Figures 4E to 4G slat-like models of porous PTs are shown after 319
rotation and presented from different angles Such models enabled the visualization 320
of the parallel arrangement of PTs and the local connections between them The PTs 321
had a slat-like and porous character and some of them had split in a dichotomous 322
manner (Figures 4E to 4G) 323
324
(Stage 18) First stacked membranes 325
After 8 h of illumination the first stacked membranes were observed (Figure 5) A 326
composite tomographic slice image was obtained in a similar way as before (Figure 327
5A) Interesting areas of thylakoid membranes especially of stacked membranes and 328
their connections to unstacked ones were drawn using 3DMOD software (Figure 5B 329
middle slice from the stack) A model of the area of interest was superimposed on the 330
TEM image (Figures 5C and 5D) In Figures 5E to 5H models of the first stacked 331
membranes are shown after magnification and presented from different angles 332
These models revealed that the appressed thylakoids (light yellow) were no longer 333
porous but had continuous membranes in the stacked region From our constructed 334
model we learned that the PTs (yellow) remained still porous although to a lesser 335
extent than at earlier stages In this model each stacked membrane was connected 336
12
to a single split PT This dichotomous splitting existed only locally where a PT joined 337
with both the upper and lower stacked membrane The PT membrane connected with 338
the stacked region not in parallel but at an angle in the range of 18 to 33deg 339
340
(Stage 20) Small grana 341
At the beginning of the second day of the experiment (Figure 6) small grana stacks 342
were observed (stage 20) A composite tomographic slice image was obtained in a 343
similar way as for the other stages of biogenesis (Figure 6A) Grana thylakoids (GTs) 344
and stroma thylakoids (STs) connected with them were drawn using the 3DMOD 345
software (Figure 6B middle slice from the stack) A small grana model was 346
superimposed on the TEM image for a better visualization of the region of interest 347
(Figures 6C and 6D) The model shows GTs (light green) arranged in parallel and no-348
longer-porous STs (green) connected with them (Figure 6E) In Figures 6F to 6I the 349
models of GTs and STs are shown from different angles Every modelled ST was 350
connected with two adjacent GTs (Figures 6F and 6G) The STs were connected with 351
the stacked region at an angle of approximately 20deg 352
As mentioned previously a CLSM study was performed for the two latest stages of 353
chloroplast biogenesis The density of the red Chl fluorescence spots in a CLSM 354
image showed the distribution of the appressed thylakoids (grana) in the chloroplast 355
(Supplemental Figure 3) There was no visible regularity of the appressed thylakoid 356
distribution (Supplemental Figure 3A) that correlated with the TEM pictures Also 3D 357
models of the computer generated isosurface of Chl fluorescence (Supplemental 358
Figures 3B to 3D) confirmed the lack of regularity of grana location within a 359
chloroplast The red fluorescence originated from the LHCII-PSII supercomplexes 360
dimers and monomers and also from LHCII trimers that were not bound and 361
localized in grana (Mehta et al 1999) Selective images of PSI and PSII in plant 362
chloroplasts in situ have shown that they are spatially separated from each other 363
however the majority of the fluorescence signals originating from PSI overlap with 364
those from PSII (Hasegawa et al 2010) Thus in the case of CLSM images of bean 365
chloroplasts the LHCI-PSI complexes can be located both in red and dark areas but 366
the LHCII-PSII and LHCII trimers are located in red fluorescence regions only 367
368
13
(Stage 33) More developed grana 369
During the third day (stage 33) chloroplasts with grana more developed than in the 370
previous stage containing numerous thylakoids were observed (Figure 7) A 371
composite tomographic slice image was obtained as in the previously analyzed 372
stages (Figure 7A) The region of interest was drawn using the 3DMOD software 373
(Figure 7B middle slice from the stack) A model of the granum (light navy) with 374
connected STs (navy) was superimposed on the TEM image (Figures 7C and 7D) In 375
Figures 7E to 7I the model is shown from different angles to visualize direct 376
connections of STs with GTs The complexity of these connections can be observed 377
Some STs were associated with two neighboring GTs as in the previous stage and 378
were connected at an angle of approximately 18deg (Fig 7E and 7F) ST can also split 379
in a dichotomous manner and connect with both the adjacent GT and the next GT in 380
the other slice (left bottom ST Figures 7F and 7H) Additionally we saw that the ST in 381
the area of our model could connect with only one GT as was observed at the top 382
and bottom of the granum (Figure 7G) This shows that the junctional slits created by 383
the connections between GTs and STs can be of different widths as was also 384
reported by Austin and Staehelin for the thylakoid network of well-developed 385
chloroplasts of mature plants (Austin and Staehelin 2011) 386
For this stage the CLSM analysis was also performed The distribution of Chl 387
autofluorescence (Supplemental Figure 4) visible in CLSM changed drastically in 388
comparison to the earlier stage of grana formation Red spots corresponding to grana 389
were uniformly distributed within the chloroplast (Supplemental Figure 4A) 3D 390
models of the computer generated isosurface of Chl fluorescence confirmed the 391
regular distribution of grana that is characteristic of a mature chloroplast (Rumak et 392
al 2010) (Figures 4B to 4D) However the size of chloroplast at this stage of 393
biogenesis was much smaller (approximately 3 μm) than the 6 μm chloroplasts found 394
in mature plants 395
Based on the TEM sections of numerous developmental stages and also on the 396
reconstruction of the membrane transformation in 3D during the 7 stages of 397
chloroplast biogenesis we proposed a 2D theoretical model (Figure 8) of the 398
membrane changes The proposed theoretical model of membrane rearrangements 399
taken together with the 3D models allow us to create a dynamic model of chloroplast 400
development which is presented as a movie (Supplemental Movie 1) 401
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
Parsed CitationsAbdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) High salt stress induces swollen prothylakoids indark-grown wheat and alters both prolamellar body transformation and reformation after irradiation J Exp Bot 58 2553-2564
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ Biophotonics International 11 36-42Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of thylakoid networks in angiosperms knowns andunknowns Plant Mol Biol 76 221-234
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend beyond the Flatland of cell membraneorganization J Cell Biol 173 839-844
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic membranes the missing dimension of cellmembrane organization Int Rev Cell Mol Biol 274 275-342
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the structure and function of photosystem II in higherplant thylakoid membranes the grana enigma Photosynth Res 98 575-587
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R and Dekker JP (2005) Origin of the F685 andF695 fluorescence in photosystem II Photosynth Res 84 173-180
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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9
Reconstruction of the very early stages of chloroplast development by CLSM was not 241
reliable due to the small dimensions and lack of red Chl fluorescence in early 242
developmental stages Because of this the images of the etioplast internal 243
membranes obtained with CLSM were not comparable with relevant structures on 244
electron micrographs Moreover the lipophilic dye (DiOC18(3)) that was used in these 245
early stages did not incorporate uniformly into the tight paracrystalline and 246
transforming PLB membranes causing imaging artefacts Therefore spatial models 247
obtained from CLSM were used only in the two latest analyzed stages of biogenesis 248
when the Chl autofluorescence of PSII was sufficiently stable and the dimensions of 249
chloroplasts were large enough 250
251
(Stage 10) Paracrystalline prolamellar body (PLB) 252
8 d-old etiolated bean leaves have etioplasts with characteristic paracrystalline 253
prolamellar bodies as was already shown by us and other researchers (Rudowska et 254
al 2012) Based on Gunning and Steer (1975) bean etioplast PLB is of a closed 255
type with hexagonal symmetry of the tubule arrangement The tetrahedrally branched 256
basic tubular units form a typical wurtzite (a zinc iron sulfide mineral) lattice For a 257
better comparison between the PLB structure and the theoretical model of a 258
hexagonal lattice we chose perpendicular sections of the closed-type PLB for ET 259
analysis (Supplemental Figure 2) 260
We found that the structure of the PLB was a regular tetrahedral arrangement of 261
tubular connections within the PLB (Figure 1) Such a composite tomographic image 262
stack was obtained by superimposing reconstructed parallel slices such as the one 263
shown in Figure 1A The volume of the PLB (Figure 1B) and isosurface visualization 264
of the 3D reconstruction of paracrystalline PLB membranes was generated (Figure 265
1C) with the help of Imaris microscopy image processing and analysis software In 266
Figures 1C and 1D the PLB volume together with the first layer of the PLB is visible 267
For better visualization of the PLB network we highlight a single unit (orange) of the 268
PLB together with the rendered volume (Figure 1E) An enlargement of the 269
isosurface of one unit is shown (Figure 1F) together with its side view (Figure 1G) In 270
Figure 1H the theoretical model created with the help of 3ds max software showing 271
the arrangement of inner plastid membranes within the prolamellar body is displayed 272
10
273
(Stage 11) Irregular prolamellar body 274
After 1 h of illumination the regularity and the symmetry of the PLB was lost The 275
structure of the PLB became irregular and PLB membranes became rearranged 276
(Figure 2) The 3D array of branched tubes in the PLB became dissociated and the 277
characteristic tetrahedral network was no longer visible and all units lost regular 278
connections with each other A composite tomographic slice image was obtained by 279
superimposing reconstructed parallel slices representing the spatial structure of an 280
irregular PLB and this composite image is shown in Figure 2A The volume (Figure 281
2B) and isosurface (Figures 2C to 2H) of an irregular PLB was rendered with the help 282
of Imaris software Already at this stage PLB membranes both within the PLB 283
(Figures 2E to 2H) and in its marginal regions (Figure 2D) had given rise to flat 284
stromal slats at the periphery of the PLB that were seen as porous PTs PTs were 285
tightly connected with the degrading PLB that were radially spreading from the PLB 286
margins (Figure 2C) In Figures 2C and 2D the isosurface of the irregular PLB 287
together with the outer layer of the PLB is visible Upon magnification the PTs 288
emerging from the degrading PLB are seen as flat slats (Figure 2D) For better 289
visualization of the transformation from tubular elements to slats a single unit of a 290
degrading PLB net (lime green) is shown from various directions (Figures 2E to 2H) 291
We strongly emphasize that electron tomography enabled the visualization of slat 292
arrangements during transformation and untwining of PLB nodes This was not 293
possible in traditional electron microscopy 294
295
(Stage 12) Remnants of PLB and numerous prothylakoids 296
After 2 h of illumination only remnants of the PLB were observed (Figure 3) A 297
composite tomographic slice image was obtained by superimposing reconstructed 298
parallel slices of remnants of the PLB and porous PTs connected with them (Figure 299
3A) The area of interest was drawn on every slice with the help of 3DMOD software 300
(Figure 3B the middle slice in the stack) We reconstructed a particular area of 301
chloroplast membranes focusing on connections between the remnants of the PLB 302
and the PTs This model was superimposed on a TEM image for better visualization 303
of the region of interest (blue) (Figures 3C and 3D) In Figures 3E to 3G slat-like 304
11
images of PTs are presented from different angles From these models we could 305
observe that the membranes that were remnants of the PLB had a continuous 306
character as opposed to the porous PT membranes that were tightly connected with 307
the former (Figures 3E to 3G) Both types of membrane were slat-like and not tubule-308
like structures At this stage of chloroplast biogenesis the inner membranes were 309
arranged in parallel to the long chloroplast axis 310
311
(Stage 14) Parallel prothylakoids 312
After 4 h of illumination there were no more remnants of PLBs in the bean 313
chloroplasts (Figure 4) A composite tomographic slice image was obtained by 314
superimposing reconstructed parallel slices of chloroplasts at this stage of 315
development (Figure 4A) A selected area of membranes was drawn with the help of 316
3DMOD software (Figure 4B middle slice from the stack) A model of the area of 317
interest was superimposed on a TEM image for better visualization (purple) (Figures 318
4C and 4D) In Figures 4E to 4G slat-like models of porous PTs are shown after 319
rotation and presented from different angles Such models enabled the visualization 320
of the parallel arrangement of PTs and the local connections between them The PTs 321
had a slat-like and porous character and some of them had split in a dichotomous 322
manner (Figures 4E to 4G) 323
324
(Stage 18) First stacked membranes 325
After 8 h of illumination the first stacked membranes were observed (Figure 5) A 326
composite tomographic slice image was obtained in a similar way as before (Figure 327
5A) Interesting areas of thylakoid membranes especially of stacked membranes and 328
their connections to unstacked ones were drawn using 3DMOD software (Figure 5B 329
middle slice from the stack) A model of the area of interest was superimposed on the 330
TEM image (Figures 5C and 5D) In Figures 5E to 5H models of the first stacked 331
membranes are shown after magnification and presented from different angles 332
These models revealed that the appressed thylakoids (light yellow) were no longer 333
porous but had continuous membranes in the stacked region From our constructed 334
model we learned that the PTs (yellow) remained still porous although to a lesser 335
extent than at earlier stages In this model each stacked membrane was connected 336
12
to a single split PT This dichotomous splitting existed only locally where a PT joined 337
with both the upper and lower stacked membrane The PT membrane connected with 338
the stacked region not in parallel but at an angle in the range of 18 to 33deg 339
340
(Stage 20) Small grana 341
At the beginning of the second day of the experiment (Figure 6) small grana stacks 342
were observed (stage 20) A composite tomographic slice image was obtained in a 343
similar way as for the other stages of biogenesis (Figure 6A) Grana thylakoids (GTs) 344
and stroma thylakoids (STs) connected with them were drawn using the 3DMOD 345
software (Figure 6B middle slice from the stack) A small grana model was 346
superimposed on the TEM image for a better visualization of the region of interest 347
(Figures 6C and 6D) The model shows GTs (light green) arranged in parallel and no-348
longer-porous STs (green) connected with them (Figure 6E) In Figures 6F to 6I the 349
models of GTs and STs are shown from different angles Every modelled ST was 350
connected with two adjacent GTs (Figures 6F and 6G) The STs were connected with 351
the stacked region at an angle of approximately 20deg 352
As mentioned previously a CLSM study was performed for the two latest stages of 353
chloroplast biogenesis The density of the red Chl fluorescence spots in a CLSM 354
image showed the distribution of the appressed thylakoids (grana) in the chloroplast 355
(Supplemental Figure 3) There was no visible regularity of the appressed thylakoid 356
distribution (Supplemental Figure 3A) that correlated with the TEM pictures Also 3D 357
models of the computer generated isosurface of Chl fluorescence (Supplemental 358
Figures 3B to 3D) confirmed the lack of regularity of grana location within a 359
chloroplast The red fluorescence originated from the LHCII-PSII supercomplexes 360
dimers and monomers and also from LHCII trimers that were not bound and 361
localized in grana (Mehta et al 1999) Selective images of PSI and PSII in plant 362
chloroplasts in situ have shown that they are spatially separated from each other 363
however the majority of the fluorescence signals originating from PSI overlap with 364
those from PSII (Hasegawa et al 2010) Thus in the case of CLSM images of bean 365
chloroplasts the LHCI-PSI complexes can be located both in red and dark areas but 366
the LHCII-PSII and LHCII trimers are located in red fluorescence regions only 367
368
13
(Stage 33) More developed grana 369
During the third day (stage 33) chloroplasts with grana more developed than in the 370
previous stage containing numerous thylakoids were observed (Figure 7) A 371
composite tomographic slice image was obtained as in the previously analyzed 372
stages (Figure 7A) The region of interest was drawn using the 3DMOD software 373
(Figure 7B middle slice from the stack) A model of the granum (light navy) with 374
connected STs (navy) was superimposed on the TEM image (Figures 7C and 7D) In 375
Figures 7E to 7I the model is shown from different angles to visualize direct 376
connections of STs with GTs The complexity of these connections can be observed 377
Some STs were associated with two neighboring GTs as in the previous stage and 378
were connected at an angle of approximately 18deg (Fig 7E and 7F) ST can also split 379
in a dichotomous manner and connect with both the adjacent GT and the next GT in 380
the other slice (left bottom ST Figures 7F and 7H) Additionally we saw that the ST in 381
the area of our model could connect with only one GT as was observed at the top 382
and bottom of the granum (Figure 7G) This shows that the junctional slits created by 383
the connections between GTs and STs can be of different widths as was also 384
reported by Austin and Staehelin for the thylakoid network of well-developed 385
chloroplasts of mature plants (Austin and Staehelin 2011) 386
For this stage the CLSM analysis was also performed The distribution of Chl 387
autofluorescence (Supplemental Figure 4) visible in CLSM changed drastically in 388
comparison to the earlier stage of grana formation Red spots corresponding to grana 389
were uniformly distributed within the chloroplast (Supplemental Figure 4A) 3D 390
models of the computer generated isosurface of Chl fluorescence confirmed the 391
regular distribution of grana that is characteristic of a mature chloroplast (Rumak et 392
al 2010) (Figures 4B to 4D) However the size of chloroplast at this stage of 393
biogenesis was much smaller (approximately 3 μm) than the 6 μm chloroplasts found 394
in mature plants 395
Based on the TEM sections of numerous developmental stages and also on the 396
reconstruction of the membrane transformation in 3D during the 7 stages of 397
chloroplast biogenesis we proposed a 2D theoretical model (Figure 8) of the 398
membrane changes The proposed theoretical model of membrane rearrangements 399
taken together with the 3D models allow us to create a dynamic model of chloroplast 400
development which is presented as a movie (Supplemental Movie 1) 401
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
10
273
(Stage 11) Irregular prolamellar body 274
After 1 h of illumination the regularity and the symmetry of the PLB was lost The 275
structure of the PLB became irregular and PLB membranes became rearranged 276
(Figure 2) The 3D array of branched tubes in the PLB became dissociated and the 277
characteristic tetrahedral network was no longer visible and all units lost regular 278
connections with each other A composite tomographic slice image was obtained by 279
superimposing reconstructed parallel slices representing the spatial structure of an 280
irregular PLB and this composite image is shown in Figure 2A The volume (Figure 281
2B) and isosurface (Figures 2C to 2H) of an irregular PLB was rendered with the help 282
of Imaris software Already at this stage PLB membranes both within the PLB 283
(Figures 2E to 2H) and in its marginal regions (Figure 2D) had given rise to flat 284
stromal slats at the periphery of the PLB that were seen as porous PTs PTs were 285
tightly connected with the degrading PLB that were radially spreading from the PLB 286
margins (Figure 2C) In Figures 2C and 2D the isosurface of the irregular PLB 287
together with the outer layer of the PLB is visible Upon magnification the PTs 288
emerging from the degrading PLB are seen as flat slats (Figure 2D) For better 289
visualization of the transformation from tubular elements to slats a single unit of a 290
degrading PLB net (lime green) is shown from various directions (Figures 2E to 2H) 291
We strongly emphasize that electron tomography enabled the visualization of slat 292
arrangements during transformation and untwining of PLB nodes This was not 293
possible in traditional electron microscopy 294
295
(Stage 12) Remnants of PLB and numerous prothylakoids 296
After 2 h of illumination only remnants of the PLB were observed (Figure 3) A 297
composite tomographic slice image was obtained by superimposing reconstructed 298
parallel slices of remnants of the PLB and porous PTs connected with them (Figure 299
3A) The area of interest was drawn on every slice with the help of 3DMOD software 300
(Figure 3B the middle slice in the stack) We reconstructed a particular area of 301
chloroplast membranes focusing on connections between the remnants of the PLB 302
and the PTs This model was superimposed on a TEM image for better visualization 303
of the region of interest (blue) (Figures 3C and 3D) In Figures 3E to 3G slat-like 304
11
images of PTs are presented from different angles From these models we could 305
observe that the membranes that were remnants of the PLB had a continuous 306
character as opposed to the porous PT membranes that were tightly connected with 307
the former (Figures 3E to 3G) Both types of membrane were slat-like and not tubule-308
like structures At this stage of chloroplast biogenesis the inner membranes were 309
arranged in parallel to the long chloroplast axis 310
311
(Stage 14) Parallel prothylakoids 312
After 4 h of illumination there were no more remnants of PLBs in the bean 313
chloroplasts (Figure 4) A composite tomographic slice image was obtained by 314
superimposing reconstructed parallel slices of chloroplasts at this stage of 315
development (Figure 4A) A selected area of membranes was drawn with the help of 316
3DMOD software (Figure 4B middle slice from the stack) A model of the area of 317
interest was superimposed on a TEM image for better visualization (purple) (Figures 318
4C and 4D) In Figures 4E to 4G slat-like models of porous PTs are shown after 319
rotation and presented from different angles Such models enabled the visualization 320
of the parallel arrangement of PTs and the local connections between them The PTs 321
had a slat-like and porous character and some of them had split in a dichotomous 322
manner (Figures 4E to 4G) 323
324
(Stage 18) First stacked membranes 325
After 8 h of illumination the first stacked membranes were observed (Figure 5) A 326
composite tomographic slice image was obtained in a similar way as before (Figure 327
5A) Interesting areas of thylakoid membranes especially of stacked membranes and 328
their connections to unstacked ones were drawn using 3DMOD software (Figure 5B 329
middle slice from the stack) A model of the area of interest was superimposed on the 330
TEM image (Figures 5C and 5D) In Figures 5E to 5H models of the first stacked 331
membranes are shown after magnification and presented from different angles 332
These models revealed that the appressed thylakoids (light yellow) were no longer 333
porous but had continuous membranes in the stacked region From our constructed 334
model we learned that the PTs (yellow) remained still porous although to a lesser 335
extent than at earlier stages In this model each stacked membrane was connected 336
12
to a single split PT This dichotomous splitting existed only locally where a PT joined 337
with both the upper and lower stacked membrane The PT membrane connected with 338
the stacked region not in parallel but at an angle in the range of 18 to 33deg 339
340
(Stage 20) Small grana 341
At the beginning of the second day of the experiment (Figure 6) small grana stacks 342
were observed (stage 20) A composite tomographic slice image was obtained in a 343
similar way as for the other stages of biogenesis (Figure 6A) Grana thylakoids (GTs) 344
and stroma thylakoids (STs) connected with them were drawn using the 3DMOD 345
software (Figure 6B middle slice from the stack) A small grana model was 346
superimposed on the TEM image for a better visualization of the region of interest 347
(Figures 6C and 6D) The model shows GTs (light green) arranged in parallel and no-348
longer-porous STs (green) connected with them (Figure 6E) In Figures 6F to 6I the 349
models of GTs and STs are shown from different angles Every modelled ST was 350
connected with two adjacent GTs (Figures 6F and 6G) The STs were connected with 351
the stacked region at an angle of approximately 20deg 352
As mentioned previously a CLSM study was performed for the two latest stages of 353
chloroplast biogenesis The density of the red Chl fluorescence spots in a CLSM 354
image showed the distribution of the appressed thylakoids (grana) in the chloroplast 355
(Supplemental Figure 3) There was no visible regularity of the appressed thylakoid 356
distribution (Supplemental Figure 3A) that correlated with the TEM pictures Also 3D 357
models of the computer generated isosurface of Chl fluorescence (Supplemental 358
Figures 3B to 3D) confirmed the lack of regularity of grana location within a 359
chloroplast The red fluorescence originated from the LHCII-PSII supercomplexes 360
dimers and monomers and also from LHCII trimers that were not bound and 361
localized in grana (Mehta et al 1999) Selective images of PSI and PSII in plant 362
chloroplasts in situ have shown that they are spatially separated from each other 363
however the majority of the fluorescence signals originating from PSI overlap with 364
those from PSII (Hasegawa et al 2010) Thus in the case of CLSM images of bean 365
chloroplasts the LHCI-PSI complexes can be located both in red and dark areas but 366
the LHCII-PSII and LHCII trimers are located in red fluorescence regions only 367
368
13
(Stage 33) More developed grana 369
During the third day (stage 33) chloroplasts with grana more developed than in the 370
previous stage containing numerous thylakoids were observed (Figure 7) A 371
composite tomographic slice image was obtained as in the previously analyzed 372
stages (Figure 7A) The region of interest was drawn using the 3DMOD software 373
(Figure 7B middle slice from the stack) A model of the granum (light navy) with 374
connected STs (navy) was superimposed on the TEM image (Figures 7C and 7D) In 375
Figures 7E to 7I the model is shown from different angles to visualize direct 376
connections of STs with GTs The complexity of these connections can be observed 377
Some STs were associated with two neighboring GTs as in the previous stage and 378
were connected at an angle of approximately 18deg (Fig 7E and 7F) ST can also split 379
in a dichotomous manner and connect with both the adjacent GT and the next GT in 380
the other slice (left bottom ST Figures 7F and 7H) Additionally we saw that the ST in 381
the area of our model could connect with only one GT as was observed at the top 382
and bottom of the granum (Figure 7G) This shows that the junctional slits created by 383
the connections between GTs and STs can be of different widths as was also 384
reported by Austin and Staehelin for the thylakoid network of well-developed 385
chloroplasts of mature plants (Austin and Staehelin 2011) 386
For this stage the CLSM analysis was also performed The distribution of Chl 387
autofluorescence (Supplemental Figure 4) visible in CLSM changed drastically in 388
comparison to the earlier stage of grana formation Red spots corresponding to grana 389
were uniformly distributed within the chloroplast (Supplemental Figure 4A) 3D 390
models of the computer generated isosurface of Chl fluorescence confirmed the 391
regular distribution of grana that is characteristic of a mature chloroplast (Rumak et 392
al 2010) (Figures 4B to 4D) However the size of chloroplast at this stage of 393
biogenesis was much smaller (approximately 3 μm) than the 6 μm chloroplasts found 394
in mature plants 395
Based on the TEM sections of numerous developmental stages and also on the 396
reconstruction of the membrane transformation in 3D during the 7 stages of 397
chloroplast biogenesis we proposed a 2D theoretical model (Figure 8) of the 398
membrane changes The proposed theoretical model of membrane rearrangements 399
taken together with the 3D models allow us to create a dynamic model of chloroplast 400
development which is presented as a movie (Supplemental Movie 1) 401
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
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Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
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Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
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Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
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Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems experimentally-investigated entropy-driven stackingof plant photosynthetic membranes Sci Rep 4 4142
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Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes BiochimBiophys Acta 1708 187-195
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Google Scholar Author Only Title Only Author and Title
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
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Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
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Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P Gruissem W and Baginsky S (2007)Proteome dynamics during plastid differentiation in rice Plant Physiol 143 912-923
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED ANDFAR-RED LIGHT J Cell Biol 22 433-442
