The Plant Cell, Vol. 20: 2552–2557, October 2008, www.plantcell.org ã 2008 American Society of Plant Biologists
PERSPECTIVE
The Three-Dimensional Network of the Thylakoid
Membranes in Plants: Quasihelical Model of the
Granum-Stroma Assembly
W
László Mustárdy,a Karolyn Buttle,b Gábor Steinbach,a and Győző Garaba,1
a Biological
b New
Research Center, Hungarian Academy of Sciences, H-6701 Szeged, Hungary
York State Department of Health, Albany, New York 12201
The three-dimensional (3-D) network of the granum-stroma thylakoid assembly of vascular plant chloroplasts exhibits
complex structural/functional heterogeneity. A complete understanding of the ultrastructure of this assembly is critical for
our understanding of thylakoid function. The prevailing historical model of thylakoid structure, based on information derived
from serial section analyses of electron microscopy (EM) images, suggests a helical arrangement of stroma membranes
wound around the granum stacks. More recently, electron tomography has emerged as the leading method for the study of
thylakoid ultrastructure, as it provides for higher resolution in the depth dimension. The first detailed 3D topological model
derived from electron tomography was in disagreement with the helical model, whereas a more recent electron tomography
study, conducted under somewhat different experimental conditions, suggested that basic features of the helical model are
still valid. Here, we review the conventional EM data and present a critical discussion of the two electron tomography data
sets in an attempt to establish a consensus model that accommodates all the information presently available.
Grana, the cylindrical stacks of thylakoids characteristic of
vascular plant chloroplasts, are relatively recent and immensely
successful products of evolution (Mullineaux, 2005). Their ubiquitous presence in vascular plants suggests that they play critical
roles in the fine-tuning of photosynthetic functions (Trissl and
Wilhelm, 1993; Albertsson, 2001; Goss et al., 2007; Kirchhoff
et al., 2007). The tightly appressed arrangement of granum
thylakoid membranes ensures that chloroplasts contain an extremely large area-to-volume ratio and a high stability of the
ultrastructure, which remarkably is combined with high flexibility
in responses to dynamically changing environmental conditions
(Anderson, 1999; Garab and Mustárdy, 1999; Horton, 1999). The
three-dimensional (3D) thylakoid network in granal chloroplasts,
the network of grana interconnected by unstacked stroma thylakoids, exhibits complex structural/functional heterogeneity
that has perplexed scientists for many decades and has led to
the postulation of a number of models (reviewed in Mustárdy and
Garab, 2003). Until recently, the most advanced of these were
based on information derived from serial section analyses of
electron microscopy (EM) images. Not long ago, electron tomography of complex membrane structures became possible,
following the availability of high-voltage electron microscopes
and relevant computer programs (Frey and Mannella, 2000). This
1 Address
correspondence to [email protected].
Online version contains Web-only data.
www.plantcell.org/cgi/doi/10.1105/tpc.108.059147
W
technique has emerged as the leading method for the study of 3D
ultrastructure in the 5- to 20-nm resolution range. It complements
serial-section reconstruction by providing higher resolution in the
depth dimension, whereas serial-section reconstruction is better
suited to tracing continuity over long distances throughout the
sample (McEwen and Marko, 2001). The first detailed 3D topological model (Shimoni et al., 2005) derived from electron tomography was in disagreement with the prevailing helical model
constructed from electron micrographs of complete, serially
sectioned granum-stroma assemblies (Paolillo, 1970; Mustárdy
and Garab, 2003). By contrast, a more recent electron tomography study, conducted under somewhat different experimental
conditions, suggested that basic features of the helical model are
still valid, although the model requires refinement (Mustárdy
et al., 2008). In this essay, we review the conventional EM data
and present a critical discussion of the two electron tomography
data sets (Shimoni et al., 2005; Mustárdy et al., 2008) in an
attempt to establish a consensus model that accommodates all
the information presently available.