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV Dekker JP and Jansson S (2005) Structureof the higher plant light harvesting complex I in vivo characterization and structural interdependence of the Lhca proteinsBiochemistry (Mosc) 44 3065-3073
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) Protein assembly and heat stability in developingthylakoid membranes during greening Proc Natl Acad Sci U S A 99 12149-12154
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Kouril R Dekker JP and Boekema EJ (2012) Supramolecular organization of photosystem II in green plants BiochimBiophys Acta 1817 2-12
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Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization of Three-Dimensional Image Data Using IMODJ Struct Biol 116 71-76
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Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 655-659
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-proteasome system in plastid developmentBiochim Biophys Acta 1847 939-948
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 58 11-26Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid membranes from plastid transcription to proteincomplex assembly Planta 237 413-428
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Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology Second Edition (CRC Press)
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography software for three-dimensional reconstructionin transmission electron microscopy BMC Bioinformatics 8 288
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Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings by white red and blue low intensity lightProtoplasma 131 166-173
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986b) Thylakoid and grana formation during the development of pea chloroplasts illuminated by white red andblue low intensity light Protoplasma 134 88-94
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mysliwa-Kurdziel B Kruk J and Strzalka K (2013) Protochlorophyllide in model systems--an approach to in vivo conditionsBiophys Chem 175-176 28-38
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture and dynamics of the photosynthetic apparatus inhigher plants Plant J Cell Mol Biol 70 157-176
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts J Cell Sci 6 243-255Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) Identification of the carotenoid isomerase providesinsight into carotenoid biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 321-332
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Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development an overview Plant Physiol155 1545-1551
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Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast biogenesis and development Biochim BiophysActa
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in land plants J Exp Bot 65 1955-1972Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes Biochim Biophys Acta BBA - Bioenerg 1847 821-830
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Google Scholar Author Only Title Only Author and Title
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
11
images of PTs are presented from different angles From these models we could 305
observe that the membranes that were remnants of the PLB had a continuous 306
character as opposed to the porous PT membranes that were tightly connected with 307
the former (Figures 3E to 3G) Both types of membrane were slat-like and not tubule-308
like structures At this stage of chloroplast biogenesis the inner membranes were 309
arranged in parallel to the long chloroplast axis 310
311
(Stage 14) Parallel prothylakoids 312
After 4 h of illumination there were no more remnants of PLBs in the bean 313
chloroplasts (Figure 4) A composite tomographic slice image was obtained by 314
superimposing reconstructed parallel slices of chloroplasts at this stage of 315
development (Figure 4A) A selected area of membranes was drawn with the help of 316
3DMOD software (Figure 4B middle slice from the stack) A model of the area of 317
interest was superimposed on a TEM image for better visualization (purple) (Figures 318
4C and 4D) In Figures 4E to 4G slat-like models of porous PTs are shown after 319
rotation and presented from different angles Such models enabled the visualization 320
of the parallel arrangement of PTs and the local connections between them The PTs 321
had a slat-like and porous character and some of them had split in a dichotomous 322
manner (Figures 4E to 4G) 323
324
(Stage 18) First stacked membranes 325
After 8 h of illumination the first stacked membranes were observed (Figure 5) A 326
composite tomographic slice image was obtained in a similar way as before (Figure 327
5A) Interesting areas of thylakoid membranes especially of stacked membranes and 328
their connections to unstacked ones were drawn using 3DMOD software (Figure 5B 329
middle slice from the stack) A model of the area of interest was superimposed on the 330
TEM image (Figures 5C and 5D) In Figures 5E to 5H models of the first stacked 331
membranes are shown after magnification and presented from different angles 332
These models revealed that the appressed thylakoids (light yellow) were no longer 333
porous but had continuous membranes in the stacked region From our constructed 334
model we learned that the PTs (yellow) remained still porous although to a lesser 335
extent than at earlier stages In this model each stacked membrane was connected 336
12
to a single split PT This dichotomous splitting existed only locally where a PT joined 337
with both the upper and lower stacked membrane The PT membrane connected with 338
the stacked region not in parallel but at an angle in the range of 18 to 33deg 339
340
(Stage 20) Small grana 341
At the beginning of the second day of the experiment (Figure 6) small grana stacks 342
were observed (stage 20) A composite tomographic slice image was obtained in a 343
similar way as for the other stages of biogenesis (Figure 6A) Grana thylakoids (GTs) 344
and stroma thylakoids (STs) connected with them were drawn using the 3DMOD 345
software (Figure 6B middle slice from the stack) A small grana model was 346
superimposed on the TEM image for a better visualization of the region of interest 347
(Figures 6C and 6D) The model shows GTs (light green) arranged in parallel and no-348
longer-porous STs (green) connected with them (Figure 6E) In Figures 6F to 6I the 349
models of GTs and STs are shown from different angles Every modelled ST was 350
connected with two adjacent GTs (Figures 6F and 6G) The STs were connected with 351
the stacked region at an angle of approximately 20deg 352
As mentioned previously a CLSM study was performed for the two latest stages of 353
chloroplast biogenesis The density of the red Chl fluorescence spots in a CLSM 354
image showed the distribution of the appressed thylakoids (grana) in the chloroplast 355
(Supplemental Figure 3) There was no visible regularity of the appressed thylakoid 356
distribution (Supplemental Figure 3A) that correlated with the TEM pictures Also 3D 357
models of the computer generated isosurface of Chl fluorescence (Supplemental 358
Figures 3B to 3D) confirmed the lack of regularity of grana location within a 359
chloroplast The red fluorescence originated from the LHCII-PSII supercomplexes 360
dimers and monomers and also from LHCII trimers that were not bound and 361
localized in grana (Mehta et al 1999) Selective images of PSI and PSII in plant 362
chloroplasts in situ have shown that they are spatially separated from each other 363
however the majority of the fluorescence signals originating from PSI overlap with 364
those from PSII (Hasegawa et al 2010) Thus in the case of CLSM images of bean 365
chloroplasts the LHCI-PSI complexes can be located both in red and dark areas but 366
the LHCII-PSII and LHCII trimers are located in red fluorescence regions only 367
368
13
(Stage 33) More developed grana 369
During the third day (stage 33) chloroplasts with grana more developed than in the 370
previous stage containing numerous thylakoids were observed (Figure 7) A 371
composite tomographic slice image was obtained as in the previously analyzed 372
stages (Figure 7A) The region of interest was drawn using the 3DMOD software 373
(Figure 7B middle slice from the stack) A model of the granum (light navy) with 374
connected STs (navy) was superimposed on the TEM image (Figures 7C and 7D) In 375
Figures 7E to 7I the model is shown from different angles to visualize direct 376
connections of STs with GTs The complexity of these connections can be observed 377
Some STs were associated with two neighboring GTs as in the previous stage and 378
were connected at an angle of approximately 18deg (Fig 7E and 7F) ST can also split 379
in a dichotomous manner and connect with both the adjacent GT and the next GT in 380
the other slice (left bottom ST Figures 7F and 7H) Additionally we saw that the ST in 381
the area of our model could connect with only one GT as was observed at the top 382
and bottom of the granum (Figure 7G) This shows that the junctional slits created by 383
the connections between GTs and STs can be of different widths as was also 384
reported by Austin and Staehelin for the thylakoid network of well-developed 385
chloroplasts of mature plants (Austin and Staehelin 2011) 386
For this stage the CLSM analysis was also performed The distribution of Chl 387
autofluorescence (Supplemental Figure 4) visible in CLSM changed drastically in 388
comparison to the earlier stage of grana formation Red spots corresponding to grana 389
were uniformly distributed within the chloroplast (Supplemental Figure 4A) 3D 390
models of the computer generated isosurface of Chl fluorescence confirmed the 391
regular distribution of grana that is characteristic of a mature chloroplast (Rumak et 392
al 2010) (Figures 4B to 4D) However the size of chloroplast at this stage of 393
biogenesis was much smaller (approximately 3 μm) than the 6 μm chloroplasts found 394
in mature plants 395
Based on the TEM sections of numerous developmental stages and also on the 396
reconstruction of the membrane transformation in 3D during the 7 stages of 397
chloroplast biogenesis we proposed a 2D theoretical model (Figure 8) of the 398
membrane changes The proposed theoretical model of membrane rearrangements 399
taken together with the 3D models allow us to create a dynamic model of chloroplast 400
development which is presented as a movie (Supplemental Movie 1) 401
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
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Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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Danielsson R Albertsson P-A Mamedov F and Styring S (2004) Quantification of photosystem I and II in different parts of thethylakoid membrane from spinach Biochim Biophys Acta 1608 53-61
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Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-M and Mamedov F (2006) Dimeric andmonomeric organization of photosystem II Distribution of five distinct complexes in the different domains of the thylakoidmembrane J Biol Chem 281 14241-14249
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Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid membranes J Exp Bot 62 2393-2402Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) Arrangement of photosystem II and ATP synthase inchloroplast membranes of spinach and pea Plant Cell 22 1299-1312
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Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants BiochimBiophys Acta 1706 12-39
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Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses subvert cholesterol homeostasis to induce host cubicmembranes Trends Cell Biol 20 371-379
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane structure in the mitochondria of amoebaeChaos carolinensis Protoplasma 20316-25
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA (1999) Cubic membrane structure in amoeba(Chaos carolinensis) mitochondria determined by electron microscopic tomography J Struct Biol 127 231-239
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister W (2015) Native architecture of theChlamydomonas chloroplast revealed by in situ cryo-electron tomography eLife 4
Pubmed Author and Title
CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gabruk M Stecka A Strzalka W Kruk J Strzalka K and Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzymecomplexes reconstituted with PORA PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS One 10e0116990
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes Biochim Biophys Acta 1837 481-494Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
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Grzyb JM Solymosi K Strzalka K and Mysliwa-Kurdziel B (2013) Visualization and characterization of prolamellar bodieswith atomic force microscopy J Plant Physiol 170 1217-1227
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Gunning BE (2001) Membrane geometry of open prolamellar bodies Protoplasma 215 4-15Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA FOLLOWING ALDEHYDE OSMIUM-TETROXIDEFIXATION J Cell Biol 24 79-93
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell (Edward Arnold London)
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective excitation of photosystems in chloroplasts inside plantleaves observed by near-infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225-238
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur R Garstka M Maksymiec W Kulik ADietler G and Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions astudy of lipid-light-harvesting complex II model membranes Plant Cell 25 2155-2170
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids Nat Rev Mol Cell Biol 14787-802
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems experimentally-investigated entropy-driven stackingof plant photosynthetic membranes Sci Rep 4 4142
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes BiochimBiophys Acta 1708 187-195
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P Gruissem W and Baginsky S (2007)Proteome dynamics during plastid differentiation in rice Plant Physiol 143 912-923
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED ANDFAR-RED LIGHT J Cell Biol 22 433-442
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV Dekker JP and Jansson S (2005) Structureof the higher plant light harvesting complex I in vivo characterization and structural interdependence of the Lhca proteinsBiochemistry (Mosc) 44 3065-3073
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) Protein assembly and heat stability in developingthylakoid membranes during greening Proc Natl Acad Sci U S A 99 12149-12154
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kouril R Dekker JP and Boekema EJ (2012) Supramolecular organization of photosystem II in green plants BiochimBiophys Acta 1817 2-12
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization of Three-Dimensional Image Data Using IMODJ Struct Biol 116 71-76
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 655-659
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
12
to a single split PT This dichotomous splitting existed only locally where a PT joined 337
with both the upper and lower stacked membrane The PT membrane connected with 338
the stacked region not in parallel but at an angle in the range of 18 to 33deg 339
340
(Stage 20) Small grana 341
At the beginning of the second day of the experiment (Figure 6) small grana stacks 342
were observed (stage 20) A composite tomographic slice image was obtained in a 343
similar way as for the other stages of biogenesis (Figure 6A) Grana thylakoids (GTs) 344
and stroma thylakoids (STs) connected with them were drawn using the 3DMOD 345
software (Figure 6B middle slice from the stack) A small grana model was 346
superimposed on the TEM image for a better visualization of the region of interest 347
(Figures 6C and 6D) The model shows GTs (light green) arranged in parallel and no-348
longer-porous STs (green) connected with them (Figure 6E) In Figures 6F to 6I the 349
models of GTs and STs are shown from different angles Every modelled ST was 350
connected with two adjacent GTs (Figures 6F and 6G) The STs were connected with 351
the stacked region at an angle of approximately 20deg 352
As mentioned previously a CLSM study was performed for the two latest stages of 353
chloroplast biogenesis The density of the red Chl fluorescence spots in a CLSM 354
image showed the distribution of the appressed thylakoids (grana) in the chloroplast 355
(Supplemental Figure 3) There was no visible regularity of the appressed thylakoid 356
distribution (Supplemental Figure 3A) that correlated with the TEM pictures Also 3D 357
models of the computer generated isosurface of Chl fluorescence (Supplemental 358
Figures 3B to 3D) confirmed the lack of regularity of grana location within a 359
chloroplast The red fluorescence originated from the LHCII-PSII supercomplexes 360
dimers and monomers and also from LHCII trimers that were not bound and 361
localized in grana (Mehta et al 1999) Selective images of PSI and PSII in plant 362
chloroplasts in situ have shown that they are spatially separated from each other 363
however the majority of the fluorescence signals originating from PSI overlap with 364
those from PSII (Hasegawa et al 2010) Thus in the case of CLSM images of bean 365
chloroplasts the LHCI-PSI complexes can be located both in red and dark areas but 366
the LHCII-PSII and LHCII trimers are located in red fluorescence regions only 367
368
13
(Stage 33) More developed grana 369
During the third day (stage 33) chloroplasts with grana more developed than in the 370
previous stage containing numerous thylakoids were observed (Figure 7) A 371
composite tomographic slice image was obtained as in the previously analyzed 372
stages (Figure 7A) The region of interest was drawn using the 3DMOD software 373
(Figure 7B middle slice from the stack) A model of the granum (light navy) with 374
connected STs (navy) was superimposed on the TEM image (Figures 7C and 7D) In 375
Figures 7E to 7I the model is shown from different angles to visualize direct 376
connections of STs with GTs The complexity of these connections can be observed 377
Some STs were associated with two neighboring GTs as in the previous stage and 378
were connected at an angle of approximately 18deg (Fig 7E and 7F) ST can also split 379
in a dichotomous manner and connect with both the adjacent GT and the next GT in 380
the other slice (left bottom ST Figures 7F and 7H) Additionally we saw that the ST in 381
the area of our model could connect with only one GT as was observed at the top 382
and bottom of the granum (Figure 7G) This shows that the junctional slits created by 383
the connections between GTs and STs can be of different widths as was also 384
reported by Austin and Staehelin for the thylakoid network of well-developed 385
chloroplasts of mature plants (Austin and Staehelin 2011) 386
For this stage the CLSM analysis was also performed The distribution of Chl 387
autofluorescence (Supplemental Figure 4) visible in CLSM changed drastically in 388
comparison to the earlier stage of grana formation Red spots corresponding to grana 389
were uniformly distributed within the chloroplast (Supplemental Figure 4A) 3D 390
models of the computer generated isosurface of Chl fluorescence confirmed the 391
regular distribution of grana that is characteristic of a mature chloroplast (Rumak et 392
al 2010) (Figures 4B to 4D) However the size of chloroplast at this stage of 393
biogenesis was much smaller (approximately 3 μm) than the 6 μm chloroplasts found 394
in mature plants 395
Based on the TEM sections of numerous developmental stages and also on the 396
reconstruction of the membrane transformation in 3D during the 7 stages of 397
chloroplast biogenesis we proposed a 2D theoretical model (Figure 8) of the 398
membrane changes The proposed theoretical model of membrane rearrangements 399
taken together with the 3D models allow us to create a dynamic model of chloroplast 400
development which is presented as a movie (Supplemental Movie 1) 401
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
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Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale genetic analysis of chloroplast biogenesis in maizeBiochim Biophys Acta 1847 1004-1016
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Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals theirsignificance in chloroplast development Photosynth Res 96 37-50
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The two spectroscopically different short wavelengthprotochlorophyllide forms in pea epicotyls are both monomeric Biochim Biophys Acta 1365 531-540
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast RNA polymerases Role in chloroplast biogenesisBiochim Biophys Acta 1847 761-769
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR (2010) Energy transfer processes in the isolated
core antenna complexes CP43 and CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606-1616Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain and loss of photosynthetic membranes duringplastid differentiation in the shoot apex of Arabidopsis Plant Cell 24 1143-1157
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar to cubic membrane transition as investigatedby electron microscopy Methods Cell Biol 108 319-343
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of thylakoid membranes in higher plant chloroplaststhe physicochemical forces at work and the functional consequences that ensue Photochem Photobiol Sci Off J EurPhotochem Assoc Eur Soc Photobiol 4 1081-1090
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DallOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting proteins Biochim Biophys Acta 1847 861-871Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) Quantification of photosystem I and II in different parts of thethylakoid membrane from spinach Biochim Biophys Acta 1608 53-61
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-M and Mamedov F (2006) Dimeric andmonomeric organization of photosystem II Distribution of five distinct complexes in the different domains of the thylakoidmembrane J Biol Chem 281 14241-14249
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid membranes J Exp Bot 62 2393-2402Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) Arrangement of photosystem II and ATP synthase inchloroplast membranes of spinach and pea Plant Cell 22 1299-1312
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants BiochimBiophys Acta 1706 12-39
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses subvert cholesterol homeostasis to induce host cubicmembranes Trends Cell Biol 20 371-379
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane structure in the mitochondria of amoebaeChaos carolinensis Protoplasma 20316-25
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA (1999) Cubic membrane structure in amoeba(Chaos carolinensis) mitochondria determined by electron microscopic tomography J Struct Biol 127 231-239
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister W (2015) Native architecture of theChlamydomonas chloroplast revealed by in situ cryo-electron tomography eLife 4
Pubmed Author and Title
CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gabruk M Stecka A Strzalka W Kruk J Strzalka K and Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzymecomplexes reconstituted with PORA PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS One 10e0116990
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes Biochim Biophys Acta 1837 481-494Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Grzyb JM Solymosi K Strzalka K and Mysliwa-Kurdziel B (2013) Visualization and characterization of prolamellar bodieswith atomic force microscopy J Plant Physiol 170 1217-1227
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (2001) Membrane geometry of open prolamellar bodies Protoplasma 215 4-15Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA FOLLOWING ALDEHYDE OSMIUM-TETROXIDEFIXATION J Cell Biol 24 79-93
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell (Edward Arnold London)
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective excitation of photosystems in chloroplasts inside plantleaves observed by near-infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225-238
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur R Garstka M Maksymiec W Kulik ADietler G and Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions astudy of lipid-light-harvesting complex II model membranes Plant Cell 25 2155-2170
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids Nat Rev Mol Cell Biol 14787-802
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems experimentally-investigated entropy-driven stackingof plant photosynthetic membranes Sci Rep 4 4142
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes BiochimBiophys Acta 1708 187-195
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
13
(Stage 33) More developed grana 369
During the third day (stage 33) chloroplasts with grana more developed than in the 370
previous stage containing numerous thylakoids were observed (Figure 7) A 371
composite tomographic slice image was obtained as in the previously analyzed 372
stages (Figure 7A) The region of interest was drawn using the 3DMOD software 373
(Figure 7B middle slice from the stack) A model of the granum (light navy) with 374
connected STs (navy) was superimposed on the TEM image (Figures 7C and 7D) In 375
Figures 7E to 7I the model is shown from different angles to visualize direct 376
connections of STs with GTs The complexity of these connections can be observed 377
Some STs were associated with two neighboring GTs as in the previous stage and 378
were connected at an angle of approximately 18deg (Fig 7E and 7F) ST can also split 379
in a dichotomous manner and connect with both the adjacent GT and the next GT in 380
the other slice (left bottom ST Figures 7F and 7H) Additionally we saw that the ST in 381
the area of our model could connect with only one GT as was observed at the top 382
and bottom of the granum (Figure 7G) This shows that the junctional slits created by 383
the connections between GTs and STs can be of different widths as was also 384
reported by Austin and Staehelin for the thylakoid network of well-developed 385
chloroplasts of mature plants (Austin and Staehelin 2011) 386
For this stage the CLSM analysis was also performed The distribution of Chl 387
autofluorescence (Supplemental Figure 4) visible in CLSM changed drastically in 388
comparison to the earlier stage of grana formation Red spots corresponding to grana 389
were uniformly distributed within the chloroplast (Supplemental Figure 4A) 3D 390
models of the computer generated isosurface of Chl fluorescence confirmed the 391
regular distribution of grana that is characteristic of a mature chloroplast (Rumak et 392
al 2010) (Figures 4B to 4D) However the size of chloroplast at this stage of 393
biogenesis was much smaller (approximately 3 μm) than the 6 μm chloroplasts found 394
in mature plants 395
Based on the TEM sections of numerous developmental stages and also on the 396
reconstruction of the membrane transformation in 3D during the 7 stages of 397
chloroplast biogenesis we proposed a 2D theoretical model (Figure 8) of the 398
membrane changes The proposed theoretical model of membrane rearrangements 399
taken together with the 3D models allow us to create a dynamic model of chloroplast 400
development which is presented as a movie (Supplemental Movie 1) 401
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR (2010) Energy transfer processes in the isolated
core antenna complexes CP43 and CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606-1616Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain and loss of photosynthetic membranes duringplastid differentiation in the shoot apex of Arabidopsis Plant Cell 24 1143-1157
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Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar to cubic membrane transition as investigatedby electron microscopy Methods Cell Biol 108 319-343
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Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of thylakoid membranes in higher plant chloroplaststhe physicochemical forces at work and the functional consequences that ensue Photochem Photobiol Sci Off J EurPhotochem Assoc Eur Soc Photobiol 4 1081-1090
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DallOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting proteins Biochim Biophys Acta 1847 861-871Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) Quantification of photosystem I and II in different parts of thethylakoid membrane from spinach Biochim Biophys Acta 1608 53-61
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Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-M and Mamedov F (2006) Dimeric andmonomeric organization of photosystem II Distribution of five distinct complexes in the different domains of the thylakoidmembrane J Biol Chem 281 14241-14249
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Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid membranes J Exp Bot 62 2393-2402Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) Arrangement of photosystem II and ATP synthase inchloroplast membranes of spinach and pea Plant Cell 22 1299-1312
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Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants BiochimBiophys Acta 1706 12-39
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses subvert cholesterol homeostasis to induce host cubicmembranes Trends Cell Biol 20 371-379
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane structure in the mitochondria of amoebaeChaos carolinensis Protoplasma 20316-25
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA (1999) Cubic membrane structure in amoeba(Chaos carolinensis) mitochondria determined by electron microscopic tomography J Struct Biol 127 231-239
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister W (2015) Native architecture of theChlamydomonas chloroplast revealed by in situ cryo-electron tomography eLife 4
Pubmed Author and Title
CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gabruk M Stecka A Strzalka W Kruk J Strzalka K and Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzymecomplexes reconstituted with PORA PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS One 10e0116990
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes Biochim Biophys Acta 1837 481-494Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Grzyb JM Solymosi K Strzalka K and Mysliwa-Kurdziel B (2013) Visualization and characterization of prolamellar bodieswith atomic force microscopy J Plant Physiol 170 1217-1227