STRUCTURE AND FUNCTIONS: BASIC FEATURES
Thylakoids are flattened membranous vesicles (flattened sacs)
that are the site of light-dependent reactions of photosynthesis
(reviewed in Wise and Hoober, 2006). Grana consist of cylindrical
stacks of ;10 to 20 tightly appressed thylakoids of 300 to 600
nm in diameter that are interconnected by single, unstacked,
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PERSPECTIVE
stroma thylakoids. Granum and stroma thylakoid membranes
differ markedly in their protein composition. Photosystem II (PSII)
and its main chlorophyll a/b light-harvesting complex, LHCII, are
situated predominantly in the granum membranes, and this
region is largely deficient in PSI and LHCI, which are enriched
in the stroma thylakoid membranes (Andersson and Anderson,
1980). Despite this remarkable differentiation and heterogeneity,
the thylakoid membrane system is formed from one continuous
membrane, and it encloses one inner aqueous phase, the thylakoid lumen. The continuum of the membrane system is important for the diffusion of mobile electron transport components
between the two laterally separated photosystems and for the
trafficking of proteins and (super)complexes between the two
regions, induced, for example, by phosphorylation (Allen and
Forsberg, 2001) or during the repair cycle of PSII (Barber and
Andersson, 1992). The contiguity of the inner aqueous phase is
essential for the formation of uniform transmembrane electric
potential and pH gradients (i.e., for chemiosmosis).
THE HELICAL MODEL
The first 3D model that was derived from systematic serial
sectioning of granum-stroma thylakoid networks was the helical
model of Paolillo (1970), which was consistent with the basic
observations and models put forward by Wehrmeyer (1964) and
von Wettstein (1959). The helical model was further modified and
supported by Brangeon and Mustárdy (1979), who performed
serial sectioning throughout the entire depth of granum-stroma
assemblies on developing chloroplasts. In the helical model, the
stroma membranes are wound around the granum in the form of
multiple right-handed helices, in which each granum thylakoid is
connected to an average of eight stroma thylakoids. The basic
features of the helical model are shown schematically in Figure
1A. The cylindrical granum pillar of stacked membranes is
surrounded by multiple helices of stroma thylakoids that are
interconnected via slits or junctions at the margins of the grana,
which ensures the contiguity of the thylakoid membranes and
their lumenal aqueous phases across the entire granum-stroma
network. The model explains why, with increasing depth in the
serial sections, a given stroma thylakoid appears to be continued
in different granum thylakoids within a granum stack and why it
appears to be shifted in opposite directions on opposite sides of
the granum: downwards and upwards on the left and right sides,
respectively (Figure 1A). It also accounts for the observation that
in near-meridian sections (which are cut close to the margin of
the granum), the stroma thylakoids are observed to be tilted at
+228, which is the tilt angle of the helix (a, Figure 1A), and when
cutting at the opposite side, right behind the granum cylinder, the
tilt angle is found to be –228 (Brangeon and Mustárdy (1979).
The helical structure of the granum-stroma thylakoid membrane system is achieved by self-assembly, which has been
assumed to be initiated by primary growth layers, followed by the
spiral cyclical overgrowth of the vesicles (Paolillo, 1970). In line
Figure 1. Comparison of the Helical Model and the Pairwise Organization Model of the Granum-Stroma Thylakoid Membrane System of
Vascular Plant Chloroplasts.
(A) Computerized form of the helical model constructed from electron
micrographs of full serial sectioning of a granum-stroma assembly.
(Reprinted from Mustárdy and Garab [2003], Figure 3A, with permission
from Elsevier.)
(B) Topological model based on electron tomography. a, tilt angle
between the granum and stroma thylakoid membranes; GT, granum
thylakoid; GTM, granum thylakoid membrane; J, junction between the
granum and stroma thylakoids; ST, STM, and STL, stroma thylakoid,
thylakoid membrane, and lumen, respectively. (Reprinted from Shimoni
et al. [2005], Figure 3.)
with this, Brangeon and Mustárdy (1979) identified dense perforations of the membranes in developing cells and postulated that
stacking was initiated via overlaps from the peripheral growth of
adjacent perforations, the step responsible for the tilt (helix)
angle. According to the suggestion of Paolillo (1970), subsequent
to the outgrowth of the stroma thylakoids populating the intergranal region, fusions take place to link adjacent grana together,
ultimately leading to the formation of the contiguous 3D network
for the entire chloroplast.
The validity of the helical model was later confirmed by other EM
investigations. The side view on the scanning EM by Mustárdy
and Jánossy (1979) showed the helical arrangement of the stroma
membranes, while the upper view on a freeze-fractured sample
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PERSPECTIVE
with a fractured plane parallel to the membrane plane of the
granum (Staehelin and van der Staay, 1996) revealed that the
stroma thylakoid junctions are arranged in a circular fashion
(cf. Mustárdy and Garab, 2003).
ELECTRON TOMOGRAPHY: CONTROVERSIAL MODELS
Recently, a radically different model was proposed on the basis
of electron tomography data. Using an EM operating at 200 kV,
Shimoni et al. (2005) performed electron tomography on 250nm-thick sections of chloroplast thylakoid membranes within
cryoimmobilized, freeze-substituted lettuce leaves stained at
2908C. By such means, this complex membrane system could
be visualized in three dimensions for the first time. As can be seen
in Figure 1B, the topological model of Shimoni et al. (2005) is in
disagreement with the helical model. First, the stroma thylakoids,
running almost perpendicular to the axes of the grana (a = 08),
were proposed to intersect the grana in multiple parallel planes
and not in a helical fashion as in Figure 1A (a = 228). Secondly, the
grana are proposed to be built up from repeating units each
consisting of two layers (shown in red and yellow in Figure 1B),
which are formed by bifurcations of the stroma lamellae (gray).
Thirdly, it is proposed that in each unit, part of the top layer (red)
bends upward and fuses with the layer above it, whereas the
other layer (yellow) bends downward at the opposite side and
fuses with the layer below, within the granum body (Figure 1B).
By contrast, in the helical model (Figure 1A), no bifurcation is
required, growth is governed by overlapping layers and overgrowth, and fusing is proposed to take place in the intergranal
region. Finally, the units of paired thylakoids are rotated relative
to each other around the axis of the granum cylinder (indicated by
blue dashed lines in Figure 1B). In the helical model, the grana
possess cylindrical symmetry and the junctions (slits) are rotated
around the rim of the discs, as dictated by the helix that is wound
around the granum (Figure 1A).
While the above features of the interpretative topological
model of Shimoni et al. (2005) are in disagreement with the
helical model, it is our view that the tomographic images themselves are not in conflict with it. In particular, the tendency of
apparent shifts of stroma membranes between granum layers
with increasing depth can be recognized in the images of
Shimoni et al. (2005) (see Supplemental Figure 1 online); also,
in the near meridian regions, the stroma membranes make an
angle of ;208 relative to the horizontal granum axis (see Supplemental Figure 2 online). Furthermore, the observation that the
stroma lamellae intersect the granum in roughly parallel planes
perpendicular to the cylinder axis does not contradict the helical
model, as middle region in silico sections of the computerassisted helical model exhibit the same feature (Figure 4E in
Mustárdy and Garab, 2003).
In addition, the tomographic images presented by Shimoni
et al. (2005) are ambiguous with respect to the junctions of the
two types of membranes. The lumen of the thylakoid membranes
was not resolved in the images; instead, the thylakoids were seen
as uniformly and negatively stained stripes. This is a relatively
common characteristic of biological specimens prepared by
freeze substitution protocols. While structural preservation is
excellent, positive staining of some or all membranes by OsO4
can be weak or absent. Thus, in the tomographic images of
Shimoni et al. (2005), there is insufficient contrast between the
thylakoid membranes and the protein-containing aqueous phase
of the lumen to achieve a clear picture of the connecting regions.
These connections determine the spatial relationship between
the granum and stroma thylakoids and are of crucial importance
for the 3D model.
In a more recent study, the technique of freeze substitution and
low-temperature fixation and staining combined with tomographic analysis was successfully applied to investigate the
fragile association of plastoglobules with the thylakoid membranes (Austin et al., 2006). In this case, membrane staining was
improved, making the lumenal aqueous phase of thylakoids
visible, and the tomographic analysis was combined with
immunolabeling. However, these authors did not explore the
structure of the junctions between the granum and stroma
membranes.
A recently published study made use of isolated spinach
thylakoid membranes, in which the proteins were washed out
from the stromal aqueous phase to improve contrast (Mustárdy
et al., 2008). Although this may be considered a compromise in
sample preparation, thylakoid membranes of mature granal
chloroplasts are robust and retain their fully functional state
even when isolated from their native environment. Tomographic
series of images were recorded from 250-nm-thick sections of
isolated thylakoid membranes fixed and stained with conventional techniques using an EM operating at 1 mV. The tomograms
obtained under these conditions clearly resolved the heavily
stained membranes, the lumen of the thylakoids, and in most
cases the junctions between the two types of membranes (Figure 2A).