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (2001) Membrane geometry of open prolamellar bodies Protoplasma 215 4-15Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA FOLLOWING ALDEHYDE OSMIUM-TETROXIDEFIXATION J Cell Biol 24 79-93
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell (Edward Arnold London)
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective excitation of photosystems in chloroplasts inside plantleaves observed by near-infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225-238
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur R Garstka M Maksymiec W Kulik ADietler G and Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions astudy of lipid-light-harvesting complex II model membranes Plant Cell 25 2155-2170
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids Nat Rev Mol Cell Biol 14787-802
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems experimentally-investigated entropy-driven stackingof plant photosynthetic membranes Sci Rep 4 4142
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes BiochimBiophys Acta 1708 187-195
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P Gruissem W and Baginsky S (2007)Proteome dynamics during plastid differentiation in rice Plant Physiol 143 912-923
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED ANDFAR-RED LIGHT J Cell Biol 22 433-442
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV Dekker JP and Jansson S (2005) Structureof the higher plant light harvesting complex I in vivo characterization and structural interdependence of the Lhca proteinsBiochemistry (Mosc) 44 3065-3073
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
14
Summarizing the structural part of our work we have presented in detail the models 402
obtained by electron tomography that describe several stages in chloroplast 403
development the PLB paracrystalline lattice and its transformation the untwining of 404
tubules from the PLB structure as a continuous process the change of their 405
conformation to stromal flat slats even inside a degrading PLB and eventually the 406
formation of a well-developed grana with STs linked to GTs at an angle of 407
approximately 18deg Additional models of the two latest of the analyzed stages of 408
chloroplast biogenesis obtained by CLSM demonstrated the 3D details of the 409
architecture of the early grana distribution 410
411
Quantitative EM Analysis of Grana Formation During Biogenesis of the 412
Chloroplast 413
To quantify the grana formation process during chloroplast biogenesis we measured 414
the diameter height and number of membrane layers of the grana (Supplemental 415
Table 1) as described in Methods Grana lateral irregularity (GLI) is defined as the 416
coefficient of variation (the ratio of the standard deviation to the mean) of membrane 417
diameters within the granum The GLI in stages 20 and 33 was lower in comparison 418
to stage 18 both for grana with different numbers of membranes (Supplemental 419
Table 2) and for subgroups with the same membrane count in the grana 420
(Supplemental Table 3) When comparing all the data from stages 20 and 33 the 421
difference in the GLI value was statistically insignificant (Supplemental Table 2) 422
However for the 4-membrane grana the irregularity of grana was lower in stage 33 423
(Supplemental Table 3) During chloroplast biogenesis the stacking repeat distance 424
(SRD) value decreased continuously in subsequent developmental stages 425
(Supplemental Table 4) Spearmanrsquos rank correlations between the height of the 426
granum and the number of stacked membranes increased in subsequent stages (18 427
lt 20 lt 33) (Supplemental Table 5) confirming a gradual increase of the membrane 428
compaction in the growing grana thus lowering the SRD value Moreover the 429
dominating direction of grana enlargement differed between successive stage-to-430
stage transitions During the transition from the first stacked membranes (stage 18) 431
to small grana (stage 20) there was a tendency for membrane expansion in the 432
lateral rather than vertical direction while during the transition from stage 20 to 33 433
the tendency was reversed (Supplemental Table 6 and Supplemental Figure 5) 434
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
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Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
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Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
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Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
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Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gabruk M Stecka A Strzalka W Kruk J Strzalka K and Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzymecomplexes reconstituted with PORA PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS One 10e0116990
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Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes Biochim Biophys Acta 1837 481-494Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
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Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
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Grzyb JM Solymosi K Strzalka K and Mysliwa-Kurdziel B (2013) Visualization and characterization of prolamellar bodieswith atomic force microscopy J Plant Physiol 170 1217-1227
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Gunning BE (2001) Membrane geometry of open prolamellar bodies Protoplasma 215 4-15Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA FOLLOWING ALDEHYDE OSMIUM-TETROXIDEFIXATION J Cell Biol 24 79-93
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Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell (Edward Arnold London)
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective excitation of photosystems in chloroplasts inside plantleaves observed by near-infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225-238
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur R Garstka M Maksymiec W Kulik ADietler G and Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions astudy of lipid-light-harvesting complex II model membranes Plant Cell 25 2155-2170
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids Nat Rev Mol Cell Biol 14787-802
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems experimentally-investigated entropy-driven stackingof plant photosynthetic membranes Sci Rep 4 4142
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes BiochimBiophys Acta 1708 187-195
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P Gruissem W and Baginsky S (2007)Proteome dynamics during plastid differentiation in rice Plant Physiol 143 912-923
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED ANDFAR-RED LIGHT J Cell Biol 22 433-442
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV Dekker JP and Jansson S (2005) Structureof the higher plant light harvesting complex I in vivo characterization and structural interdependence of the Lhca proteinsBiochemistry (Mosc) 44 3065-3073
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) Protein assembly and heat stability in developingthylakoid membranes during greening Proc Natl Acad Sci U S A 99 12149-12154
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kouril R Dekker JP and Boekema EJ (2012) Supramolecular organization of photosystem II in green plants BiochimBiophys Acta 1817 2-12
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization of Three-Dimensional Image Data Using IMODJ Struct Biol 116 71-76
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 655-659
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-proteasome system in plastid developmentBiochim Biophys Acta 1847 939-948
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 58 11-26Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid membranes from plastid transcription to proteincomplex assembly Planta 237 413-428
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology Second Edition (CRC Press)
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography software for three-dimensional reconstructionin transmission electron microscopy BMC Bioinformatics 8 288
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings by white red and blue low intensity lightProtoplasma 131 166-173
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986b) Thylakoid and grana formation during the development of pea chloroplasts illuminated by white red andblue low intensity light Protoplasma 134 88-94
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
15
435
Formation of Chlorophyll-Protein Complexes During Biogenesis of the 436
Chloroplast 437
The association of Chl species with photosynthetic proteins and the formation of the 438
CP complexes in isolated intact etioplasts and in developing bean chloroplasts were 439
analyzed from data obtained by the application of complementary methods low 440
temperature fluorescence emission and excitation spectroscopy mild-denaturing 441
electrophoresis and immunodetection of proteins associated with PSII (Figure 9) 442
When normalized to the same area steady-state 77 K fluorescence emission spectra 443
reveal the relative contribution of specific species to the overall fluorescence pattern 444
As shown in Figure 9A two bands (at 630 nm and 653 nm) were observed in 445
etiolated bean seedlings The first one corresponds to free protochlorophyllide 446
(Pchlide) species whereas the latter is related to the Pchlide-LPOR-NADPH complex 447
in PLB (Schoefs and Franck 2008 Adam et al 2011 and literature therein) After 448
one h of illumination the 653 nm band completely disappeared and a new red-shifted 449
band at approximately 679 nm was observed This indicates a decline of Pchlide 450
associated with LPOR complex despite the significant band still present 451
corresponding to free Pchlide (Schoefs and Franck 2008 Gabruk et al 2015) The 452
corresponding excitation spectra reflecting relative energy transfer from the 453
absorbing pigments to the emitting Chl species (Figure 9B) showed a ChlideChl a 454
related band at approximately 440 nm (Gabruk et al 2015) suggesting energy 455
transfer to ChlideChl a species only Simultaneous structural investigation by mild-456
denaturing electrophoresis (Figure 9D) and immunodetection (Figure 9E) did not 457
reveal the presence of either CP complexes or proteins associated with PSII 458
Illumination for two h (Figure 9A) caused a shift of a red band to 683 nm and 459
formation of a new wide far-red band at approximately 724 nm These changes 460
indicated further degradation of Pchlide-LPOR complexes with simultaneous 461
appearance of the core complexes The far-red band is related to the spectrum of the 462
PSI core complex (Klimmek et al 2005 Rumak et al 2012) The presence of the 463
683 nm band in the emission spectra (Figure 9A) and the excitation band at 437 nm 464
corresponding solely to light-harvesting by Chl a (Figure 9B) is a counterpart of the 465
CP43CP47 spectra seen previously (Andrizhiyevskaya et al 2005 Casazza et al 466
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
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Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
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41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 655-659
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Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-proteasome system in plastid developmentBiochim Biophys Acta 1847 939-948
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Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 58 11-26Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid membranes from plastid transcription to proteincomplex assembly Planta 237 413-428
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Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology Second Edition (CRC Press)
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography software for three-dimensional reconstructionin transmission electron microscopy BMC Bioinformatics 8 288
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Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings by white red and blue low intensity lightProtoplasma 131 166-173
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Mostowska A (1986b) Thylakoid and grana formation during the development of pea chloroplasts illuminated by white red andblue low intensity light Protoplasma 134 88-94
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Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mysliwa-Kurdziel B Kruk J and Strzalka K (2013) Protochlorophyllide in model systems--an approach to in vivo conditionsBiophys Chem 175-176 28-38
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Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture and dynamics of the photosynthetic apparatus inhigher plants Plant J Cell Mol Biol 70 157-176
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Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts J Cell Sci 6 243-255Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) Identification of the carotenoid isomerase providesinsight into carotenoid biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 321-332
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Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in land plants J Exp Bot 65 1955-1972Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes Biochim Biophys Acta BBA - Bioenerg 1847 821-830
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Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur R and Garstka M (2010) 3-D modelling ofchloroplast structure under (Mg2+) magnesium ion treatment Relationship between thylakoid membrane arrangement andstacking Biochim Biophys Acta 1797 1736-1748
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Rumak I Mazur R Gieczewska K Koziol-Lipinska J Kierdaszuk B Michalski WP Shiell BJ Venema JH VredenbergWJ Mostowska A and Garstka M (2012) Correlation between spatial (3D) structure of pea and bean thylakoid membranes andarrangement of chlorophyll-protein complexes BMC Plant Biol 12 72
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Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and prothylakoids fractionated from wheat etioplastsPhysiol Plant 56 125-132
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SAS Institute Inc 2013 SASSTATreg 123 Users Guide Cary NC SAS Institute IncPubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH protochlorophyllide oxidoreductase in primary bean leaves(Phaseolus vulgaris) during the first days of photoperiodic growth Photosynth Res 96 15-26
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Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In Lipids in Photosynthesis Structure Functionand Genetics S Paul-Andreacute and M Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 209-224
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Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
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Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
16
2010) The immunodetection pattern of the stage 12 sample showed traces of CP43 467
and a lack of visible CP47 D1 and D2 bands (Figure 9E) indicating that after two h 468
of illumination the CP43 inner antenna was the dominating chlorophyll-protein 469
complex In the emission spectrum of the stage 14 sample besides the 683 nm 470
band a shoulder at approximately 691 nm appeared (Figure 9A) with simultaneous 471
significant increase of the 470 nm Chl b band in the excitation spectrum (Figure 9C) 472
The 691 nm band originates from the PSII core and CP43 intrinsic antenna bound 473
with Chl a (Rumak et al 2012) The 683 nm band can be related to LHCII complexes 474
containing both Chls a and b apart from the CP47 complex (Rumak et al 2012) 475
Immunoblot analysis revealed only traces of CP43 and Lhcb2 in the stage 14 476
sample (Figure 9E) suggesting that these proteins create the first CP complexes 477
related to PSII However no green bands assigned to more organized CP complexes 478
were resolved by mild-denaturing electrophoresis (Figure 9D) This suggests that in 479
the first parallel PT membranes (stages 12 and 14) the arrangement of rare CP 480
complexes differs substantially from that in mature thylakoids 481
Eight h of seedling illumination radically changed the spectroscopic and 482
electrophoretic pattern The emission and excitation spectra (Figure 9A and 9C) are 483
very similar in shape to those observed in thylakoids isolated from mature leaves 484
The red band revealed two separate maxima at 683 nm both from trimers and 485
monomers of LHCII and CP43 while the 691 nm band corresponds to the PSII core 486
(Rumak et al 2012) The appearance of the 728 nm band suggests incorporation of 487
the LHCI antenna complexes into membranes (Klimmek et al 2005 Rumak et al 488
2012) The excitation spectrum indicates the presence of both Chl a and b (Figure 489
9C) Furthermore the D1 core protein was the only nonvisible protein associated with 490
LHCIIPSII (Rumak et al 2012) (Figure 9E) Mild-denaturing electrophoresis (Figure 491
9D) revealed only traces of LHCI-PSI LHCII-PSII supercomplexes (upper bands) 492
and LHCII trimers (middle band) (Rumak et al 2012) These data indicate an early 493
phase of the CP organization in the lateral plane of the thylakoid membranes 494
probably restricted to smaller dispersed microdomains (Rumak et al 2010) The 495
ordered arrangement of LHCII and of LHCII-PSII complexes stabilizes the structure 496
of grana stacks (Rumak et al 2010) but due to the still limited number of 497
complexes the interaction between adjacent membranes occurs only in a small 498
group of membranes (Figure 5) 499
17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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17
The spectra and electrophoretic patterns obtained for developing chloroplasts 500
isolated from two and three d-old seedlings (Figure 9) do not differ qualitatively from 501
those of mature thylakoids (Rumak et al 2012) Sharp bands in the spectra (Figure 502
9A and 9C) suggest precise arrangements of pigments in the CP complexes The 503
total number of supercomplexes and LHCII trimers and monomers (Figure 9D) was 504
less than in mature thylakoids (Garstka et al 2005 Rumak et al 2012) and 505
corresponded to the grana seen in two and three d-old plants (Figure 6 and 7) A 506
simple relationship was also observed between the gradual accumulation of the 507
LHCII apoproteins (Figure 9E) and an increase of the grana stacks (Supplemental 508
Table 1) 509
510
DISCUSSION 511
This work describes in detail the spatial 3D reconstruction of the paracrystalline 512
arrangement of PLB and its gradual transformation from a tubular to a linear system 513
during the greening process The structural changes during the early stages of 514
chloroplast biogenesis have been visualized 515
The PLB is a paracrystalline membrane structure typical for angiosperm etioplasts 516
(Gunning and Steer 1975) The most basic structures of the PLB lattice correspond 517
in their symmetry to two crystal forms of zinc sulfide in which tetrahedrally branched 518
units join together in 3D networks of hexagons The first wurtzite type is that of the 519
hexagonal close-packed structure Hexagons of the neighboring crystallographic 520
planes (above and below) form a hexagonal prism The second lattice type 521
corresponding to zinc-blende (sphalerite) is a cubic close-packed structure In this 522
lattice type successive planes of hexagonal rings are displaced half a ring with 523
respect to one another These two types are the most common among the basic 524
structures of PLBs Other crystallographic lattices eg pentagonal dodecahedron 525
open or centric type can also be present Two lattice structures can be present in one 526
PLB resembling polycrystals In addition other combinations and configurations of 527
the PLB lattice can be found (Gunning 2001) The only type of PLB lattice observed 528
in the etiolated bean plastids was of the wurtzite-type hexagonal prism (Figure 1) 529
However the type of lattice might be in different under growing conditions 530
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
Parsed CitationsAbdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) High salt stress induces swollen prothylakoids indark-grown wheat and alters both prolamellar body transformation and reformation after irradiation J Exp Bot 58 2553-2564
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ Biophotonics International 11 36-42Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of thylakoid networks in angiosperms knowns andunknowns Plant Mol Biol 76 221-234
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend beyond the Flatland of cell membraneorganization J Cell Biol 173 839-844
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic membranes the missing dimension of cellmembrane organization Int Rev Cell Mol Biol 274 275-342
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the structure and function of photosystem II in higherplant thylakoid membranes the grana enigma Photosynth Res 98 575-587
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R and Dekker JP (2005) Origin of the F685 andF695 fluorescence in photosystem II Photosynth Res 84 173-180
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants asdetermined by electron tomography Plant Physiol 155 1601-1611
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of photosystem II units Philos Trans R Soc LondB Biol Sci 357 1451-1459 discussion 1459-1460
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale genetic analysis of chloroplast biogenesis in maizeBiochim Biophys Acta 1847 1004-1016
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals theirsignificance in chloroplast development Photosynth Res 96 37-50
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The two spectroscopically different short wavelengthprotochlorophyllide forms in pea epicotyls are both monomeric Biochim Biophys Acta 1365 531-540
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast RNA polymerases Role in chloroplast biogenesisBiochim Biophys Acta 1847 761-769
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR (2010) Energy transfer processes in the isolated
core antenna complexes CP43 and CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606-1616Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain and loss of photosynthetic membranes duringplastid differentiation in the shoot apex of Arabidopsis Plant Cell 24 1143-1157
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar to cubic membrane transition as investigatedby electron microscopy Methods Cell Biol 108 319-343
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of thylakoid membranes in higher plant chloroplaststhe physicochemical forces at work and the functional consequences that ensue Photochem Photobiol Sci Off J EurPhotochem Assoc Eur Soc Photobiol 4 1081-1090
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
DallOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting proteins Biochim Biophys Acta 1847 861-871Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) Quantification of photosystem I and II in different parts of thethylakoid membrane from spinach Biochim Biophys Acta 1608 53-61
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-M and Mamedov F (2006) Dimeric andmonomeric organization of photosystem II Distribution of five distinct complexes in the different domains of the thylakoidmembrane J Biol Chem 281 14241-14249
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid membranes J Exp Bot 62 2393-2402Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) Arrangement of photosystem II and ATP synthase inchloroplast membranes of spinach and pea Plant Cell 22 1299-1312
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants BiochimBiophys Acta 1706 12-39
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses subvert cholesterol homeostasis to induce host cubicmembranes Trends Cell Biol 20 371-379
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane structure in the mitochondria of amoebaeChaos carolinensis Protoplasma 20316-25
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA (1999) Cubic membrane structure in amoeba(Chaos carolinensis) mitochondria determined by electron microscopic tomography J Struct Biol 127 231-239
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister W (2015) Native architecture of theChlamydomonas chloroplast revealed by in situ cryo-electron tomography eLife 4
Pubmed Author and Title
CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gabruk M Stecka A Strzalka W Kruk J Strzalka K and Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzymecomplexes reconstituted with PORA PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS One 10e0116990
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes Biochim Biophys Acta 1837 481-494Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
18
Different kinds of such highly organized and complex cubic or tubule-reticular 531
structures evolve not only from plastid inner membranes or smooth endoplasmic 532
reticulum but also directly from plasma membranes nuclear envelopes 533
mitochondrial cristae systems and Golgi complexes and are ubiquitous in many 534
different cell types under specific environmental conditions (for a review of cubic 535
membrane occurrence in biological systems see Almsherqi et al 2009) A hexagonal 536
paracrystalline membrane arrangement of ER structurally similar to a PLB was 537
observed in cytoplasm of compactin-resistant Chinese hamster ovary cells that were 538
grown for 72 h in stressed conditions in the presence of 40 microM compactin Compactin 539
is a competitive inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase the 540
rate limiting enzyme in cholesterol synthesis This confirms the possibility of creating 541
such unique structure via a different combination of lipids and proteins in organisms 542
that are evolutionarily distant (Chong and Deng 2012) 543
Although the structural aspects of chloroplast biogenesis have been the subject of 544
research over the last 30 years (Ryberg and Sundqvist 1982 Mostowska 1986a 545
1986b Von Wettstein et al 1995 Gunning 2001 Adam et al 2011) the character 546
of the transformation of the tubular paracrystalline PLB structure to a linear thylakoid 547
arrangement was not observed as a continuous process Other authors have 548
described the disintegration of PLBs into vesicles upon illumination in particular as a 549
disruption of isolated paracrystalline wheat PLBs into vesicles that rearrange into 550
strands dispersed through the stroma (Klein et al 1964 Grzyb et al 2013) and also 551
as vesicle formation on the surface of the PLB together with a transition of the tubular 552
network into lamellae (Solymosi et al 2006) Such observations were not confirmed 553
by our results using ET on bean leaf sections Even in the 1970rsquos a PLB 554
transformation to porous primary thylakoids was described as a rearrangement of 555
existing membranes and pores of PTs as relics of the lattice spacing of the PLB 556
(Gunning and Steer 1975) We have demonstrated that the paracrystalline structure 557
of the PLB transforms directly to lamellar structures that are porous from the 558
beginning This direct transformation can explain the presence of so many 559
photosynthetic proteins in the PLB in the darkness which results in 560
photomorphogenic growth upon illumination (Blomqvist et al 2008) Already at the 561
beginning of the untangling of the paracrystalline network tubules were transformed 562
into porous flat slats even in the midst of the degrading PLB (Figure 2) 563
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
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Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
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Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
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Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
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Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P Gruissem W and Baginsky S (2007)Proteome dynamics during plastid differentiation in rice Plant Physiol 143 912-923
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Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED ANDFAR-RED LIGHT J Cell Biol 22 433-442
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV Dekker JP and Jansson S (2005) Structureof the higher plant light harvesting complex I in vivo characterization and structural interdependence of the Lhca proteinsBiochemistry (Mosc) 44 3065-3073
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Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) Protein assembly and heat stability in developingthylakoid membranes during greening Proc Natl Acad Sci U S A 99 12149-12154
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Kouril R Dekker JP and Boekema EJ (2012) Supramolecular organization of photosystem II in green plants BiochimBiophys Acta 1817 2-12
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Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 655-659
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-proteasome system in plastid developmentBiochim Biophys Acta 1847 939-948
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Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 58 11-26Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid membranes from plastid transcription to proteincomplex assembly Planta 237 413-428
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Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology Second Edition (CRC Press)
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography software for three-dimensional reconstructionin transmission electron microscopy BMC Bioinformatics 8 288
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Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings by white red and blue low intensity lightProtoplasma 131 166-173
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Mostowska A (1986b) Thylakoid and grana formation during the development of pea chloroplasts illuminated by white red andblue low intensity light Protoplasma 134 88-94
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Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mysliwa-Kurdziel B Kruk J and Strzalka K (2013) Protochlorophyllide in model systems--an approach to in vivo conditionsBiophys Chem 175-176 28-38
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture and dynamics of the photosynthetic apparatus inhigher plants Plant J Cell Mol Biol 70 157-176
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Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts J Cell Sci 6 243-255Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) Identification of the carotenoid isomerase providesinsight into carotenoid biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 321-332
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Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast biogenesis and development Biochim BiophysActa
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Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in land plants J Exp Bot 65 1955-1972Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes Biochim Biophys Acta BBA - Bioenerg 1847 821-830
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Google Scholar Author Only Title Only Author and Title
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Rudowska L Gieczewska K Mazur R Garstka M and Mostowska A (2012) Chloroplast biogenesis mdash Correlation betweenstructure and function Biochim Biophys Acta BBA - Bioenerg 1817 1380-1387
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Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur R and Garstka M (2010) 3-D modelling ofchloroplast structure under (Mg2+) magnesium ion treatment Relationship between thylakoid membrane arrangement andstacking Biochim Biophys Acta 1797 1736-1748
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Rumak I Mazur R Gieczewska K Koziol-Lipinska J Kierdaszuk B Michalski WP Shiell BJ Venema JH VredenbergWJ Mostowska A and Garstka M (2012) Correlation between spatial (3D) structure of pea and bean thylakoid membranes andarrangement of chlorophyll-protein complexes BMC Plant Biol 12 72
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Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and prothylakoids fractionated from wheat etioplastsPhysiol Plant 56 125-132
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SAS Institute Inc 2013 SASSTATreg 123 Users Guide Cary NC SAS Institute IncPubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
19
In Chlamydomonas the pyrenoid which is considered to be a nucleation center for 564
thylakoid maturation is penetrated by thylakoid tubules In other algal chloroplasts 565
translation membranes surround or cut across the pyrenoid Although our study deals 566
with the chloroplasts of an angiosperm which differ from the chloroplasts of algae it 567
can be speculated that during the thylakoid biogenesis of the angiosperm 568
chloroplast PLBs with connected PTs and the pyrenoid of the algae chloroplast can 569
play a similar structural role (Rast et al 2015) Regularity of PLBs in the bean 570
plastids (Figure 1) was observed simultaneously with the band at 653 nm 571
corresponding to the Pchlide-LPOR-NADPH complex (Figure 9A) (Abdelkader et al 572
2007 Blomqvist et al 2008 Schoefs and Franck 2008 Adam et al 2011 and 573
literature therein) The transformation of PLBs observed after one h of illumination 574
was seen as a loss of regular connections through interconnecting tubules (Figure 2) 575
At the same time as the nodes of the paracrystalline network vanished the 576
fluorescence of Pchlide-LPOR-NADPH complex was no longer observed (Figure 9A) 577
In some other species growing in the daynight cycle eg in pea (Pisum sativum L) 578
a partial reconstruction of the PLBs after the dark period during the chloroplast 579
differentiation was observed (Rudowska et al 2012 Abdelkader et al 2007 580
Schoefs and Franck 2008) It is not clear why such a reconstruction of PLBs in bean 581
plastids (ie a reconstruction of the cubic phase after the dark period) was not 582
observed Fourier transform infrared spectroscopy analysis showed that the 583
proteinlipid ratio (ie the average protein density) was higher in bean than in pea 584
thylakoids which might limit the protein diffusion within bean thylakoid membranes 585
and their plasticity (Rumak et al 2010) This might be the reason why bean PLB 586
reconstruction does not take place 587
During the first hours of illumination the flat slats emerging directly from the bean 588
PLB visualized by ET remain porous (Figures 2 to 4) until the first neighboring 589
thylakoids overlap (Figure 5) Formation of the first parallel or partially overlapping 590
membranes (Figure 5) coincides with the appearance of the first CP complexes 591
Appearance of the extrinsic antennae follow the core complexes but the 592
arrangement of the CP complexes is much different from the final structure observed 593
in mature thylakoids (Figure 9) Such immaturity of the stacked membrane 594
arrangement in stage 18 was also reflected in the highest SRD value which then 595
gradually declined during the biogenesis process (Supplemental Tables 4 and 5) 596
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
Parsed CitationsAbdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) High salt stress induces swollen prothylakoids indark-grown wheat and alters both prolamellar body transformation and reformation after irradiation J Exp Bot 58 2553-2564
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ Biophotonics International 11 36-42Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of thylakoid networks in angiosperms knowns andunknowns Plant Mol Biol 76 221-234
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend beyond the Flatland of cell membraneorganization J Cell Biol 173 839-844
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic membranes the missing dimension of cellmembrane organization Int Rev Cell Mol Biol 274 275-342
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the structure and function of photosystem II in higherplant thylakoid membranes the grana enigma Photosynth Res 98 575-587
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R and Dekker JP (2005) Origin of the F685 andF695 fluorescence in photosystem II Photosynth Res 84 173-180
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants asdetermined by electron tomography Plant Physiol 155 1601-1611
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of photosystem II units Philos Trans R Soc LondB Biol Sci 357 1451-1459 discussion 1459-1460
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale genetic analysis of chloroplast biogenesis in maizeBiochim Biophys Acta 1847 1004-1016
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals theirsignificance in chloroplast development Photosynth Res 96 37-50
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The two spectroscopically different short wavelengthprotochlorophyllide forms in pea epicotyls are both monomeric Biochim Biophys Acta 1365 531-540
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast RNA polymerases Role in chloroplast biogenesisBiochim Biophys Acta 1847 761-769
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR (2010) Energy transfer processes in the isolated
core antenna complexes CP43 and CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606-1616Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain and loss of photosynthetic membranes duringplastid differentiation in the shoot apex of Arabidopsis Plant Cell 24 1143-1157
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
20
Stacking of thylakoids in order to form grana interconnected by non-stacked 597
thylakoids is a complicated process that includes protein-protein and protein-lipid 598
interactions in the lateral and vertical plane of the membranes as well as 599
thermodynamic changes inside the chloroplast environment (Jia et al 2014) Vertical 600
appression of adjacent membranes is associated with an increase of van der Waals 601
attractions and a decrease of the electrostatic and hydration repulsion (Chow et al 602
2005) The appression process is feasible due to lateral separation of CP complexes 603
PSI which has a large protrusion at the stroma-facing surface is segregated to 604
nonappressed thylakoids (Chow et al 2005) while the LHCII-PSII and LHCII are 605
localized in appressed membranes by a self-organized process (Kirchhoff et al 606
2007 Rumak et al 2010) 607
Commonly accepted models point out the essential role played by the amount of 608
LHCII in grana formation based on the observation of LHCII-deficient barley 609
(Hordeum vulgare L) mutants on liposomes with incorporated LHCII and on pea 610
thylakoid membranes with a removed stromal-exposed N-terminal segment of LHCII 611
(Nevo et al 2012) In this last model a positively charged N-terminal segment of 612
LHCII in one membrane interacts with a negatively charged stromal surface of the 613
opposite LHCII trimer (Standfuss et al 2005 Daum et al 2010) Recently however 614
the significance of LHCII-PSII supercomplexes and the LHCII trimer arrangement in 615
grana membranes has been emphasized (Kim et al 2009 Kouřil et al 2012 Tietz 616
et al 2015) The contact between stacked adjacent membranes is made by the 617
stromal surfaces of polypeptides of supercomplexes mainly LHCII trimers PSII core 618
and minor antennae (Daum et al 2010) The adjacent membranes are separated by 619
a stromal gap (Kim et al 2005) whereas supercomplexes form more or less ordered 620
arrays in appressed grana thylakoids (Kirchhoff et al 2008 Daum et al 2010) The 621
size of the lumen space of the thylakoids depends on the interaction between oxygen 622
evolving complexes of the PSII from opposite lamellae (Anderson et al 2008 623
Kirchhoff et al 2008) Furthermore the participation of other proteins such as PsbS 624
and CURT1 has been considered (Goral et al 2012 Pribil et al 2014) 625
In a developing chloroplast after 8 h of illumination (stage 18) (Figure 5) the first 626
small stacks appear at the same time as the first ordered structures of LHCII and 627
LHCII-PSII (Figure 9) The close association of the membranes causes a 628
coalescence of perforations while the neighboring stroma lamellae still remain 629
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
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Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
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41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-proteasome system in plastid developmentBiochim Biophys Acta 1847 939-948
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Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 58 11-26Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology Second Edition (CRC Press)
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography software for three-dimensional reconstructionin transmission electron microscopy BMC Bioinformatics 8 288
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Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings by white red and blue low intensity lightProtoplasma 131 166-173
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Mostowska A (1986b) Thylakoid and grana formation during the development of pea chloroplasts illuminated by white red andblue low intensity light Protoplasma 134 88-94
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Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mysliwa-Kurdziel B Kruk J and Strzalka K (2013) Protochlorophyllide in model systems--an approach to in vivo conditionsBiophys Chem 175-176 28-38
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Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture and dynamics of the photosynthetic apparatus inhigher plants Plant J Cell Mol Biol 70 157-176
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Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts J Cell Sci 6 243-255Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) Identification of the carotenoid isomerase providesinsight into carotenoid biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 321-332
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Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in land plants J Exp Bot 65 1955-1972Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes Biochim Biophys Acta BBA - Bioenerg 1847 821-830
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Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur R and Garstka M (2010) 3-D modelling ofchloroplast structure under (Mg2+) magnesium ion treatment Relationship between thylakoid membrane arrangement andstacking Biochim Biophys Acta 1797 1736-1748
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Rumak I Mazur R Gieczewska K Koziol-Lipinska J Kierdaszuk B Michalski WP Shiell BJ Venema JH VredenbergWJ Mostowska A and Garstka M (2012) Correlation between spatial (3D) structure of pea and bean thylakoid membranes andarrangement of chlorophyll-protein complexes BMC Plant Biol 12 72
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Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and prothylakoids fractionated from wheat etioplastsPhysiol Plant 56 125-132
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SAS Institute Inc 2013 SASSTATreg 123 Users Guide Cary NC SAS Institute IncPubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH protochlorophyllide oxidoreductase in primary bean leaves(Phaseolus vulgaris) during the first days of photoperiodic growth Photosynth Res 96 15-26
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In Lipids in Photosynthesis Structure Functionand Genetics S Paul-Andreacute and M Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 209-224
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Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
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Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
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Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-dimensional organization of higher-plant chloroplastthylakoid membranes revealed by electron tomography Plant Cell 17 2580-2586
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Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P Holzenburg A and Garab G (2000) Self-assemblyof large ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S A 97 1473-1476
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
21
porous (Figure 5) The ET model of the 18 stage (Figure 5) revealed that even in the 630
case of the first stacked membranes the STs associate with GTs in a helical way 631
forming an angle of 18 to 33deg This pattern of spatial structure is similar to that in the 632
fully developed grana where the observed angle was approximately 20deg (Mustaacuterdy et 633
al 2008 Austin and Staehelin 2011 Daum and Kuumlhlbrandt 2011) The formation of 634
gradually more complicated grana structure observed in the two and three day-old 635
seedlings (Figure 6 and 7) correlates not only with the increase of LHCII abundance 636
but also with arrangement of supercomplexes (Figure 9) In these phases of 637
development the pores in thylakoids are no longer observed neither in grana nor 638
stroma (Figures 6 and 7) 639
The interpretation of tomographic fluorescence and electrophoretic data taken 640
together suggest that both the accumulation of CP complexes and their arrangement 641
in supercomplexes influence the formation of appressed membranes during 642
chloroplast biogenesis Development during illumination changes the grana size and 643
the appressed thylakoid distribution (Supplemental Figures 3 and 4) The increased 644
size of the grana can occur through enlargement in lateral and vertical directions We 645
have shown that the expansion of the grana membrane changes direction from 646
lateral to vertical during illumination (Supplemental Table 6 and Supplemental Figure 647
5) Upon illumination not only do the grana become more regularly distributed but 648
also the irregularity of the grana structure expressed by the GLI parameter decreases 649
(Supplemental Table 1-3) The spatial organization of thylakoids inside the 650
chloroplast of higher plants varies between species and mutant lines (Kim et al 651
2009 Rumak et al 2012) These effects might depend on the qualitative and 652
quantitative properties of CP complexes and their arrangements as demonstrated on 653
3D CLSM models of developed pea and bean chloroplasts (Rumak et al 2012) 654
Thus the composition of the thylakoid microdomains and the lateral separation of 655
photosystems might be another mechanism involved in grana formation (Rumak et 656
al 2010) Despite this diversity the general lamellar organization is similar as 657
shown by the broad plasticity of the system (Pribil et al 2014) The structural ET 658
analyses performed on thylakoids of mature spinach (Spinacia oleracea L) tobacco 659
(Nicotiana tabacum L) pea and Arabidopsis (Arabidopsis thaliana) chloroplasts and 660
also our results performed on developing bean chloroplasts confirm the presence of 661
a helical grana arrangement of GTs connected with STs by staggered membrane 662
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
Parsed CitationsAbdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) High salt stress induces swollen prothylakoids indark-grown wheat and alters both prolamellar body transformation and reformation after irradiation J Exp Bot 58 2553-2564
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ Biophotonics International 11 36-42Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of thylakoid networks in angiosperms knowns andunknowns Plant Mol Biol 76 221-234
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend beyond the Flatland of cell membraneorganization J Cell Biol 173 839-844
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic membranes the missing dimension of cellmembrane organization Int Rev Cell Mol Biol 274 275-342
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the structure and function of photosystem II in higherplant thylakoid membranes the grana enigma Photosynth Res 98 575-587
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R and Dekker JP (2005) Origin of the F685 andF695 fluorescence in photosystem II Photosynth Res 84 173-180
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants asdetermined by electron tomography Plant Physiol 155 1601-1611
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of photosystem II units Philos Trans R Soc LondB Biol Sci 357 1451-1459 discussion 1459-1460
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale genetic analysis of chloroplast biogenesis in maizeBiochim Biophys Acta 1847 1004-1016
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals theirsignificance in chloroplast development Photosynth Res 96 37-50
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The two spectroscopically different short wavelengthprotochlorophyllide forms in pea epicotyls are both monomeric Biochim Biophys Acta 1365 531-540
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast RNA polymerases Role in chloroplast biogenesisBiochim Biophys Acta 1847 761-769
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR (2010) Energy transfer processes in the isolated
core antenna complexes CP43 and CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606-1616Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain and loss of photosynthetic membranes duringplastid differentiation in the shoot apex of Arabidopsis Plant Cell 24 1143-1157
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar to cubic membrane transition as investigatedby electron microscopy Methods Cell Biol 108 319-343
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of thylakoid membranes in higher plant chloroplaststhe physicochemical forces at work and the functional consequences that ensue Photochem Photobiol Sci Off J EurPhotochem Assoc Eur Soc Photobiol 4 1081-1090
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
DallOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting proteins Biochim Biophys Acta 1847 861-871Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) Quantification of photosystem I and II in different parts of thethylakoid membrane from spinach Biochim Biophys Acta 1608 53-61
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-M and Mamedov F (2006) Dimeric andmonomeric organization of photosystem II Distribution of five distinct complexes in the different domains of the thylakoidmembrane J Biol Chem 281 14241-14249
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid membranes J Exp Bot 62 2393-2402Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) Arrangement of photosystem II and ATP synthase inchloroplast membranes of spinach and pea Plant Cell 22 1299-1312
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants BiochimBiophys Acta 1706 12-39
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses subvert cholesterol homeostasis to induce host cubicmembranes Trends Cell Biol 20 371-379
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane structure in the mitochondria of amoebaeChaos carolinensis Protoplasma 20316-25
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA (1999) Cubic membrane structure in amoeba(Chaos carolinensis) mitochondria determined by electron microscopic tomography J Struct Biol 127 231-239
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister W (2015) Native architecture of theChlamydomonas chloroplast revealed by in situ cryo-electron tomography eLife 4
Pubmed Author and Title
CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gabruk M Stecka A Strzalka W Kruk J Strzalka K and Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzymecomplexes reconstituted with PORA PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS One 10e0116990
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes Biochim Biophys Acta 1837 481-494Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Grzyb JM Solymosi K Strzalka K and Mysliwa-Kurdziel B (2013) Visualization and characterization of prolamellar bodieswith atomic force microscopy J Plant Physiol 170 1217-1227
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (2001) Membrane geometry of open prolamellar bodies Protoplasma 215 4-15Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA FOLLOWING ALDEHYDE OSMIUM-TETROXIDEFIXATION J Cell Biol 24 79-93
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell (Edward Arnold London)
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective excitation of photosystems in chloroplasts inside plantleaves observed by near-infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225-238
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur R Garstka M Maksymiec W Kulik ADietler G and Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions astudy of lipid-light-harvesting complex II model membranes Plant Cell 25 2155-2170
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids Nat Rev Mol Cell Biol 14787-802
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Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
22
protrusions (Daum et al 2010 Austin and Staehelin 2011) We showed that the 663
arrangement of spiraling STs and stack forming exactly parallel GT membranes 664
originates very early during grana formation (Figure 5) The next stages (Figure 6 665
and 7) follow this helical pattern of grana arrangement emphasizing its importance 666
for the structural mechanism of grana thylakoid assembly Thus our observation 667
serves as a general pattern of thylakoid biogenesis 668
Our study has provided the spatial models of chloroplast biogenesis that have 669
allowed the reconstruction of the 3D structure of internal membranes of a developing 670
chloroplast It also allowed us to visualize their interconnections and their 671
transformation from a tubular arrangement to a linear one We show that the tubular 672
structure of the prolamellar body transforms directly into flat slats without dispersion 673
to vesicles a matter that has been the subject of debate We have also 674
demonstrated that the helical character of the grana-stroma thylakoid connections is 675
observed from the beginning of the formation process of the stacked membrane 676
arrangement Moreover we have described the importance of particular CP complex 677
components in the membrane appression during biogenesis The main stages of the 678
biogenesis of the plastid internal membrane network are presented by a dynamic 679
model in the associated movie (Supplemental File 1) 680
681
METHODS 682
Plant Material and Growth Conditions 683
Runner bean (Phaseolus coccineus L cv Eureka) seeds were germinated on Petri 684
dishes in darkness After 7 d of germination the seedlings were transferred to 3-L 685
perlite-containing pots with nutrient solution containing 3 mM Ca(NO3)2 15 mM 686
KNO3 12 mM MgSO4 11 mM KH2PO4 01 mM C10H12N2O8FeNa 5 μM CuSO4 2 687
μM MnSO4 times 5 H2O 2 μM ZnSO4 times 7 H2O and 15 nM (NH4)6Mo7O24 times 4 H2O pH 688
60-65 in a climate-controlled room (18degC) for the next 8 d (etiolation) The first 689
samples were collected under photosynthetically inactive dim green light directly after 690
etiolation Then the light was switched on and the growing conditions were changed 691
to 21degC18degC (daynight) with photosynthetic active radiation of 40 μmol photons mminus2 692
sminus1 during a 16-h light8-h dark photoperiod at a relative humidity of 60ndash70 Leaf 693
samples were taken at selected collection times during the 3 d of the experiment 694
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
Parsed CitationsAbdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) High salt stress induces swollen prothylakoids indark-grown wheat and alters both prolamellar body transformation and reformation after irradiation J Exp Bot 58 2553-2564
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ Biophotonics International 11 36-42Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of thylakoid networks in angiosperms knowns andunknowns Plant Mol Biol 76 221-234
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend beyond the Flatland of cell membraneorganization J Cell Biol 173 839-844
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic membranes the missing dimension of cellmembrane organization Int Rev Cell Mol Biol 274 275-342
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the structure and function of photosystem II in higherplant thylakoid membranes the grana enigma Photosynth Res 98 575-587
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R and Dekker JP (2005) Origin of the F685 andF695 fluorescence in photosystem II Photosynth Res 84 173-180
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants asdetermined by electron tomography Plant Physiol 155 1601-1611
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
23
(Supplemental Figure 1) Sample selection was based on our preliminary 695
experiments which indicated that these moments correspond to significant steps in 696
chloroplast biogenesis Samples from each stage of development were taken for 697
various measurements as required transmission electron microscopy (TEM) 698
electron tomography (ET) confocal laser scanning microscopy (CLSM) as well as 699
for the fluorescence measurements and at the same time for electrophoresis and 700
immunoblotting The sample collection times corresponding to the structural stages 701
are labeled according to the number of days and hours of illumination (eg 12 702
denotes two hours of illumination during the first day of illuminated growth) Seven 703
stages from three days of greening were analyzed by ET paracrystalline prolamellar 704
body (stage 10) irregular prolamellar body (stage 11) remnants of PLB and 705
numerous prothylakoids (stage 12) parallel prothylakoids (stage 14) first stacked 706
membranes (stage 18) from the second day - small grana (stage 20) and from the 707
third day ndash more developed grana (stage 33) Additionally the last two stages of the 708
daynight growth were also analyzed via CLSM 709
710
Transmission Electron Microscopy (TEM) 711
Samples from each developmental stage were taken for the TEM analysis Material 712
cut from the middle part of the leaf was fixed in 25 glutaraldehyde in 005 M 713
cacodylate buffer (pH 74) for 2 h washed in buffer and post-fixed in 2 OsO4 at 4ordmC 714
in 005 M cacodylate buffer for approximately 12 h We used glutaraldehyde as a 715
preferred primary fixative in protocols for the preservation of paracrystalline 716
arrangements (Chong and Deng 2012) Immediately after that the specimens were 717
dehydrated in a graded acetone series and then embedded in epoxy resin (Epon 718
Sigma-Aldrich) Polymerization was performed at 50degC for 3 d The material was cut 719
on a Leica UCT ultramicrotome into 70-nm sections Specimens on nickel 720
formvarded grids with 100 mesh were stained with uranyl acetate and lead citrate 721
and examined with the JEM 1400 electron microscope (Jeol Japan) of the Nencki 722
Institute of the Polish Academy of Sciences Warsaw 723
724
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
24
Grana Measurements and Statistical Analysis 725
Based on the TEM micrographs of the 18 20 and 33 developmental stages we 726
measured the diameter height and number of membrane layers for 100 grana in 727
each of the analyzed stages using ImageJ software (Abramoff et al 2004) From 728
these data we calculated the stacking repeat distance (SRD) which is defined as the 729
distance between the adjacent partition gaps in the stacks (Kirchhoff et al 2011) 730
The analysis of the changes in grana regularity was based on these data We have 731
also introduced a parameter named granum lateral irregularity (GLI) as a measure of 732
grana stack irregularity The GLI value is defined as the coefficient of variation (the 733
ratio of the standard deviation to the mean) of membrane diameters within the 734
granum The minimum theoretically possible GLI value of 0 would be attained for 735
grana consisting of membranes of the same diameter the larger the irregularity 736
(diameter fluctuations) the larger the GLI value The relative variation gives a better 737
measure of irregularity than an absolute one for many reasons in particular chord 738
error caused by measurements of random cross-sections of grana stacks influences 739
the absolute values more than the relative ones 740
An analysis of the measurement protocol drew attention to an ambiguity in the 741
definition of the ending positions of stacked membranes that led us to omit two-742
membrane stacks from the statistical analysis This was in order to eliminate a 743
potential source of artefacts in the membrane diameter calculation 744
To compare the GLI values between stages we found the interval estimates (at 95 745
confidence level) of the GLI ratios for pairs of stages Whenever possible we also 746
performed such a comparison separately for classes of grana consisting of the same 747
number of membranes This was to avoid possible artefacts due to a potential 748
dependence of the diameter measurement on the number of membranes To 749
compare the vertical compactness between stages we found the interval estimates 750
(at 95 confidence level) of the SRD ratios between respective stages For 751
consistency two-membrane grana were also omitted The statistical analysis was 752
performed using SAS 94 (SAS Institute 2013) 753
The tendency of grana to grow in the vertical or lateral direction was quantified as 754