The series of tomographic images recorded under these
conditions were fully consistent with the basic features of the
helical model. In particular, it was observed that with increasing
depth, the stroma thylakoids tended to shift in opposite directions on the opposite sides of the granum cylinder. This can be
seen in Supplemental Movie 1 online, which contains the frames
between 35 and 75 (representing the highest clarity images) of
the 95 frames of the tomographic series recorded by Mustárdy
et al. (2008). (The individual frames can be seen in Supplemental
Figure 3 online, which contains every second tomograms of the
same series.) The apparent shifts of two or three levels of the
same stroma thylakoids, observed in this tomographic series
(Figure 1 in Mustárdy et al., 2008) and in the serial sections
(Figure 4 in Mustárdy and Garab, 2003), respectively, cannot be
reconciled with the organization of paired layers proposed by
Shimoni et al. (2005).
Furthermore, an analysis of the images of Mustárdy et al.
(2008) revealed that in the interconnecting region the apparent
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PERSPECTIVE
Figure 2. Equidistant Tomographic Sections of Chloroplast Granum-Stroma Thylakoid Assemblies.
(A) Close-up views of images from the data set of Mustárdy et al. (2008).
(B) Close-up views of images extracted from Supplemental Movie 1 in Shimoni et al. (2005). F, fork-like structures at the junction of the granum and
stroma thylakoids; GT, GTL, and GTM, granum thylakoid, thylakoid membrane, and lumen, respectively; J and J’, junctions between the granum and
stroma thylakoids; ST, STM, and STL, stroma thylakoid, thylakoid membrane, and lumen, respectively.
shifts between two layers (Figure 2A) usually occurred within
three to five frames. This corresponds to ;8 to 13 nm, which is
close to the estimated 10 to 15 nm resolution limit in the z
direction (McEwen and Marko, 2001). Again, these data are fully
consistent with the helical model and do not support a pairwise
organization of the membrane vesicles. It is worth noting that the
computer-generated surface models applied on the data set of
Mustárdy et al. (2008) were also consistent with the helical
model. These models were derived by hand-tracing of membrane contours in slices from the tomogram using the Sterecon
program (Marko and Leith, 1996) and application of a graphics
accelerator card. Admittedly, there were some uncertainties in
membrane tracing due to the large differences in staining of
granum and stroma membranes.
With respect to the data set of Shimoni et al. (2005), it is more
difficult to determine the number of frames required for the
transition between two layers because the interconnections
cannot be verified at the lumen. Nevertheless, the apparent
shifts also appear to occur within ;30 nm (Figure 2B). These
images are dominated by bifurcated, fork-like structures (Figure
2B), which might argue for a pairwise organization of the thylakoid vesicles. Mustárdy et al. (2008) offered an explanation for
this in terms of the helical model, taking into account the limited z
resolution of the micrographs: when the section includes two
junctions, it can readily combine into a fork in the image (Figure 2
in Mustárdy et al., 2008). Hence, the occurrence of forks in the
images largely depends on the z resolution. Indeed, while some
15 to 20% of the junctions in the serial section micrographs of
Brangeon and Mustárdy (1979), with ;60-nm resolution, obviously formed forks, clear fork-like structures could not be identified in the images of Mustárdy et al. (2008), though in some
cases the fuzziness did not rule out their occurrence in the
transitions.
TOWARD CONSENSUS: A MODIFIED,
QUASIHELICAL MODEL
The above analysis reveals that all the presently available electron tomography and EM data are consistent or at least can be
reconciled with the basic features of the helical model. Further inspection of the data also shows, however, that the helical model
needs important refinements. The proposed self-assembly
mechanism of spiral cyclical overgrowth (Paolillo, 1970) and
the model (Figure 1A) implies a strict periodicity related to the
helical structure. Analysis of the data set of Mustárdy et al. (2008)
shows that the lengths of the slits and the closed margins vary in
a wide range: for single connections when the lumen of a stroma
thylakoid clearly continued into the lumen of a granum thylakoid,
the length varied between 13 and 70 nm, with a mean value of
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PERSPECTIVE
36.4 nm (617.5 nm, n = 19). The length of the marginal regions
(i.e., when the granum membrane was not continued in stroma
thylakoids) varied between 29 and 88 nm, with an average of 52
nm (615.5 nm, n = 11). While the multiplicity of the connecting
junctions around the rim of granum thylakoids is in good agreement with the helical model, these data show that the periodicity
of the slits (and of the closed margins) is far less marked than
would be expected from the model. This finding calls into
question the mechanism of self-assembly of the granum-stroma
thylakoid membrane system via spiral cyclical overgrowth
(Paolillo, 1970). The hypothesis put forward in the following
paragraphs takes into account these data and other up-to-date
information on the membrane constituents and on relevant
molecular mechanisms.