follows First the lateral growth tendency was expressed as a ratio of the lateral 755
growth to the vertical growth during transition between stages Next the ratios of 756
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
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Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
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41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
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Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes J Biol Chem 29014091-14106
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Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with protochlorophyll and protochlorophyllide forms in theunder-soil epicotyl segments of pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 148 307-315
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes Biochim Biophys Acta 1541 91-101Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms BiochimBiophys Acta 1847 838-848
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Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
Supplemental Data contentsuppl20160322tpc1501053DC2html contentsuppl20160321tpc1501053DC1html
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is available atPlant Physiology and The Plant CellSubscription Information for
ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
25
these quantities found for the stage 20 to 33 and the stage 18 to 20 transitions 757
were calculated This ratio is a measure of the tendency of the lateralvertical growth 758
change between the transitions The interval estimates (at 95 confidence level) of 759
these ratios were found using a simple percentile bootstrap and the standard normal 760
bootstrap (Manly 1997) 761
762
Electron Tomography (ET) 763
Samples for the electron tomography were cut into 250 nm thick sections and placed 764
on 100 mesh nickel formvarded grids The electron tomograms were collected with 765
the JEM 1400 electron microscope (Jeol Japan) of the Nencki Institute of the Polish 766
Academy of Sciences Warsaw with tomography supply at the voltage of 120 kV 767
The images were taken at a magnification of 60000times from +60deg to minus60deg at 1deg 768
intervals around one axis When necessary for alignment colloidal gold was 769
precipitated onto grids containing thick sections Forty tomograms from seven 770
developmental stages were collected Each set of aligned single-axis tomogram tilts 771
was reconstructed using the TomoJ software (component of ImageJ) (MessaoudiI et 772
al 2007) For the reconstruction 30 iterations of the SIRT algorithm or 15 iterations 773
of the ART algorithm were applied (MessaoudiI et al 2007) depending on the 774
quality of the reconstructed image stacks Tomograms were displayed and analyzed 775
with the Imaris software to create the isosurface of the internal plastid membranes 776
Additionally the outlines of regions of interest of the tomograms were shaped and 777
analyzed with the 3DMOD software (IMOD) (Kremer et al 1996) in order to 778
reconstruct selected areas of the developing chloroplast membranes 3D theoretical 779
models of PLB units were created with the help of 3ds max software (Autodesk Inc 780
USA) 781
782
Confocal Laser Scanning Microscopy (CLSM) and 3D Reconstruction 783
Etioplasts and developing chloroplasts were isolated in a semi-frozen 20 mM Tricine-784
NaOH (pH 75) buffer containing 330 mM sorbitol 40 mM ascorbate 15 mM NaCl 785
and 4 mM MgCl2 by gentle homogenization After filtration homogenates were 786
centrifuged at 7000 g for 10 min (first day of experiment) or at 2000 g for 5 min 787
(second and third day of experiment) Pellets obtained in such a way were very 788
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
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41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
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Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
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Mysliwa-Kurdziel B Kruk J and Strzalka K (2013) Protochlorophyllide in model systems--an approach to in vivo conditionsBiophys Chem 175-176 28-38
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Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture and dynamics of the photosynthetic apparatus inhigher plants Plant J Cell Mol Biol 70 157-176
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Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts J Cell Sci 6 243-255Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) Identification of the carotenoid isomerase providesinsight into carotenoid biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 321-332
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Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and prothylakoids fractionated from wheat etioplastsPhysiol Plant 56 125-132
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SAS Institute Inc 2013 SASSTATreg 123 Users Guide Cary NC SAS Institute IncPubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH protochlorophyllide oxidoreductase in primary bean leaves(Phaseolus vulgaris) during the first days of photoperiodic growth Photosynth Res 96 15-26
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Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In Lipids in Photosynthesis Structure Functionand Genetics S Paul-Andreacute and M Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 209-224
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Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
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Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
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Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-dimensional organization of higher-plant chloroplastthylakoid membranes revealed by electron tomography Plant Cell 17 2580-2586
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Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P Holzenburg A and Garab G (2000) Self-assemblyof large ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S A 97 1473-1476
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Google Scholar Author Only Title Only Author and Title
Solymosi K Mysliwa-Kurdziel B Boacuteka K Strzalka K and Boumlddi B (2006) Disintegration of the Prolamellar Body Structure atHigh Concentrations of Hg 2+ Plant Biol 8 627-635
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Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions the dark side of chlorophyllbiosynthesis in angiosperms Photosynth Res 105 143-166
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Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in sunflower (Helianthus annuus) cotyledons partiallycovered by the pericarp of the achene Ann Bot 99 857-867
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W (2005) Mechanisms of photoprotection andnonphotochemical quenching in pea light-harvesting complex at 25 A resolution EMBO J 24 919-928
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of chloroplast biogenesis maize as a model systemTrends Plant Sci 9 293-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for development and homeostasis Biochim Biophys Acta1847 809-820
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of glycophorin on lipid polymorphism A 31P-NMRstudy Biochim Biophys Acta 685 153-161
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Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes J Biol Chem 29014091-14106
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with protochlorophyll and protochlorophyllide forms in theunder-soil epicotyl segments of pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 148 307-315
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes Biochim Biophys Acta 1541 91-101Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms BiochimBiophys Acta 1847 838-848
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
Supplemental Data contentsuppl20160322tpc1501053DC2html contentsuppl20160321tpc1501053DC1html
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
26
gently resuspended in a small amount of 20 mM HEPES-NaOH (pH 70) buffer 789
containing 330 mM sorbitol 15 mM NaCl 4 mM MgCl2 790
Isolated intact chloroplasts were suspended in 20 mM HEPES-NaOH (pH 75) 791
containing 330 mM sorbitol 6 (vv) glycerol 15 mM NaCl 4 mM MgCl2 to a final 792
Chl concentration of 30 μg mL-1 After 10 min of incubation in the dark and on ice the 793
suspension was immobilized on a microscope glass covered with poly-L-lysine 794
(Rumak et al 2010) Chloroplast images from three independent experiments were 795
taken using the Nikon A1 MP confocal laser scanning fluorescence microscope as 796
described previously (Janik et al 2013) Briefly the excitation beam was set at 561 797
nm and fluorescence emission was recorded in the range of 662 to 737 nm 798
Fluorescence images of 512 times 512 pixels were collected from different focal planes (z 799
axis step = 25 nm) using a fast resonant scanner with the scanning speed of 15 800
frames per second and each optical slice was an average of 16 separate frames 801
The collected data stacks were subjected to a deconvolution procedure using the 802
AutoQuant X3 software (Media Cybernetics Inc USA) to remove the spherical 803
aberration effect and unspecific fluorescence signals The deconvolution parameter 804
values were chosen to maximize the image quality while keeping a minimal data 805
loss which corresponds to 10 iterations with a medium noise level The 3D models 806
were created based on the algorithm of the intensity gradient using Imaris 631 807
software (Bitplane AG Switzerland) (Rumak et al 2012) 808
809
Low-Temperature (77K) Fluorescence Measurements 810
A modified Cary Eclipse (Varian Inc Australia) spectrofluorimeter with optical fibers 811
guiding the excitation and emission beams was used to record the low temperature 812
(77 K) fluorescence emission and excitation spectra Samples containing 813
preparations of etioplasts or developing chloroplasts were placed in a 814
polytetrafluoroethylene cuvette and subsequently submerged in liquid nitrogen The 815
emission spectra were recorded in the range of 600 to 800 nm with the wavelength of 816
the excitation beam set at 440 nm The fluorescence excitation spectra were 817
recorded in the range of 350 to 600 nm and the emission was set at the center of the 818
main emission bands of the analyzed samples All spectra were recorded through the 819
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
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41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
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Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
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Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-dimensional organization of higher-plant chloroplastthylakoid membranes revealed by electron tomography Plant Cell 17 2580-2586
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Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P Holzenburg A and Garab G (2000) Self-assemblyof large ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S A 97 1473-1476
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Google Scholar Author Only Title Only Author and Title
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Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in sunflower (Helianthus annuus) cotyledons partiallycovered by the pericarp of the achene Ann Bot 99 857-867
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Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W (2005) Mechanisms of photoprotection andnonphotochemical quenching in pea light-harvesting complex at 25 A resolution EMBO J 24 919-928
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of chloroplast biogenesis maize as a model systemTrends Plant Sci 9 293-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for development and homeostasis Biochim Biophys Acta1847 809-820
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of glycophorin on lipid polymorphism A 31P-NMRstudy Biochim Biophys Acta 685 153-161
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes J Biol Chem 29014091-14106
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Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with protochlorophyll and protochlorophyllide forms in theunder-soil epicotyl segments of pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 148 307-315
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes Biochim Biophys Acta 1541 91-101Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms BiochimBiophys Acta 1847 838-848
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Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
Supplemental Data contentsuppl20160322tpc1501053DC2html contentsuppl20160321tpc1501053DC1html
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
27
LP610 emission filter and the excitation spectra were corrected for the Xenon lamp 820
intensity 821
Mild Denaturing Electrophoresis 822
Etioplastchloroplast membranes were solubilized in a 10 mM Tricine buffer (pH 76) 823
containing 20 (wv) sucrose to a Chl concentration of 05 mg mL-1 Next the n-824
dodecyl-β-D-maltopyranoside and lithium dodecylsulfate were added to a final 825
concentration of 05 (wv) and 005 (wv) respectively After 20 min of dark 826
incubation on ice samples containing 4 μg of Chl were loaded into wells of an SDS-827
depleted 3 (wv) polyacrylamide stacking gel Electrophoresis was performed using 828
a SDS-depleted 8 (wv) polyacrylamide resolving gel supplemented with 10 (wv) 829
sucrose The electrophoresis was conducted with a 25 mM Tris buffer (pH 83) 830
containing 192 mM glycine and 01 (wv) lithium dodecylsulfate in a MiniProtean3 831
electrophoresis cell (Bio-Rad Laboratories USA) 832
SDS-PAGE and Immunoblot Analysis 833
Isolated etioplastschloroplasts were suspended in Laemmli Sample Buffer (Bio-Rad 834
Laboratories USA) and samples containing an equal amount of protein were loaded 835
into polyacrylamide gel wells After separation by the standard SDS-PAGE proteins 836
were detected on the PVDF membrane by using primary antibodies against D1 D2 837
CP43 CP47 Lhcb1 and Lhcb2 (Agrisera Sweden) followed by anti-rabbit 838
horseradish peroxidase conjugate and ECL Detection System (Bio-Rad Laboratories 839
USA) Primary and secondary antibodies were diluted according to the 840
manufacturers protocols Agrisera and Bio-Rad respectively 841
842
SUPPLEMENTAL DATA 843
Supplemental Movie 1 is available at datadryadorg doixxxxx 844
Supplemental Figure 1 Scheme of the Experiment 845
Supplemental Figure 2 Theoretical Model of the Hexagonal Lattice 846
Supplemental Figure 3 Model of the Chl Fluorescence of Intact Chloroplasts 847
(CLSM) and 3D Reconstruction of Grana Distribution at the 20 Developmental 848
Stage 849
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
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Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
Supplemental Data contentsuppl20160322tpc1501053DC2html contentsuppl20160321tpc1501053DC1html
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
28
Supplemental Figure 4 Model of the Chl Fluorescence of Intact Chloroplasts 850
(CLSM) and 3D Reconstruction of Grana Distribution at the 33 Developmental 851
Stage 852
Supplemental Figure 5 Distribution of Grana Size in the 18 20 and 33 853
Developmental Stages 854
Supplemental Table 1 Characterization of the Chloroplast Grana from the 18 20 855
and 33 Developmental Stages 856
Supplemental Table 2 Ratios of the Geometric Means of GLI for Pairs of Stages 857
Grana Consisting of Different Number of Membranes (gt2) Taken Together 858
Supplemental Table 3 Ratios of the Geometric Means of GLI for Pairs of Stages 859
Calculated Separately for Grana Consisting of a Particular Number of Membranes 860
Supplemental Table 4 Ratios of the Geometric Means of SRD for Pairs of Stages 861
Grana Consisting of Different Number of Membranes (gt2) Taken Together 862
Supplemental Table 5 Spearman Rank Correlations Between the Granum Height 863
and Number of Membranes (when gt2) for Subsequent Stages 864
Supplemental Table 6 Tendency of Grana for the Lateral or Vertical Enlargement 865
and its Change in Subsequent Stage-to-Stage Transitions 866
Supplemental Movie 1 Video (MOV) File Presenting the Dynamic Model of the 867
Chloroplast Biogenesis Based on the Electron Tomography Reconstructions of 868
Seven Subsequent Developmental Stages and on 2D Theoretical Models 869
Supplemental Movie 1 Legend 870
871
ACKNOWLEDGEMENTS 872
This work was supported by the Polish Ministry of Science and Higher Education 873
Grant N N303 530438 874
TEM images were performed in the Laboratory of Electron Microscopy Nencki 875
Institute of Experimental Biology using a JEM 1400 electron microscope (JEOL Co 876
Japan) This equipment was installed within the project sponsored by the EU 877
Structural Funds Centre of Advanced Technology BIM ndash Equipment purchase for the 878
Laboratory of Biological and Medical Imaging The authors thank Dr Tomasz 879
Wyszomirski for his help in the statistical analysis Prof Wiesław I Gruszecki for 880
making available the Cary Eclipse spectrofluorimeter and Dr Piotr Deuar for critical 881
reading of the manuscript 882
883
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
29
Authors contribution 884
ŁK RM AM MG designed the research ŁK RM SS performed measurements ŁK 885
RM MG analyzed data AM ŁK RM MG wrote the paper 886
887
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
Parsed CitationsAbdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) High salt stress induces swollen prothylakoids indark-grown wheat and alters both prolamellar body transformation and reformation after irradiation J Exp Bot 58 2553-2564
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ Biophotonics International 11 36-42Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of thylakoid networks in angiosperms knowns andunknowns Plant Mol Biol 76 221-234
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend beyond the Flatland of cell membraneorganization J Cell Biol 173 839-844
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic membranes the missing dimension of cellmembrane organization Int Rev Cell Mol Biol 274 275-342
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the structure and function of photosystem II in higherplant thylakoid membranes the grana enigma Photosynth Res 98 575-587
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R and Dekker JP (2005) Origin of the F685 andF695 fluorescence in photosystem II Photosynth Res 84 173-180
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants asdetermined by electron tomography Plant Physiol 155 1601-1611
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of photosystem II units Philos Trans R Soc LondB Biol Sci 357 1451-1459 discussion 1459-1460
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale genetic analysis of chloroplast biogenesis in maizeBiochim Biophys Acta 1847 1004-1016
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals theirsignificance in chloroplast development Photosynth Res 96 37-50
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The two spectroscopically different short wavelengthprotochlorophyllide forms in pea epicotyls are both monomeric Biochim Biophys Acta 1365 531-540
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast RNA polymerases Role in chloroplast biogenesisBiochim Biophys Acta 1847 761-769
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR (2010) Energy transfer processes in the isolated
core antenna complexes CP43 and CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606-1616Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain and loss of photosynthetic membranes duringplastid differentiation in the shoot apex of Arabidopsis Plant Cell 24 1143-1157
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar to cubic membrane transition as investigatedby electron microscopy Methods Cell Biol 108 319-343
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of thylakoid membranes in higher plant chloroplaststhe physicochemical forces at work and the functional consequences that ensue Photochem Photobiol Sci Off J EurPhotochem Assoc Eur Soc Photobiol 4 1081-1090
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
DallOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting proteins Biochim Biophys Acta 1847 861-871Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) Quantification of photosystem I and II in different parts of thethylakoid membrane from spinach Biochim Biophys Acta 1608 53-61
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-M and Mamedov F (2006) Dimeric andmonomeric organization of photosystem II Distribution of five distinct complexes in the different domains of the thylakoidmembrane J Biol Chem 281 14241-14249
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid membranes J Exp Bot 62 2393-2402Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) Arrangement of photosystem II and ATP synthase inchloroplast membranes of spinach and pea Plant Cell 22 1299-1312
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants BiochimBiophys Acta 1706 12-39
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses subvert cholesterol homeostasis to induce host cubicmembranes Trends Cell Biol 20 371-379
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane structure in the mitochondria of amoebaeChaos carolinensis Protoplasma 20316-25
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA (1999) Cubic membrane structure in amoeba(Chaos carolinensis) mitochondria determined by electron microscopic tomography J Struct Biol 127 231-239
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister W (2015) Native architecture of theChlamydomonas chloroplast revealed by in situ cryo-electron tomography eLife 4
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
30
FIGURE LEGENDS 888
Figure 1 Model of the Paracrystalline Tubular Structure of a Prolamellar Body 889
(PLB) after Eight Days of Etiolation (Stage 10) 890
(A) Middle layer of the tomography stack 891
(B) Volume of the 3D reconstructed PLB 892
(C) and (D) Isosurface visualization with magnification showing a regular 893
paracrystalline network The image in (D) shows a magnification of the light-colored 894
surface area in (C) 895
(E) Isosurface view of a single PLB unit (orange) 896
(F) and (G) Magnification of a PLB unit viewed from two different angles (orange) 897
(H) Theoretical model of a single layer of the PLB network (3ds max) 898
All bars = 250 nm 899
900
Figure 2 Model of the PLB Irregular Structure after one Hour of Illumination 901
(Stage 11) 902
(A) Middle layer of the tomography stack 903
(B) Volume of the 3D reconstructed irregular PLB 904
(C) and (D) Isosurface visualization with magnification Note the lamellar character of 905
porous (arrowheads) prothylakoids at the PLB edges The image in (D) shows a 906
magnification of the part of the light-colored surface area in (C) PT prothylakoid 907
(E) (F) (G) (H) magnification of the irregular PLB network viewed from four different 908
angles showing a portion of a degraded PLB unit (lime green) forming sheet-like 909
structures (SLS) 910
All bars = 500 nm 911
912
Figure 3 Model of Degraded PLB Structure with Numerous PTs in Plastid 913
Stroma after Two Hours of Illumination (Stage 12) 914
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
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Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
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Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-M and Mamedov F (2006) Dimeric andmonomeric organization of photosystem II Distribution of five distinct complexes in the different domains of the thylakoidmembrane J Biol Chem 281 14241-14249
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Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid membranes J Exp Bot 62 2393-2402Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
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Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses subvert cholesterol homeostasis to induce host cubicmembranes Trends Cell Biol 20 371-379
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane structure in the mitochondria of amoebaeChaos carolinensis Protoplasma 20316-25
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA (1999) Cubic membrane structure in amoeba(Chaos carolinensis) mitochondria determined by electron microscopic tomography J Struct Biol 127 231-239
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister W (2015) Native architecture of theChlamydomonas chloroplast revealed by in situ cryo-electron tomography eLife 4
Pubmed Author and Title
CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gabruk M Stecka A Strzalka W Kruk J Strzalka K and Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzymecomplexes reconstituted with PORA PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS One 10e0116990
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes Biochim Biophys Acta 1837 481-494Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
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Grzyb JM Solymosi K Strzalka K and Mysliwa-Kurdziel B (2013) Visualization and characterization of prolamellar bodieswith atomic force microscopy J Plant Physiol 170 1217-1227
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Gunning BE (2001) Membrane geometry of open prolamellar bodies Protoplasma 215 4-15Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA FOLLOWING ALDEHYDE OSMIUM-TETROXIDEFIXATION J Cell Biol 24 79-93
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell (Edward Arnold London)
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective excitation of photosystems in chloroplasts inside plantleaves observed by near-infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225-238
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur R Garstka M Maksymiec W Kulik ADietler G and Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions astudy of lipid-light-harvesting complex II model membranes Plant Cell 25 2155-2170
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids Nat Rev Mol Cell Biol 14787-802
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems experimentally-investigated entropy-driven stackingof plant photosynthetic membranes Sci Rep 4 4142
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes BiochimBiophys Acta 1708 187-195
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P Gruissem W and Baginsky S (2007)Proteome dynamics during plastid differentiation in rice Plant Physiol 143 912-923
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED ANDFAR-RED LIGHT J Cell Biol 22 433-442
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV Dekker JP and Jansson S (2005) Structureof the higher plant light harvesting complex I in vivo characterization and structural interdependence of the Lhca proteinsBiochemistry (Mosc) 44 3065-3073
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) Protein assembly and heat stability in developingthylakoid membranes during greening Proc Natl Acad Sci U S A 99 12149-12154
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kouril R Dekker JP and Boekema EJ (2012) Supramolecular organization of photosystem II in green plants BiochimBiophys Acta 1817 2-12
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization of Three-Dimensional Image Data Using IMODJ Struct Biol 116 71-76
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 655-659
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-proteasome system in plastid developmentBiochim Biophys Acta 1847 939-948
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
31
(A) Middle layer of the tomography stack 915
(B) Magnification of the modeled region (blue) 916
(C) (D) Surface model (blue) embedded in the middle TEM layer viewed from two 917
different angles 918
(E) (F) (G) Surface visualization from three different angles showing the radial 919
arrangement of porous (arrowheads) prothylakoid structures PT prothylakoid 920
All bars = 200 nm 921
922
Figure 4 Model of PTs Loosely Arranged in Plastid Stroma After Four Hours of 923
Illumination (Stage 14) 924
(A) Middle layer of the tomography stack 925
(B) Magnification of the modeled region (purple) 926
(C) (D) Surface model (purple) embedded in the middle TEM layer viewed from two 927
different angles 928
(E) (F) (G) Surface visualization from three different angles showing parallel porous 929
(arrowheads) prothylakoid structures with a locally visible dichotomous split of a 930
prothylakoid (star) PT prothylakoid 931
All bars = 200 nm 932
933
Figure 5 Model of the First Stacked Membranes After Eight Hours of 934
Illumination (Stage 18) 935
(A) Middle layer of the tomography stack 936
(B) Magnification of the modeled region (yellow) 937
(C) (D) Surface model embedded in the selected TEM layer viewed from two 938
different angles 939
(E) (F) (G) (H) Surface visualization from four different angles showing three layers 940
of a non-porous thylakoid stack (light yellow) and associated porous (arrowhead) 941
prothylakoid membrane (yellow) connected with the stacked region at an angle in the 942
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
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Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
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Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
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41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
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Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
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Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P Holzenburg A and Garab G (2000) Self-assemblyof large ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S A 97 1473-1476
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Sun Y and Zerges W (2015) Translational regulation in chloroplasts for development and homeostasis Biochim Biophys Acta1847 809-820
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of glycophorin on lipid polymorphism A 31P-NMRstudy Biochim Biophys Acta 685 153-161
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes J Biol Chem 29014091-14106
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with protochlorophyll and protochlorophyllide forms in theunder-soil epicotyl segments of pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 148 307-315
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes Biochim Biophys Acta 1541 91-101Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms BiochimBiophys Acta 1847 838-848
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
32
range of 18-33deg with a locally visible splitting of a prothylakoid (star) PT 943
prothylakoid GT grana thylakoid 944
All bars = 250 nm 945
946
Figure 6 Model of Small Grana at the Beginning of the Second Day of the 947
Experiment (Stage 20) 948
(A) Middle layer of the tomography stack 949
(B) Magnification of the modeled region (green) 950
(C) (D) Surface model embedded in the selected TEM layer viewed from two 951
different angles 952
(E) (F) (G) (H) (I) Surface visualization from five different angles showing five 953
grana thylakoid layers (light green) arranged in parallel These grana are directly 954
connected with three non-porous stroma thylakoids (green) The stroma thylakoids 955
are connected with a stacked region at an angle of approximately 20deg GT grana 956
thylakoid ST stroma thylakoid 957
All bars = 200 nm 958
959
Figure 7 Model of More Developed Grana Visible During the Third Day of 960
DayNight Growth (Stage 33) 961
(A) Middle layer of the tomography stack 962
(B) Magnification of the modeled region (green) 963
(C) (D) Surface model embedded in the selected TEM layer viewed from two 964
different angles 965
(E) (F) (G) (H) (I) Surface visualization from five different angles showing a very 966
regular parallel arrangement of grana thylakoid layers (light navy) associated with six 967
stroma thylakoids (navy) 968
(F) Splitting of the bottom stroma thylakoid (star) 969
33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
Parsed CitationsAbdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) High salt stress induces swollen prothylakoids indark-grown wheat and alters both prolamellar body transformation and reformation after irradiation J Exp Bot 58 2553-2564
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ Biophotonics International 11 36-42Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of thylakoid networks in angiosperms knowns andunknowns Plant Mol Biol 76 221-234
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend beyond the Flatland of cell membraneorganization J Cell Biol 173 839-844
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic membranes the missing dimension of cellmembrane organization Int Rev Cell Mol Biol 274 275-342
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the structure and function of photosystem II in higherplant thylakoid membranes the grana enigma Photosynth Res 98 575-587
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R and Dekker JP (2005) Origin of the F685 andF695 fluorescence in photosystem II Photosynth Res 84 173-180
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants asdetermined by electron tomography Plant Physiol 155 1601-1611
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of photosystem II units Philos Trans R Soc LondB Biol Sci 357 1451-1459 discussion 1459-1460
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale genetic analysis of chloroplast biogenesis in maizeBiochim Biophys Acta 1847 1004-1016
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals theirsignificance in chloroplast development Photosynth Res 96 37-50
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The two spectroscopically different short wavelengthprotochlorophyllide forms in pea epicotyls are both monomeric Biochim Biophys Acta 1365 531-540
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast RNA polymerases Role in chloroplast biogenesisBiochim Biophys Acta 1847 761-769
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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33
(G) Stroma thylakoids are connected with two neighboring grana thylakoids at an 970
angle of approximately 18deg 971
(H) (I) A particular stroma thylakoid is split in two and connected with the adjacent 972
grana thylakoid (H) and with the next grana thylakoid in another slice (I) as shown 973
inside the small white rectangles GT grana thylakoid ST stroma thylakoid 974
All bars = 200 nm 975
976
Figure 8 Theoretical 2D Models of Subsequent Stages of Inner Chloroplast 977
Membrane Transformations 978
Membrane transformations during the etioplast-chloroplast transition induced by 979
illumination with the corresponding developmental stages illustrated (left panels) and 980
visualized by TEM (right panels) The theoretical models show membrane 981
connections at a selected depth on the Z axis of the chloroplast volume Bars = 200 982
nm 983
984
Figure 9 Analysis of CP Complexes During the Biogenesis of Chloroplasts 985
(A) Low temperature (77K) fluorescence emission spectra (excitation at 440 nm) of 986
isolated intact bean etioplasts and developing chloroplasts from subsequent 987
developmental stages as shown in the key at upper right 988
(B) and (C) Low temperature (77K) fluorescence excitation spectra obtained from 989
emission at 653 nm (stage 10) 680 nm (stage 11) or 683 nm (stages 12 to 33) 990
(line styles are the same as on panel A) 991
(D) Mild-denaturing green gel electrophoresis of chlorophyll-protein complexes 992
(E) Immunodetection analysis of PSII core (D1 D2 CP43 CP47) and extrinsic 993
antenna (Lhcb1 Lhcb2) proteins All measurements were repeated at least three 994
times all spectra presented were normalized to equal area under the curve 995
996
34
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Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
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Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
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Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
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Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
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Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
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Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
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Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
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Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gabruk M Stecka A Strzalka W Kruk J Strzalka K and Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzymecomplexes reconstituted with PORA PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS One 10e0116990
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Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes Biochim Biophys Acta 1837 481-494Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
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Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
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Grzyb JM Solymosi K Strzalka K and Mysliwa-Kurdziel B (2013) Visualization and characterization of prolamellar bodieswith atomic force microscopy J Plant Physiol 170 1217-1227
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Gunning BE (2001) Membrane geometry of open prolamellar bodies Protoplasma 215 4-15Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA FOLLOWING ALDEHYDE OSMIUM-TETROXIDEFIXATION J Cell Biol 24 79-93
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Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell (Edward Arnold London)
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective excitation of photosystems in chloroplasts inside plantleaves observed by near-infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225-238
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur R Garstka M Maksymiec W Kulik ADietler G and Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions astudy of lipid-light-harvesting complex II model membranes Plant Cell 25 2155-2170
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids Nat Rev Mol Cell Biol 14787-802
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems experimentally-investigated entropy-driven stackingof plant photosynthetic membranes Sci Rep 4 4142
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes BiochimBiophys Acta 1708 187-195
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P Gruissem W and Baginsky S (2007)Proteome dynamics during plastid differentiation in rice Plant Physiol 143 912-923
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED ANDFAR-RED LIGHT J Cell Biol 22 433-442
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV Dekker JP and Jansson S (2005) Structureof the higher plant light harvesting complex I in vivo characterization and structural interdependence of the Lhca proteinsBiochemistry (Mosc) 44 3065-3073
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) Protein assembly and heat stability in developingthylakoid membranes during greening Proc Natl Acad Sci U S A 99 12149-12154
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kouril R Dekker JP and Boekema EJ (2012) Supramolecular organization of photosystem II in green plants BiochimBiophys Acta 1817 2-12
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization of Three-Dimensional Image Data Using IMODJ Struct Biol 116 71-76
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 655-659
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-proteasome system in plastid developmentBiochim Biophys Acta 1847 939-948
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 58 11-26Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid membranes from plastid transcription to proteincomplex assembly Planta 237 413-428
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology Second Edition (CRC Press)
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography software for three-dimensional reconstructionin transmission electron microscopy BMC Bioinformatics 8 288
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings by white red and blue low intensity lightProtoplasma 131 166-173
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986b) Thylakoid and grana formation during the development of pea chloroplasts illuminated by white red andblue low intensity light Protoplasma 134 88-94
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mysliwa-Kurdziel B Kruk J and Strzalka K (2013) Protochlorophyllide in model systems--an approach to in vivo conditionsBiophys Chem 175-176 28-38
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture and dynamics of the photosynthetic apparatus inhigher plants Plant J Cell Mol Biol 70 157-176
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts J Cell Sci 6 243-255Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) Identification of the carotenoid isomerase providesinsight into carotenoid biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 321-332
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development an overview Plant Physiol155 1545-1551
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast biogenesis and development Biochim BiophysActa
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in land plants J Exp Bot 65 1955-1972Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes Biochim Biophys Acta BBA - Bioenerg 1847 821-830
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) The effect of cytochrome c oxidase on lipidpolymorphism of model membranes containing cardiolipin Eur J Biochem FEBS 164 137-140
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and Chlorophyll Synthesis Q Rev Biol 47 160-191Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rudowska L Gieczewska K Mazur R Garstka M and Mostowska A (2012) Chloroplast biogenesis mdash Correlation betweenstructure and function Biochim Biophys Acta BBA - Bioenerg 1817 1380-1387
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur R and Garstka M (2010) 3-D modelling ofchloroplast structure under (Mg2+) magnesium ion treatment Relationship between thylakoid membrane arrangement andstacking Biochim Biophys Acta 1797 1736-1748
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rumak I Mazur R Gieczewska K Koziol-Lipinska J Kierdaszuk B Michalski WP Shiell BJ Venema JH VredenbergWJ Mostowska A and Garstka M (2012) Correlation between spatial (3D) structure of pea and bean thylakoid membranes andarrangement of chlorophyll-protein complexes BMC Plant Biol 12 72
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and prothylakoids fractionated from wheat etioplastsPhysiol Plant 56 125-132
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
SAS Institute Inc 2013 SASSTATreg 123 Users Guide Cary NC SAS Institute IncPubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH protochlorophyllide oxidoreductase in primary bean leaves(Phaseolus vulgaris) during the first days of photoperiodic growth Photosynth Res 96 15-26
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In Lipids in Photosynthesis Structure Functionand Genetics S Paul-Andreacute and M Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 209-224
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-dimensional organization of higher-plant chloroplastthylakoid membranes revealed by electron tomography Plant Cell 17 2580-2586
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P Holzenburg A and Garab G (2000) Self-assemblyof large ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S A 97 1473-1476
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Solymosi K Mysliwa-Kurdziel B Boacuteka K Strzalka K and Boumlddi B (2006) Disintegration of the Prolamellar Body Structure atHigh Concentrations of Hg 2+ Plant Biol 8 627-635
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions the dark side of chlorophyllbiosynthesis in angiosperms Photosynth Res 105 143-166
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in sunflower (Helianthus annuus) cotyledons partiallycovered by the pericarp of the achene Ann Bot 99 857-867
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W (2005) Mechanisms of photoprotection andnonphotochemical quenching in pea light-harvesting complex at 25 A resolution EMBO J 24 919-928
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of chloroplast biogenesis maize as a model systemTrends Plant Sci 9 293-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for development and homeostasis Biochim Biophys Acta1847 809-820
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of glycophorin on lipid polymorphism A 31P-NMRstudy Biochim Biophys Acta 685 153-161
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes J Biol Chem 29014091-14106
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with protochlorophyll and protochlorophyllide forms in theunder-soil epicotyl segments of pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 148 307-315
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes Biochim Biophys Acta 1541 91-101Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms BiochimBiophys Acta 1847 838-848
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
34
REFERENCES 997
Abdelkader AF Aronsson H Solymosi K Boumlddi B and Sundqvist C (2007) 998 High salt stress induces swollen prothylakoids in dark-grown wheat and alters both 999 prolamellar body transformation and reformation after irradiation J Exp Bot 58 1000 2553ndash2564 1001
Abramoff MD Magalhaes PJ Ram SJ (2004) Image Processing with ImageJ 1002 Biophotonics International 11 36ndash42 1003 1004 Adam Z Charuvi D Tsabari O Knopf RR and Reich Z (2011) Biogenesis of 1005 thylakoid networks in angiosperms knowns and unknowns Plant Mol Biol 76 221ndash1006 234 1007
Almsherqi ZA Kohlwein SD and Deng Y (2006) Cubic membranes a legend 1008 beyond the Flatland of cell membrane organization J Cell Biol 173 839ndash844 1009
Almsherqi ZA Landh T Kohlwein SD and Deng Y (2009) Chapter 6 cubic 1010 membranes the missing dimension of cell membrane organization Int Rev Cell Mol 1011 Biol 274 275ndash342 1012
Anderson JM Chow WS and Rivas JDL (2008) Dynamic flexibility in the 1013 structure and function of photosystem II in higher plant thylakoid membranes the 1014 grana enigma Photosynth Res 98 575ndash587 1015
Andrizhiyevskaya EG Chojnicka A Bautista JA Diner BA van Grondelle R 1016 and Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II 1017 Photosynth Res 84 173ndash180 1018
Austin JR and Staehelin LA (2011) Three-dimensional architecture of grana and 1019 stroma thylakoids of higher plants as determined by electron tomography Plant 1020 Physiol 155 1601ndash1611 1021
Baena-Gonzaacutelez E and Aro E-M (2002) Biogenesis assembly and turnover of 1022 photosystem II units Philos Trans R Soc Lond B Biol Sci 357 1451ndash1459 1023 discussion 1459ndash1460 1024
Belcher S Williams-Carrier R Stiffler N and Barkan A (2015) Large-scale 1025 genetic analysis of chloroplast biogenesis in maize Biochim Biophys Acta 1847 1026 1004ndash1016 1027
Blomqvist LA Ryberg M and Sundqvist C (2008) Proteomic analysis of highly 1028 purified prolamellar bodies reveals their significance in chloroplast development 1029 Photosynth Res 96 37ndash50 1030
Boumlddi null Kis-Petik null Kaposi null Fidy null and Sundqvist null (1998) The 1031 two spectroscopically different short wavelength protochlorophyllide forms in pea 1032 epicotyls are both monomeric Biochim Biophys Acta 1365 531ndash540 1033
Boumlrner T Aleynikova AY Zubo YO and Kusnetsov VV (2015) Chloroplast 1034 RNA polymerases Role in chloroplast biogenesis Biochim Biophys Acta 1847 1035 761ndash769 1036
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Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
35
Casazza AP Szczepaniak M Muumlller MG Zucchelli G and Holzwarth AR 1037 (2010) Energy transfer processes in the isolated core antenna complexes CP43 and 1038 CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606ndash1616 1039
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain 1040 and loss of photosynthetic membranes during plastid differentiation in the shoot apex 1041 of Arabidopsis Plant Cell 24 1143ndash1157 1042
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar 1043 to cubic membrane transition as investigated by electron microscopy Methods Cell 1044 Biol 108 319ndash343 1045
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of 1046 thylakoid membranes in higher plant chloroplasts the physicochemical forces at work 1047 and the functional consequences that ensue Photochem Photobiol Sci Off J Eur 1048 Photochem Assoc Eur Soc Photobiol 4 1081ndash1090 1049
DallrsquoOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting 1050 proteins Biochim Biophys Acta 1847 861ndash871 1051
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) 1052 Quantification of photosystem I and II in different parts of the thylakoid membrane 1053 from spinach Biochim Biophys Acta 1608 53ndash61 1054
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-1055 M and Mamedov F (2006) Dimeric and monomeric organization of photosystem II 1056 Distribution of five distinct complexes in the different domains of the thylakoid 1057 membrane J Biol Chem 281 14241ndash14249 1058
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid 1059 membranes J Exp Bot 62 2393ndash2402 1060
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) 1061 Arrangement of photosystem II and ATP synthase in chloroplast membranes of 1062 spinach and pea Plant Cell 22 1299ndash1312 1063
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid 1064 membrane proteins in green plants Biochim Biophys Acta 1706 12ndash39 1065
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses 1066 subvert cholesterol homeostasis to induce host cubic membranes Trends Cell Biol 1067 20 371ndash379 1068
Deng Y and Mieczkowski M (1998) Three-dimensional periodic cubic membrane 1069 structure in the mitochondria of amoebae Chaos carolinensis Protoplasma 20316ndash1070 25 1071 1072 Deng Y Marko M Buttle KF Leith A Mieczkowski M and Mannella CA 1073 (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria 1074 determined by electron microscopic tomography J Struct Biol 127 231ndash239 1075
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
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Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
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Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
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Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
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Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
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Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
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Grzyb JM Solymosi K Strzalka K and Mysliwa-Kurdziel B (2013) Visualization and characterization of prolamellar bodieswith atomic force microscopy J Plant Physiol 170 1217-1227
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Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA FOLLOWING ALDEHYDE OSMIUM-TETROXIDEFIXATION J Cell Biol 24 79-93
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Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell (Edward Arnold London)
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective excitation of photosystems in chloroplasts inside plantleaves observed by near-infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225-238
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur R Garstka M Maksymiec W Kulik ADietler G and Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions astudy of lipid-light-harvesting complex II model membranes Plant Cell 25 2155-2170
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Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids Nat Rev Mol Cell Biol 14787-802
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Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems experimentally-investigated entropy-driven stackingof plant photosynthetic membranes Sci Rep 4 4142
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes BiochimBiophys Acta 1708 187-195
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P Gruissem W and Baginsky S (2007)Proteome dynamics during plastid differentiation in rice Plant Physiol 143 912-923
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED ANDFAR-RED LIGHT J Cell Biol 22 433-442
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV Dekker JP and Jansson S (2005) Structureof the higher plant light harvesting complex I in vivo characterization and structural interdependence of the Lhca proteinsBiochemistry (Mosc) 44 3065-3073
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) Protein assembly and heat stability in developingthylakoid membranes during greening Proc Natl Acad Sci U S A 99 12149-12154
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kouril R Dekker JP and Boekema EJ (2012) Supramolecular organization of photosystem II in green plants BiochimBiophys Acta 1817 2-12
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization of Three-Dimensional Image Data Using IMODJ Struct Biol 116 71-76
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 655-659
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-proteasome system in plastid developmentBiochim Biophys Acta 1847 939-948
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 58 11-26Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid membranes from plastid transcription to proteincomplex assembly Planta 237 413-428
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology Second Edition (CRC Press)
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography software for three-dimensional reconstructionin transmission electron microscopy BMC Bioinformatics 8 288
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings by white red and blue low intensity lightProtoplasma 131 166-173
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986b) Thylakoid and grana formation during the development of pea chloroplasts illuminated by white red andblue low intensity light Protoplasma 134 88-94
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mysliwa-Kurdziel B Kruk J and Strzalka K (2013) Protochlorophyllide in model systems--an approach to in vivo conditionsBiophys Chem 175-176 28-38
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture and dynamics of the photosynthetic apparatus inhigher plants Plant J Cell Mol Biol 70 157-176
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts J Cell Sci 6 243-255Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) Identification of the carotenoid isomerase providesinsight into carotenoid biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 321-332
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development an overview Plant Physiol155 1545-1551
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast biogenesis and development Biochim BiophysActa
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in land plants J Exp Bot 65 1955-1972Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes Biochim Biophys Acta BBA - Bioenerg 1847 821-830
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) The effect of cytochrome c oxidase on lipidpolymorphism of model membranes containing cardiolipin Eur J Biochem FEBS 164 137-140
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and Chlorophyll Synthesis Q Rev Biol 47 160-191Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rudowska L Gieczewska K Mazur R Garstka M and Mostowska A (2012) Chloroplast biogenesis mdash Correlation betweenstructure and function Biochim Biophys Acta BBA - Bioenerg 1817 1380-1387
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur R and Garstka M (2010) 3-D modelling ofchloroplast structure under (Mg2+) magnesium ion treatment Relationship between thylakoid membrane arrangement andstacking Biochim Biophys Acta 1797 1736-1748
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rumak I Mazur R Gieczewska K Koziol-Lipinska J Kierdaszuk B Michalski WP Shiell BJ Venema JH VredenbergWJ Mostowska A and Garstka M (2012) Correlation between spatial (3D) structure of pea and bean thylakoid membranes andarrangement of chlorophyll-protein complexes BMC Plant Biol 12 72
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and prothylakoids fractionated from wheat etioplastsPhysiol Plant 56 125-132
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
SAS Institute Inc 2013 SASSTATreg 123 Users Guide Cary NC SAS Institute IncPubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH protochlorophyllide oxidoreductase in primary bean leaves(Phaseolus vulgaris) during the first days of photoperiodic growth Photosynth Res 96 15-26
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In Lipids in Photosynthesis Structure Functionand Genetics S Paul-Andreacute and M Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 209-224
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-dimensional organization of higher-plant chloroplastthylakoid membranes revealed by electron tomography Plant Cell 17 2580-2586
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P Holzenburg A and Garab G (2000) Self-assemblyof large ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S A 97 1473-1476
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Solymosi K Mysliwa-Kurdziel B Boacuteka K Strzalka K and Boumlddi B (2006) Disintegration of the Prolamellar Body Structure atHigh Concentrations of Hg 2+ Plant Biol 8 627-635
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions the dark side of chlorophyllbiosynthesis in angiosperms Photosynth Res 105 143-166
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in sunflower (Helianthus annuus) cotyledons partiallycovered by the pericarp of the achene Ann Bot 99 857-867
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W (2005) Mechanisms of photoprotection andnonphotochemical quenching in pea light-harvesting complex at 25 A resolution EMBO J 24 919-928
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of chloroplast biogenesis maize as a model systemTrends Plant Sci 9 293-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for development and homeostasis Biochim Biophys Acta1847 809-820
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of glycophorin on lipid polymorphism A 31P-NMRstudy Biochim Biophys Acta 685 153-161
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes J Biol Chem 29014091-14106
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with protochlorophyll and protochlorophyllide forms in theunder-soil epicotyl segments of pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 148 307-315
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes Biochim Biophys Acta 1541 91-101Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms BiochimBiophys Acta 1847 838-848
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
36
Engel BD Schaffer M Kuhn Cuellar L Villa E Plitzko JM and Baumeister 1076 W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ 1077 cryo-electron tomography eLife 4 1078
Gabruk M Stecka A Strzałka W Kruk J Strzałka K and Mysliwa-Kurdziel B 1079 (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA 1080 PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS 1081 One 10 e0116990 1082
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid 1083 membranes Biochim Biophys Acta 1837 481ndash494 1084
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E 1085 van Hasselt PR Dobrucki J and Mostowska A (2005) Light-dependent reversal 1086 of dark-chilling induced changes in chloroplast structure and arrangement of 1087 chlorophyll-protein complexes in bean thylakoid membranes Biochim Biophys Acta 1088 1710 13ndash23 1089
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and 1090 Mullineaux CW (2012) Light-harvesting antenna composition controls the 1091 macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell 1092 Mol Biol 69 289ndash301 1093
Grzyb JM Solymosi K Strzałka K and Mysliwa-Kurdziel B (2013) Visualization 1094 and characterization of prolamellar bodies with atomic force microscopy J Plant 1095 Physiol 170 1217ndash1227 1096
Gunning BE (2001) Membrane geometry of ldquoopenrdquo prolamellar bodies 1097 Protoplasma 215 4ndash15 1098
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA 1099 FOLLOWING ALDEHYDE OSMIUM-TETROXIDE FIXATION J Cell Biol 24 79ndash93 1100
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell 1101 (Edward Arnold London) 1102
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective 1103 excitation of photosystems in chloroplasts inside plant leaves observed by near-1104 infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225ndash1105 238 1106
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur 1107 R Garstka M Maksymiec W Kulik A Dietler G and Gruszecki WI (2013) 1108 Molecular architecture of plant thylakoids under physiological and light stress 1109 conditions a study of lipid-light-harvesting complex II model membranes Plant Cell 1110 25 2155ndash2170 1111
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts 1112 and other plastids Nat Rev Mol Cell Biol 14 787ndash802 1113
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions 1114 F1000prime Rep 6 40 1115
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
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Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems experimentally-investigated entropy-driven stackingof plant photosynthetic membranes Sci Rep 4 4142