First, it is important to stress that stacking can occur only
between PSII membranes, which possess flat surfaces: LHCII
and the PSII supercomplex display merely a very low level of
protrusion to the stroma, while PSI and ATP synthase have
extensive stroma-exposed structures (Dekker and Boekema,
2005). The lateral heterogeneity of the stacked and unstacked
thylakoid membrane regions is induced by (and depends on) the
formation of large domains enriched in flat LHCII and PSII
complexes, stacking of these regions, and the extrusion of the
complexes with large stroma exposed structures (Arntzen, 1978;
Andersson and Anderson, 1980; Barber, 1982; Garab and
Mustárdy, 1999; Chow et al., 2005). From a structural point of
view, these latter complexes will act as spacers between the
unstacked membranes. Nevertheless, by their segregation the
packing density of the entire membrane system becomes optimized (Mustárdy and Garab, 2003).
For the self-assembly, let us consider a pair of membranes
with a stacked region; this can be formed via overlaps from
the peripheral growth of adjacent perforations (Brangeon and
Mustárdy, 1979). Instead of the cyclical growth of this unit, we
hypothesize that new layers can be added to this initiation of
granum from independently growing thylakoid membranes, provided that they arrive from a proper angle, to avoid spatial
hindrance. This step introduces an asymmetry (i.e., a helical
element). When the newly synthesized thylakoid approaches an
existing granum-stroma unit, again to an appropriate distance
and at a suitable angle, it can fuse with the granum in the marginal
region, opening a slit and thus making the junction. Upon further
growth, this thylakoid might flip over the granum to form a new
layer, as can be seen in Figure 1A (top layer; see also Figure 2 in
Mustárdy et al., 2008).
In summary, in our view, all electron tomography data are
basically in harmony with the helical organization of the stroma
thylakoid membranes around the granum but also suggest
significant refinements both in the 3D arrangement of the membranes and the molecular mechanisms that are involved in their
buildup. The self-assembly of this quasihelical membrane system, with less periodicity than earlier thought, is probably
governed by the growth, fusion, and overlapping of the membrane vesicles and mechanisms that sort the membrane com-
ponents between the grana stacks and the intervening
unstacked stroma membranes, rather than by spiral cyclical
growth proposed in the original helical model (Paolillo, 1970).
Future systematic tomographic experiments, perhaps with refined preparative techniques on a variety of plant materials and
under a variety of physiological conditions, possibly combined
with other, noninvasive physical investigations, such as small
angle x-ray and neutron scattering, are required for a deeper
understanding of the structure and structural flexibility of this
intricate membrane system.
Supplemental Data
The following materials are available in the online version of this article.
Supplemental Figure 1. Electron Tomographic Sections of a
Granum-Stroma Thylakoid Assembly from Cryoimmobilized, FreezeSubstituted Lettuce Leaves.
Supplemental Figure 2. Electron Tomographic Sections of a Chloroplast from Cryoimmobilized, Freeze-Substituted Lettuce Leaves.
Supplemental Figure 3. A TIFF Series of 20 Electron Tomographic
Sections of Granum-Stroma Thylakoid Assemblies, Showing Every
Second Tomogram of the Series Shown in the Supplemental Movie 1.
Supplemental Movie 1. A Sequence of Electron Tomographic Sections of Granum-Stroma Thylakoid Assemblies of Isolated Spinach
Thylakoid Membranes.
ACKNOWLEDGMENTS
We benefited from helpful discussions with C. Mannella; his continued
interest and support are also gratefully acknowledged. We also thank
the help from the group at the Resource for Visualization of Biological
Complexity (RVBC; Albany, NY), in particular, Michael Marko and David
Barnard. This work has been supported by Marie Curie Grant MCRTNCT-2003-505069 and grants from the Hungarian Fund for Basic
Research (OTKA T42696 and K63252). Development of electron tomography at the RVBC is supported by the National Center for Research Resources, National Institutes of Health, Grant RR01219.
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The Three-Dimensional Network of the Thylakoid Membranes in Plants: Quasihelical Model of
the Granum-Stroma Assembly
László Mustárdy, Karolyn Buttle, Gábor Steinbach and Gyozo Garab
Plant Cell 2008;20;2552-2557; originally published online October 24, 2008;
DOI 10.1105/tpc.108.059147
This information is current as of March 5, 2014
Supplemental Data
http://www.plantcell.org/content/suppl/2008/06/30/tpc.108.059147.DC1.html
References
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