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes BiochimBiophys Acta 1708 187-195
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
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Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P Gruissem W and Baginsky S (2007)Proteome dynamics during plastid differentiation in rice Plant Physiol 143 912-923
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED ANDFAR-RED LIGHT J Cell Biol 22 433-442
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV Dekker JP and Jansson S (2005) Structureof the higher plant light harvesting complex I in vivo characterization and structural interdependence of the Lhca proteinsBiochemistry (Mosc) 44 3065-3073
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) Protein assembly and heat stability in developingthylakoid membranes during greening Proc Natl Acad Sci U S A 99 12149-12154
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kouril R Dekker JP and Boekema EJ (2012) Supramolecular organization of photosystem II in green plants BiochimBiophys Acta 1817 2-12
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization of Three-Dimensional Image Data Using IMODJ Struct Biol 116 71-76
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 655-659
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-proteasome system in plastid developmentBiochim Biophys Acta 1847 939-948
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 58 11-26Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid membranes from plastid transcription to proteincomplex assembly Planta 237 413-428
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology Second Edition (CRC Press)
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography software for three-dimensional reconstructionin transmission electron microscopy BMC Bioinformatics 8 288
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings by white red and blue low intensity lightProtoplasma 131 166-173
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986b) Thylakoid and grana formation during the development of pea chloroplasts illuminated by white red andblue low intensity light Protoplasma 134 88-94
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mysliwa-Kurdziel B Kruk J and Strzalka K (2013) Protochlorophyllide in model systems--an approach to in vivo conditionsBiophys Chem 175-176 28-38
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture and dynamics of the photosynthetic apparatus inhigher plants Plant J Cell Mol Biol 70 157-176
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Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts J Cell Sci 6 243-255Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) Identification of the carotenoid isomerase providesinsight into carotenoid biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 321-332
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Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development an overview Plant Physiol155 1545-1551
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Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast biogenesis and development Biochim BiophysActa
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Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in land plants J Exp Bot 65 1955-1972Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes Biochim Biophys Acta BBA - Bioenerg 1847 821-830
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Google Scholar Author Only Title Only Author and Title
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) The effect of cytochrome c oxidase on lipidpolymorphism of model membranes containing cardiolipin Eur J Biochem FEBS 164 137-140
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Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and Chlorophyll Synthesis Q Rev Biol 47 160-191Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rudowska L Gieczewska K Mazur R Garstka M and Mostowska A (2012) Chloroplast biogenesis mdash Correlation betweenstructure and function Biochim Biophys Acta BBA - Bioenerg 1817 1380-1387
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Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur R and Garstka M (2010) 3-D modelling ofchloroplast structure under (Mg2+) magnesium ion treatment Relationship between thylakoid membrane arrangement andstacking Biochim Biophys Acta 1797 1736-1748
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Rumak I Mazur R Gieczewska K Koziol-Lipinska J Kierdaszuk B Michalski WP Shiell BJ Venema JH VredenbergWJ Mostowska A and Garstka M (2012) Correlation between spatial (3D) structure of pea and bean thylakoid membranes andarrangement of chlorophyll-protein complexes BMC Plant Biol 12 72
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Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and prothylakoids fractionated from wheat etioplastsPhysiol Plant 56 125-132
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SAS Institute Inc 2013 SASSTATreg 123 Users Guide Cary NC SAS Institute IncPubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH protochlorophyllide oxidoreductase in primary bean leaves(Phaseolus vulgaris) during the first days of photoperiodic growth Photosynth Res 96 15-26
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Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In Lipids in Photosynthesis Structure Functionand Genetics S Paul-Andreacute and M Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 209-224
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-dimensional organization of higher-plant chloroplastthylakoid membranes revealed by electron tomography Plant Cell 17 2580-2586
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Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P Holzenburg A and Garab G (2000) Self-assemblyof large ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S A 97 1473-1476
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Google Scholar Author Only Title Only Author and Title
Solymosi K Mysliwa-Kurdziel B Boacuteka K Strzalka K and Boumlddi B (2006) Disintegration of the Prolamellar Body Structure atHigh Concentrations of Hg 2+ Plant Biol 8 627-635
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Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions the dark side of chlorophyllbiosynthesis in angiosperms Photosynth Res 105 143-166
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Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in sunflower (Helianthus annuus) cotyledons partiallycovered by the pericarp of the achene Ann Bot 99 857-867
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
37
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems 1116 experimentally-investigated entropy-driven stacking of plant photosynthetic 1117 membranes Sci Rep 4 4142 1118
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted 1119 stacking of thylakoid membranes Biochim Biophys Acta 1708 187ndash195 1120
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and 1121 Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein 1122 complexes define structure and optimize function of Arabidopsis chloroplasts a study 1123 using two chlorophyll b-less mutants Biochim Biophys Acta 1787 973ndash984 1124
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U 1125 and Roumlgner M (2007) Structural and functional self-organization of Photosystem II 1126 in grana thylakoids Biochim Biophys Acta 1767 1180ndash1188 1127
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D 1128 Shimoni E and Reich Z (2011) Dynamic control of protein diffusion within the 1129 granal thylakoid lumen Proc Natl Acad Sci 108 20248ndash20253 1130
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the 1131 organization of photosystem II in photosynthetic membranes by atomic force 1132 microscopy Biochemistry (Mosc) 47 431ndash440 1133
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P 1134 Gruissem W and Baginsky S (2007) Proteome dynamics during plastid 1135 differentiation in rice Plant Physiol 143 912ndash923 1136
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE 1137 DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED AND FAR-RED LIGHT 1138 J Cell Biol 22 433ndash442 1139
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV 1140 Dekker JP and Jansson S (2005) Structure of the higher plant light harvesting 1141 complex I in vivo characterization and structural interdependence of the Lhca 1142 proteins Biochemistry (Mosc) 44 3065ndash3073 1143
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) 1144 Protein assembly and heat stability in developing thylakoid membranes during 1145 greening Proc Natl Acad Sci U S A 99 12149ndash12154 1146
Kouřil R Dekker JP and Boekema EJ (2012) Supramolecular organization of 1147 photosystem II in green plants Biochim Biophys Acta 1817 2ndash12 1148
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization 1149 of Three-Dimensional Image Data Using IMOD J Struct Biol 116 71ndash76 1150
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is 1151 regulated by direct action of the ubiquitin-proteasome system Science 338 655ndash1152 659 1153
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
38
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-1154 proteasome system in plastid development Biochim Biophys Acta 1847 939ndash948 1155
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 1156 58 11ndash26 1157
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid 1158 membranes from plastid transcription to protein complex assembly Planta 237 1159 413ndash428 1160
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology 1161 Second Edition (CRC Press) 1162
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture 1163 Funct Plant Biol 26 709ndash716 1164
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography 1165 software for three-dimensional reconstruction in transmission electron microscopy 1166 BMC Bioinformatics 8 288 1167
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings 1168 by white red and blue low intensity light Protoplasma 131 166ndash173 1169
Mostowska A (1986b) Thylakoid and grana formation during the development of 1170 pea chloroplasts illuminated by white red and blue low intensity light Protoplasma 1171 134 88ndash94 1172
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional 1173 network of the thylakoid membranes in plants quasihelical model of the granum-1174 stroma assembly Plant Cell 20 2552ndash2557 1175
Mysliwa-Kurdziel B Kruk J and Strzałka K (2013) Protochlorophyllide in model 1176 systems--an approach to in vivo conditions Biophys Chem 175-176 28ndash38 1177
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture 1178 and dynamics of the photosynthetic apparatus in higher plants Plant J Cell Mol Biol 1179 70 157ndash176 1180
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in 1181 chloroplasts J Cell Sci 6 243ndash255 1182
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) 1183 Identification of the carotenoid isomerase provides insight into carotenoid 1184 biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 1185 321ndash332 1186
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis 1187 and development an overview Plant Physiol 155 1545ndash1551 1188
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast 1189 biogenesis and development Biochim Biophys Acta 1190
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
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41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
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Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
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Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
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Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-dimensional organization of higher-plant chloroplastthylakoid membranes revealed by electron tomography Plant Cell 17 2580-2586
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Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P Holzenburg A and Garab G (2000) Self-assemblyof large ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S A 97 1473-1476
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Google Scholar Author Only Title Only Author and Title
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Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of chloroplast biogenesis maize as a model systemTrends Plant Sci 9 293-301
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Sun Y and Zerges W (2015) Translational regulation in chloroplasts for development and homeostasis Biochim Biophys Acta1847 809-820
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of glycophorin on lipid polymorphism A 31P-NMRstudy Biochim Biophys Acta 685 153-161
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes J Biol Chem 29014091-14106
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with protochlorophyll and protochlorophyllide forms in theunder-soil epicotyl segments of pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 148 307-315
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes Biochim Biophys Acta 1541 91-101Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms BiochimBiophys Acta 1847 838-848
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
39
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in 1191 land plants J Exp Bot 65 1955ndash1972 1192
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes 1193 Biochim Biophys Acta BBA - Bioenerg 1847 821ndash830 1194
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) 1195 The effect of cytochrome c oxidase on lipid polymorphism of model membranes 1196 containing cardiolipin Eur J Biochem FEBS 164 137ndash140 1197
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and 1198 Chlorophyll Synthesis Q Rev Biol 47 160ndash191 1199
Rudowska Ł Gieczewska K Mazur R Garstka M and Mostowska A (2012) 1200 Chloroplast biogenesis mdash Correlation between structure and function Biochim 1201 Biophys Acta BBA - Bioenerg 1817 1380ndash1387 1202
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur 1203 R and Garstka M (2010) 3-D modelling of chloroplast structure under (Mg2+) 1204 magnesium ion treatment Relationship between thylakoid membrane arrangement 1205 and stacking Biochim Biophys Acta 1797 1736ndash1748 1206
Rumak I Mazur R Gieczewska K Kozioł-Lipińska J Kierdaszuk B Michalski 1207 WP Shiell BJ Venema JH Vredenberg WJ Mostowska A and Garstka M 1208 (2012) Correlation between spatial (3D) structure of pea and bean thylakoid 1209 membranes and arrangement of chlorophyll-protein complexes BMC Plant Biol 12 1210 72 1211
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and 1212 prothylakoids fractionated from wheat etioplasts Physiol Plant 56 125ndash132 1213
SAS Institute Inc 2013 SASSTATreg 123 Userrsquos Guide Cary NC SAS Institute Inc 1214
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH 1215 protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) 1216 during the first days of photoperiodic growth Photosynth Res 96 15ndash26 1217
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In 1218 Lipids in Photosynthesis Structure Function and Genetics S Paul-Andreacute and M 1219 Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 1220 209ndash224 1221
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH 1222 on the properties of protochlorophyllide oxidoreductase and the organization of 1223 prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336ndash2346 1224
Selstam E Schelin J Williams WP and Brain APR (2007) Structural 1225 organisation of prolamellar bodies (PLB) isolated from Zea mays Parallel TEM 1226 SAXS and absorption spectra measurements on samples subjected to freeze-thaw 1227 reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235ndash2245 1228
40
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
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Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
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Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-dimensional organization of higher-plant chloroplastthylakoid membranes revealed by electron tomography Plant Cell 17 2580-2586
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Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P Holzenburg A and Garab G (2000) Self-assemblyof large ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S A 97 1473-1476
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Solymosi K Mysliwa-Kurdziel B Boacuteka K Strzalka K and Boumlddi B (2006) Disintegration of the Prolamellar Body Structure atHigh Concentrations of Hg 2+ Plant Biol 8 627-635
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Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions the dark side of chlorophyllbiosynthesis in angiosperms Photosynth Res 105 143-166
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Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in sunflower (Helianthus annuus) cotyledons partiallycovered by the pericarp of the achene Ann Bot 99 857-867
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Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W (2005) Mechanisms of photoprotection andnonphotochemical quenching in pea light-harvesting complex at 25 A resolution EMBO J 24 919-928
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Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of chloroplast biogenesis maize as a model systemTrends Plant Sci 9 293-301
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Sun Y and Zerges W (2015) Translational regulation in chloroplasts for development and homeostasis Biochim Biophys Acta1847 809-820
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Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of glycophorin on lipid polymorphism A 31P-NMRstudy Biochim Biophys Acta 685 153-161
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Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes Biochim Biophys Acta 1541 91-101Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms BiochimBiophys Acta 1847 838-848
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Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
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Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-1229 dimensional organization of higher-plant chloroplast thylakoid membranes revealed 1230 by electron tomography Plant Cell 17 2580ndash2586 1231
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P 1232 Holzenburg A and Garab G (2000) Self-assembly of large ordered lamellae from 1233 non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S 1234 A 97 1473ndash1476 1235
Solymosi K Myśliwa-Kurdziel B Boacuteka K Strzałka K and Boumlddi B (2006) 1236 Disintegration of the Prolamellar Body Structure at High Concentrations of Hg 2+ 1237 Plant Biol 8 627ndash635 1238
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under 1239 natural conditions the dark side of chlorophyll biosynthesis in angiosperms 1240 Photosynth Res 105 143ndash166 1241
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in 1242 sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the 1243 achene Ann Bot 99 857ndash867 1244
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W 1245 (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea 1246 light-harvesting complex at 25 A resolution EMBO J 24 919ndash928 1247
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of 1248 chloroplast biogenesis maize as a model system Trends Plant Sci 9 293ndash301 1249
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for 1250 development and homeostasis Biochim Biophys Acta 1847 809ndash820 1251
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of 1252 glycophorin on lipid polymorphism A 31P-NMR study Biochim Biophys Acta 685 1253 153ndash161 1254
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in 1255 Photosynthetic Membranes J Biol Chem 290 14091ndash14106 1256
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with 1257 protochlorophyll and protochlorophyllide forms in the under-soil epicotyl segments of 1258 pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 1259 148 307ndash315 1260
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid 1261 membranes Biochim Biophys Acta 1541 91ndash101 1262
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 1263 2861ndash2873 1264
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll 1265 Biosynthesis Plant Cell 7 1039ndash1057 1266
41
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I 1267 assembly in oxygenic organisms Biochim Biophys Acta 1847 838ndash848 1268
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and 1269 Gruissem W (2005) Proteome analysis of the rice etioplast metabolic and 1270 regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072ndash1271 1084 1272
1273
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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core antenna complexes CP43 and CP47 of photosystem II Biochim Biophys Acta BBA - Bioenerg 1797 1606-1616Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Charuvi D Kiss V Nevo R Shimoni E Adam Z and Reich Z (2012) Gain and loss of photosynthetic membranes duringplastid differentiation in the shoot apex of Arabidopsis Plant Cell 24 1143-1157
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chong K and Deng Y (2012) The three dimensionality of cell membranes lamellar to cubic membrane transition as investigatedby electron microscopy Methods Cell Biol 108 319-343
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Chow WS Kim E-H Horton P and Anderson JM (2005) Granal stacking of thylakoid membranes in higher plant chloroplaststhe physicochemical forces at work and the functional consequences that ensue Photochem Photobiol Sci Off J EurPhotochem Assoc Eur Soc Photobiol 4 1081-1090
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
DallOsto L Bressan M and Bassi R (2015) Biogenesis of light harvesting proteins Biochim Biophys Acta 1847 861-871Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Albertsson P-A Mamedov F and Styring S (2004) Quantification of photosystem I and II in different parts of thethylakoid membrane from spinach Biochim Biophys Acta 1608 53-61
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Danielsson R Suorsa M Paakkarinen V Albertsson P-A Styring S Aro E-M and Mamedov F (2006) Dimeric andmonomeric organization of photosystem II Distribution of five distinct complexes in the different domains of the thylakoidmembrane J Biol Chem 281 14241-14249
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B and Kuumlhlbrandt W (2011) Electron tomography of plant thylakoid membranes J Exp Bot 62 2393-2402Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Daum B Nicastro D Austin J McIntosh JR and Kuumlhlbrandt W (2010) Arrangement of photosystem II and ATP synthase inchloroplast membranes of spinach and pea Plant Cell 22 1299-1312
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants BiochimBiophys Acta 1706 12-39
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Deng Y Almsherqi ZA Ng MML and Kohlwein SD (2010) Do viruses subvert cholesterol homeostasis to induce host cubicmembranes Trends Cell Biol 20 371-379
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Gabruk M Stecka A Strzalka W Kruk J Strzalka K and Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzymecomplexes reconstituted with PORA PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS One 10e0116990
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes Biochim Biophys Acta 1837 481-494Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Grzyb JM Solymosi K Strzalka K and Mysliwa-Kurdziel B (2013) Visualization and characterization of prolamellar bodieswith atomic force microscopy J Plant Physiol 170 1217-1227
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (2001) Membrane geometry of open prolamellar bodies Protoplasma 215 4-15Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA FOLLOWING ALDEHYDE OSMIUM-TETROXIDEFIXATION J Cell Biol 24 79-93
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell (Edward Arnold London)
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective excitation of photosystems in chloroplasts inside plantleaves observed by near-infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225-238
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur R Garstka M Maksymiec W Kulik ADietler G and Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions astudy of lipid-light-harvesting complex II model membranes Plant Cell 25 2155-2170
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Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids Nat Rev Mol Cell Biol 14787-802
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems experimentally-investigated entropy-driven stackingof plant photosynthetic membranes Sci Rep 4 4142
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes BiochimBiophys Acta 1708 187-195
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P Gruissem W and Baginsky S (2007)Proteome dynamics during plastid differentiation in rice Plant Physiol 143 912-923
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED ANDFAR-RED LIGHT J Cell Biol 22 433-442
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV Dekker JP and Jansson S (2005) Structureof the higher plant light harvesting complex I in vivo characterization and structural interdependence of the Lhca proteinsBiochemistry (Mosc) 44 3065-3073
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Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) Protein assembly and heat stability in developingthylakoid membranes during greening Proc Natl Acad Sci U S A 99 12149-12154
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kouril R Dekker JP and Boekema EJ (2012) Supramolecular organization of photosystem II in green plants BiochimBiophys Acta 1817 2-12
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Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization of Three-Dimensional Image Data Using IMODJ Struct Biol 116 71-76
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Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 655-659
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-proteasome system in plastid developmentBiochim Biophys Acta 1847 939-948
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Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 58 11-26Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid membranes from plastid transcription to proteincomplex assembly Planta 237 413-428
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Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology Second Edition (CRC Press)
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography software for three-dimensional reconstructionin transmission electron microscopy BMC Bioinformatics 8 288
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Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings by white red and blue low intensity lightProtoplasma 131 166-173
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Mostowska A (1986b) Thylakoid and grana formation during the development of pea chloroplasts illuminated by white red andblue low intensity light Protoplasma 134 88-94
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Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
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Mysliwa-Kurdziel B Kruk J and Strzalka K (2013) Protochlorophyllide in model systems--an approach to in vivo conditionsBiophys Chem 175-176 28-38
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Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture and dynamics of the photosynthetic apparatus inhigher plants Plant J Cell Mol Biol 70 157-176
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DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
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CrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gabruk M Stecka A Strzalka W Kruk J Strzalka K and Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzymecomplexes reconstituted with PORA PORB and PORC proteins of A thaliana fluorescence and catalytic properties PloS One 10e0116990
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garab G (2014) Hierarchical organization and structural flexibility of thylakoid membranes Biochim Biophys Acta 1837 481-494Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Garstka M Drozak A Rosiak M Venema JH Kierdaszuk B Simeonova E van Hasselt PR Dobrucki J and Mostowska A(2005) Light-dependent reversal of dark-chilling induced changes in chloroplast structure and arrangement of chlorophyll-proteincomplexes in bean thylakoid membranes Biochim Biophys Acta 1710 13-23
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Goral TK Johnson MP Duffy CDP Brain APR Ruban AV and Mullineaux CW (2012) Light-harvesting antennacomposition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis Plant J Cell Mol Biol 69 289-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Grzyb JM Solymosi K Strzalka K and Mysliwa-Kurdziel B (2013) Visualization and characterization of prolamellar bodieswith atomic force microscopy J Plant Physiol 170 1217-1227
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (2001) Membrane geometry of open prolamellar bodies Protoplasma 215 4-15Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BE (1965) THE FINE STRUCTURE OF CHLOROPLAST STROMA FOLLOWING ALDEHYDE OSMIUM-TETROXIDEFIXATION J Cell Biol 24 79-93
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Gunning BES and Steer MW (1975) Ultrastructure and the biology of plant cell (Edward Arnold London)
Hasegawa M Shiina T Terazima M and Kumazaki S (2010) Selective excitation of photosystems in chloroplasts inside plantleaves observed by near-infrared laser-based fluorescence spectral microscopy Plant Cell Physiol 51 225-238
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Janik E Bednarska J Zubik M Puzio M Luchowski R Grudzinski W Mazur R Garstka M Maksymiec W Kulik ADietler G and Gruszecki WI (2013) Molecular architecture of plant thylakoids under physiological and light stress conditions astudy of lipid-light-harvesting complex II model membranes Plant Cell 25 2155-2170
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jarvis P and Loacutepez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids Nat Rev Mol Cell Biol 14787-802
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jensen PE and Leister D (2014) Chloroplast evolution structure and functions F1000prime Rep 6 40Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Jia H Liggins JR and Chow WS (2014) Entropy and biological systems experimentally-investigated entropy-driven stackingof plant photosynthetic membranes Sci Rep 4 4142
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kim E-H Chow WS Horton P and Anderson JM (2005) Entropy-assisted stacking of thylakoid membranes BiochimBiophys Acta 1708 187-195
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P Gruissem W and Baginsky S (2007)Proteome dynamics during plastid differentiation in rice Plant Physiol 143 912-923
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED ANDFAR-RED LIGHT J Cell Biol 22 433-442
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV Dekker JP and Jansson S (2005) Structureof the higher plant light harvesting complex I in vivo characterization and structural interdependence of the Lhca proteinsBiochemistry (Mosc) 44 3065-3073
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) Protein assembly and heat stability in developingthylakoid membranes during greening Proc Natl Acad Sci U S A 99 12149-12154
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kouril R Dekker JP and Boekema EJ (2012) Supramolecular organization of photosystem II in green plants BiochimBiophys Acta 1817 2-12
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization of Three-Dimensional Image Data Using IMODJ Struct Biol 116 71-76
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 655-659
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-proteasome system in plastid developmentBiochim Biophys Acta 1847 939-948
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 58 11-26Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid membranes from plastid transcription to proteincomplex assembly Planta 237 413-428
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology Second Edition (CRC Press)
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography software for three-dimensional reconstructionin transmission electron microscopy BMC Bioinformatics 8 288
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings by white red and blue low intensity lightProtoplasma 131 166-173
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986b) Thylakoid and grana formation during the development of pea chloroplasts illuminated by white red andblue low intensity light Protoplasma 134 88-94
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mysliwa-Kurdziel B Kruk J and Strzalka K (2013) Protochlorophyllide in model systems--an approach to in vivo conditionsBiophys Chem 175-176 28-38
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture and dynamics of the photosynthetic apparatus inhigher plants Plant J Cell Mol Biol 70 157-176
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts J Cell Sci 6 243-255Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) Identification of the carotenoid isomerase providesinsight into carotenoid biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 321-332
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development an overview Plant Physiol155 1545-1551
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast biogenesis and development Biochim BiophysActa
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in land plants J Exp Bot 65 1955-1972Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes Biochim Biophys Acta BBA - Bioenerg 1847 821-830
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) The effect of cytochrome c oxidase on lipidpolymorphism of model membranes containing cardiolipin Eur J Biochem FEBS 164 137-140
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and Chlorophyll Synthesis Q Rev Biol 47 160-191Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rudowska L Gieczewska K Mazur R Garstka M and Mostowska A (2012) Chloroplast biogenesis mdash Correlation betweenstructure and function Biochim Biophys Acta BBA - Bioenerg 1817 1380-1387
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur R and Garstka M (2010) 3-D modelling ofchloroplast structure under (Mg2+) magnesium ion treatment Relationship between thylakoid membrane arrangement andstacking Biochim Biophys Acta 1797 1736-1748
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rumak I Mazur R Gieczewska K Koziol-Lipinska J Kierdaszuk B Michalski WP Shiell BJ Venema JH VredenbergWJ Mostowska A and Garstka M (2012) Correlation between spatial (3D) structure of pea and bean thylakoid membranes andarrangement of chlorophyll-protein complexes BMC Plant Biol 12 72
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and prothylakoids fractionated from wheat etioplastsPhysiol Plant 56 125-132
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
SAS Institute Inc 2013 SASSTATreg 123 Users Guide Cary NC SAS Institute IncPubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH protochlorophyllide oxidoreductase in primary bean leaves(Phaseolus vulgaris) during the first days of photoperiodic growth Photosynth Res 96 15-26
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In Lipids in Photosynthesis Structure Functionand Genetics S Paul-Andreacute and M Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 209-224
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-dimensional organization of higher-plant chloroplastthylakoid membranes revealed by electron tomography Plant Cell 17 2580-2586
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P Holzenburg A and Garab G (2000) Self-assemblyof large ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S A 97 1473-1476
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Solymosi K Mysliwa-Kurdziel B Boacuteka K Strzalka K and Boumlddi B (2006) Disintegration of the Prolamellar Body Structure atHigh Concentrations of Hg 2+ Plant Biol 8 627-635
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions the dark side of chlorophyllbiosynthesis in angiosperms Photosynth Res 105 143-166
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in sunflower (Helianthus annuus) cotyledons partiallycovered by the pericarp of the achene Ann Bot 99 857-867
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W (2005) Mechanisms of photoprotection andnonphotochemical quenching in pea light-harvesting complex at 25 A resolution EMBO J 24 919-928
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of chloroplast biogenesis maize as a model systemTrends Plant Sci 9 293-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for development and homeostasis Biochim Biophys Acta1847 809-820
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of glycophorin on lipid polymorphism A 31P-NMRstudy Biochim Biophys Acta 685 153-161
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes J Biol Chem 29014091-14106
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with protochlorophyll and protochlorophyllide forms in theunder-soil epicotyl segments of pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 148 307-315
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes Biochim Biophys Acta 1541 91-101Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms BiochimBiophys Acta 1847 838-848
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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Kim E-H Li X-P Razeghifard R Anderson JM Niyogi KK Pogson BJ and Chow WS (2009) The multiple roles of light-harvesting chlorophyll ab-protein complexes define structure and optimize function of Arabidopsis chloroplasts a study usingtwo chlorophyll b-less mutants Biochim Biophys Acta 1787 973-984
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Kirchhoff H Haase W Haferkamp S Schott T Borinski M Kubitscheck U and Roumlgner M (2007) Structural and functionalself-organization of Photosystem II in grana thylakoids Biochim Biophys Acta 1767 1180-1188
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Kirchhoff H Hall C Wood M Herbstovaacute M Tsabari O Nevo R Charuvi D Shimoni E and Reich Z (2011) Dynamiccontrol of protein diffusion within the granal thylakoid lumen Proc Natl Acad Sci 108 20248-20253
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Kirchhoff H Lenhert S Buumlchel C Chi L and Nield J (2008) Probing the organization of photosystem II in photosyntheticmembranes by atomic force microscopy Biochemistry (Mosc) 47 431-440
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Kleffmann T von Zychlinski A Russenberger D Hirsch-Hoffmann M Gehrig P Gruissem W and Baginsky S (2007)Proteome dynamics during plastid differentiation in rice Plant Physiol 143 912-923
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Klein S Bryan G and Bogorad L (1964) EARLY STAGES IN THE DEVELOPMENT OF PLASTID FINE STRUCTURE IN RED ANDFAR-RED LIGHT J Cell Biol 22 433-442
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Klimmek F Ganeteg U Ihalainen JA van Roon H Jensen PE Scheller HV Dekker JP and Jansson S (2005) Structureof the higher plant light harvesting complex I in vivo characterization and structural interdependence of the Lhca proteinsBiochemistry (Mosc) 44 3065-3073
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Kota Z Horvath LI Droppa M Horvath G Farkas T and Pali T (2002) Protein assembly and heat stability in developingthylakoid membranes during greening Proc Natl Acad Sci U S A 99 12149-12154
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Kouril R Dekker JP and Boekema EJ (2012) Supramolecular organization of photosystem II in green plants BiochimBiophys Acta 1817 2-12
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Kremer JR Mastronarde DN and McIntosh JR (1996) Computer Visualization of Three-Dimensional Image Data Using IMODJ Struct Biol 116 71-76
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Ling Q Huang W Baldwin A and Jarvis P (2012) Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 655-659
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ling Q and Jarvis P (2015) Functions of plastid protein import and the ubiquitin-proteasome system in plastid developmentBiochim Biophys Acta 1847 939-948
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Loacutepez-Juez E (2007) Plastid biogenesis between light and shadows J Exp Bot 58 11-26Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid membranes from plastid transcription to proteincomplex assembly Planta 237 413-428
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology Second Edition (CRC Press)
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography software for three-dimensional reconstructionin transmission electron microscopy BMC Bioinformatics 8 288
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings by white red and blue low intensity lightProtoplasma 131 166-173
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986b) Thylakoid and grana formation during the development of pea chloroplasts illuminated by white red andblue low intensity light Protoplasma 134 88-94
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mysliwa-Kurdziel B Kruk J and Strzalka K (2013) Protochlorophyllide in model systems--an approach to in vivo conditionsBiophys Chem 175-176 28-38
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture and dynamics of the photosynthetic apparatus inhigher plants Plant J Cell Mol Biol 70 157-176
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts J Cell Sci 6 243-255Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) Identification of the carotenoid isomerase providesinsight into carotenoid biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 321-332
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development an overview Plant Physiol155 1545-1551
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast biogenesis and development Biochim BiophysActa
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in land plants J Exp Bot 65 1955-1972Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes Biochim Biophys Acta BBA - Bioenerg 1847 821-830
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) The effect of cytochrome c oxidase on lipidpolymorphism of model membranes containing cardiolipin Eur J Biochem FEBS 164 137-140
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and Chlorophyll Synthesis Q Rev Biol 47 160-191Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rudowska L Gieczewska K Mazur R Garstka M and Mostowska A (2012) Chloroplast biogenesis mdash Correlation betweenstructure and function Biochim Biophys Acta BBA - Bioenerg 1817 1380-1387
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur R and Garstka M (2010) 3-D modelling ofchloroplast structure under (Mg2+) magnesium ion treatment Relationship between thylakoid membrane arrangement andstacking Biochim Biophys Acta 1797 1736-1748
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rumak I Mazur R Gieczewska K Koziol-Lipinska J Kierdaszuk B Michalski WP Shiell BJ Venema JH VredenbergWJ Mostowska A and Garstka M (2012) Correlation between spatial (3D) structure of pea and bean thylakoid membranes andarrangement of chlorophyll-protein complexes BMC Plant Biol 12 72
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and prothylakoids fractionated from wheat etioplastsPhysiol Plant 56 125-132
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
SAS Institute Inc 2013 SASSTATreg 123 Users Guide Cary NC SAS Institute IncPubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH protochlorophyllide oxidoreductase in primary bean leaves(Phaseolus vulgaris) during the first days of photoperiodic growth Photosynth Res 96 15-26
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In Lipids in Photosynthesis Structure Functionand Genetics S Paul-Andreacute and M Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 209-224
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-dimensional organization of higher-plant chloroplastthylakoid membranes revealed by electron tomography Plant Cell 17 2580-2586
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P Holzenburg A and Garab G (2000) Self-assemblyof large ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S A 97 1473-1476
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Solymosi K Mysliwa-Kurdziel B Boacuteka K Strzalka K and Boumlddi B (2006) Disintegration of the Prolamellar Body Structure atHigh Concentrations of Hg 2+ Plant Biol 8 627-635
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions the dark side of chlorophyllbiosynthesis in angiosperms Photosynth Res 105 143-166
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in sunflower (Helianthus annuus) cotyledons partiallycovered by the pericarp of the achene Ann Bot 99 857-867
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W (2005) Mechanisms of photoprotection andnonphotochemical quenching in pea light-harvesting complex at 25 A resolution EMBO J 24 919-928
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of chloroplast biogenesis maize as a model systemTrends Plant Sci 9 293-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for development and homeostasis Biochim Biophys Acta1847 809-820
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of glycophorin on lipid polymorphism A 31P-NMRstudy Biochim Biophys Acta 685 153-161
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes J Biol Chem 29014091-14106
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with protochlorophyll and protochlorophyllide forms in theunder-soil epicotyl segments of pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 148 307-315
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes Biochim Biophys Acta 1541 91-101Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms BiochimBiophys Acta 1847 838-848
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
Supplemental Data contentsuppl20160322tpc1501053DC2html contentsuppl20160321tpc1501053DC1html
Permissions httpswwwcopyrightcomcccopenurldosid=pd_hw1532298Xampissn=1532298XampWTmc_id=pd_hw1532298X
eTOCs httpwwwplantcellorgcgialertsctmain
Sign up for eTOCs at
CiteTrack Alerts httpwwwplantcellorgcgialertsctmain
Sign up for CiteTrack Alerts at
Subscription Information httpwwwaspborgpublicationssubscriptionscfm
is available atPlant Physiology and The Plant CellSubscription Information for
ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
Lyska D Meierhoff K and Westhoff P (2013) How to build functional thylakoid membranes from plastid transcription to proteincomplex assembly Planta 237 413-428
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Manly BFJ (1997) Randomization Bootstrap and Monte Carlo Methods in Biology Second Edition (CRC Press)
Mehta M Sarafis V and Critchley C (1999) Thylakoid membrane architecture Funct Plant Biol 26 709-716Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
MessaoudiI C Boudier T Sorzano C and Marco S (2007) TomoJ tomography software for three-dimensional reconstructionin transmission electron microscopy BMC Bioinformatics 8 288
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986a) Changes induced on the prolamellar body of pea seedlings by white red and blue low intensity lightProtoplasma 131 166-173
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mostowska A (1986b) Thylakoid and grana formation during the development of pea chloroplasts illuminated by white red andblue low intensity light Protoplasma 134 88-94
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mustaacuterdy L Buttle K Steinbach G and Garab G (2008) The three-dimensional network of the thylakoid membranes in plantsquasihelical model of the granum-stroma assembly Plant Cell 20 2552-2557
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Mysliwa-Kurdziel B Kruk J and Strzalka K (2013) Protochlorophyllide in model systems--an approach to in vivo conditionsBiophys Chem 175-176 28-38
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Nevo R Charuvi D Tsabari O and Reich Z (2012) Composition architecture and dynamics of the photosynthetic apparatus inhigher plants Plant J Cell Mol Biol 70 157-176
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Paolillo DJ (1970) The three-dimensional arrangement of intergranal lamellae in chloroplasts J Cell Sci 6 243-255Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Park H Kreunen SS Cuttriss AJ DellaPenna D and Pogson BJ (2002) Identification of the carotenoid isomerase providesinsight into carotenoid biosynthesis prolamellar body formation and photomorphogenesis Plant Cell 14 321-332
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pogson BJ and Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development an overview Plant Physiol155 1545-1551
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pogson BJ Ganguly D and Albrecht-Borth V (2015) Insights into chloroplast biogenesis and development Biochim BiophysActa
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Pribil M Labs M and Leister D (2014) Structure and dynamics of thylakoids in land plants J Exp Bot 65 1955-1972Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rast A Heinz S and Nickelsen J (2015) Biogenesis of thylakoid membranes Biochim Biophys Acta BBA - Bioenerg 1847 821-830
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Rietveld A van Kemenade TJ Hak T Verkleij AJ and de Kruijff B (1987) The effect of cytochrome c oxidase on lipidpolymorphism of model membranes containing cardiolipin Eur J Biochem FEBS 164 137-140
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rosinski J and Rosen WG (1972) Chloroplast Development Fine Structure and Chlorophyll Synthesis Q Rev Biol 47 160-191Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rudowska L Gieczewska K Mazur R Garstka M and Mostowska A (2012) Chloroplast biogenesis mdash Correlation betweenstructure and function Biochim Biophys Acta BBA - Bioenerg 1817 1380-1387
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur R and Garstka M (2010) 3-D modelling ofchloroplast structure under (Mg2+) magnesium ion treatment Relationship between thylakoid membrane arrangement andstacking Biochim Biophys Acta 1797 1736-1748
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Rumak I Mazur R Gieczewska K Koziol-Lipinska J Kierdaszuk B Michalski WP Shiell BJ Venema JH VredenbergWJ Mostowska A and Garstka M (2012) Correlation between spatial (3D) structure of pea and bean thylakoid membranes andarrangement of chlorophyll-protein complexes BMC Plant Biol 12 72
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and prothylakoids fractionated from wheat etioplastsPhysiol Plant 56 125-132
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
SAS Institute Inc 2013 SASSTATreg 123 Users Guide Cary NC SAS Institute IncPubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH protochlorophyllide oxidoreductase in primary bean leaves(Phaseolus vulgaris) during the first days of photoperiodic growth Photosynth Res 96 15-26
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In Lipids in Photosynthesis Structure Functionand Genetics S Paul-Andreacute and M Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 209-224
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-dimensional organization of higher-plant chloroplastthylakoid membranes revealed by electron tomography Plant Cell 17 2580-2586
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P Holzenburg A and Garab G (2000) Self-assemblyof large ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S A 97 1473-1476
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Solymosi K Mysliwa-Kurdziel B Boacuteka K Strzalka K and Boumlddi B (2006) Disintegration of the Prolamellar Body Structure atHigh Concentrations of Hg 2+ Plant Biol 8 627-635
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions the dark side of chlorophyllbiosynthesis in angiosperms Photosynth Res 105 143-166
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in sunflower (Helianthus annuus) cotyledons partiallycovered by the pericarp of the achene Ann Bot 99 857-867
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W (2005) Mechanisms of photoprotection andnonphotochemical quenching in pea light-harvesting complex at 25 A resolution EMBO J 24 919-928
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of chloroplast biogenesis maize as a model systemTrends Plant Sci 9 293-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for development and homeostasis Biochim Biophys Acta1847 809-820
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of glycophorin on lipid polymorphism A 31P-NMRstudy Biochim Biophys Acta 685 153-161
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes J Biol Chem 29014091-14106
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with protochlorophyll and protochlorophyllide forms in theunder-soil epicotyl segments of pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 148 307-315
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes Biochim Biophys Acta 1541 91-101Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms BiochimBiophys Acta 1847 838-848
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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Rumak I Gieczewska K Kierdaszuk B Gruszecki WI Mostowska A Mazur R and Garstka M (2010) 3-D modelling ofchloroplast structure under (Mg2+) magnesium ion treatment Relationship between thylakoid membrane arrangement andstacking Biochim Biophys Acta 1797 1736-1748
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Rumak I Mazur R Gieczewska K Koziol-Lipinska J Kierdaszuk B Michalski WP Shiell BJ Venema JH VredenbergWJ Mostowska A and Garstka M (2012) Correlation between spatial (3D) structure of pea and bean thylakoid membranes andarrangement of chlorophyll-protein complexes BMC Plant Biol 12 72
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Ryberg M and Sundqvist C (1982) Characterization of prolamellar bodies and prothylakoids fractionated from wheat etioplastsPhysiol Plant 56 125-132
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SAS Institute Inc 2013 SASSTATreg 123 Users Guide Cary NC SAS Institute IncPubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Schoefs B and Franck F (2008) The photoenzymatic cycle of NADPH protochlorophyllide oxidoreductase in primary bean leaves(Phaseolus vulgaris) during the first days of photoperiodic growth Photosynth Res 96 15-26
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Selstam E (1998) Development of Thylakoid Membranes with Respect to Lipids In Lipids in Photosynthesis Structure Functionand Genetics S Paul-Andreacute and M Norio eds Advances in Photosynthesis and Respiration (Springer Netherlands) pp 209-224
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Brain T and Williams WP (2002) The effects of low pH on the properties of protochlorophyllideoxidoreductase and the organization of prolamellar bodies of maize (Zea mays) Eur J Biochem FEBS 269 2336-2346
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Selstam E Schelin J Williams WP and Brain APR (2007) Structural organisation of prolamellar bodies (PLB) isolated fromZea mays Parallel TEM SAXS and absorption spectra measurements on samples subjected to freeze-thaw reduced pH and high-salt perturbation Biochim Biophys Acta 1768 2235-2245
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Shimoni E Rav-Hon O Ohad I Brumfeld V and Reich Z (2005) Three-dimensional organization of higher-plant chloroplastthylakoid membranes revealed by electron tomography Plant Cell 17 2580-2586
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Simidjiev I Stoylova S Amenitsch H Javorfi T Mustardy L Laggner P Holzenburg A and Garab G (2000) Self-assemblyof large ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro Proc Natl Acad Sci U S A 97 1473-1476
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
Solymosi K Mysliwa-Kurdziel B Boacuteka K Strzalka K and Boumlddi B (2006) Disintegration of the Prolamellar Body Structure atHigh Concentrations of Hg 2+ Plant Biol 8 627-635
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions the dark side of chlorophyllbiosynthesis in angiosperms Photosynth Res 105 143-166
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in sunflower (Helianthus annuus) cotyledons partiallycovered by the pericarp of the achene Ann Bot 99 857-867
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W (2005) Mechanisms of photoprotection andnonphotochemical quenching in pea light-harvesting complex at 25 A resolution EMBO J 24 919-928
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of chloroplast biogenesis maize as a model systemTrends Plant Sci 9 293-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for development and homeostasis Biochim Biophys Acta1847 809-820
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of glycophorin on lipid polymorphism A 31P-NMRstudy Biochim Biophys Acta 685 153-161
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes J Biol Chem 29014091-14106
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with protochlorophyll and protochlorophyllide forms in theunder-soil epicotyl segments of pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 148 307-315
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes Biochim Biophys Acta 1541 91-101Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms BiochimBiophys Acta 1847 838-848
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
Google Scholar Author Only Title Only Author and Title
Solymosi K Mysliwa-Kurdziel B Boacuteka K Strzalka K and Boumlddi B (2006) Disintegration of the Prolamellar Body Structure atHigh Concentrations of Hg 2+ Plant Biol 8 627-635
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K and Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions the dark side of chlorophyllbiosynthesis in angiosperms Photosynth Res 105 143-166
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Solymosi K Vitaacutenyi B Hideg E and Boumlddi B (2007) Etiolation symptoms in sunflower (Helianthus annuus) cotyledons partiallycovered by the pericarp of the achene Ann Bot 99 857-867
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Standfuss J Terwisscha van Scheltinga AC Lamborghini M and Kuumlhlbrandt W (2005) Mechanisms of photoprotection andnonphotochemical quenching in pea light-harvesting complex at 25 A resolution EMBO J 24 919-928
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Stern DB Hanson MR and Barkan A (2004) Genetics and genomics of chloroplast biogenesis maize as a model systemTrends Plant Sci 9 293-301
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Sun Y and Zerges W (2015) Translational regulation in chloroplasts for development and homeostasis Biochim Biophys Acta1847 809-820
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Taraschi TF De Kruijff B Verkleij A and Van Echteld CJ (1982) Effect of glycophorin on lipid polymorphism A 31P-NMRstudy Biochim Biophys Acta 685 153-161
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Tietz S et al (2015) Functional Implications of Photosystem II Crystal Formation in Photosynthetic Membranes J Biol Chem 29014091-14106
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vitaacutenyi B Koacutesa A Solymosi K and Boumlddi B (2013) Etioplasts with protochlorophyll and protochlorophyllide forms in theunder-soil epicotyl segments of pea (Pisum sativum) seedlings grown under natural light conditions Physiol Plant 148 307-315
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Vothknecht UC and Westhoff P (2001) Biogenesis and origin of thylakoid membranes Biochim Biophys Acta 1541 91-101Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Waters MT and Langdale JA (2009) The making of a chloroplast EMBO J 28 2861-2873Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Wettstein D Gough S and Kannangara CG (1995) Chlorophyll Biosynthesis Plant Cell 7 1039-1057Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Yang H Liu J Wen X and Lu C (2015) Molecular mechanism of photosystem I assembly in oxygenic organisms BiochimBiophys Acta 1847 838-848
Pubmed Author and TitleCrossRef Author and TitleGoogle Scholar Author Only Title Only Author and Title
Von Zychlinski A Kleffmann T Krishnamurthy N Sjoumllander K Baginsky S and Gruissem W (2005) Proteome analysis of therice etioplast metabolic and regulatory networks and novel protein functions Mol Cell Proteomics MCP 4 1072-1084
Pubmed Author and TitleCrossRef Author and Title
Google Scholar Author Only Title Only Author and Title
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
Supplemental Data contentsuppl20160322tpc1501053DC2html contentsuppl20160321tpc1501053DC1html
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
Google Scholar Author Only Title Only Author and Title
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
Supplemental Data contentsuppl20160322tpc1501053DC2html contentsuppl20160321tpc1501053DC1html
Permissions httpswwwcopyrightcomcccopenurldosid=pd_hw1532298Xampissn=1532298XampWTmc_id=pd_hw1532298X
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Subscription Information httpwwwaspborgpublicationssubscriptionscfm
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ADVANCING THE SCIENCE OF PLANT BIOLOGY copy American Society of Plant Biologists
DOI 101105tpc1501053 originally published online March 21 2016Plant Cell
Lucja Maria Kowalewska Radoslaw Mazur Szymon Suski Maciej Garstka and Agnieszka Mostowskachloroplast biogenesis Dynamic model of the tubular-lamellar transformation
Three-dimensional visualization of the internal plastid membrane network during runner bean
This information is current as of September 29 2020
Supplemental Data contentsuppl20160322tpc1501053DC2html contentsuppl20160321tpc1501053DC1html
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