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. 2011 Apr;155(4):1601-11.
doi: 10.1104/pp.110.170647. Epub 2011 Jan 11.

Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography

Jotham R Austin 2nd  1 , L Andrew Staehelin
Affiliations

Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography

Jotham R Austin 2nd et al. Plant Physiol. 2011 Apr.

Abstract

We have investigated the three-dimensional (3D) architecture of the thylakoid membranes of Arabidopsis (Arabidopsis thaliana), tobacco (Nicotiana tabacum), and spinach (Spinacia oleracea) with a resolution of approximately 7 nm by electron tomography of high-pressure-frozen/freeze-substituted intact chloroplasts. Higher-plant thylakoids are differentiated into two interconnected and functionally distinct domains, the photosystem II/light-harvesting complex II-enriched stacked grana thylakoids and the photosystem I/ATP synthase-enriched, nonstacked stroma thylakoids. The grana thylakoids are organized in the form of cylindrical stacks and are connected to the stroma thylakoids via tubular junctions. Our data confirm that the stroma thylakoids are wound around the grana stacks in the form of multiple, right-handed helices at an angle of 20° to 25° as postulated by a helical thylakoid model. The junctional connections between the grana and stroma thylakoids all have a slit-like architecture, but their size varies tremendously from approximately 15 × 30 nm to approximately 15 × 435 nm, which is approximately 5 times larger than seen in chemically fixed thylakoids. The variable slit length results in less periodicity in grana/stroma thylakoid organization than proposed in the original helical model. The stroma thylakoids also exhibit considerable architectural variability, which is dependent, in part, on the number and the orientation of adjacent grana stacks to which they are connected. Whereas some stroma thylakoids form solid, sheet-like bridges between adjacent grana, others exhibit a branching geometry with small, more tubular sheet domains also connecting adjacent, parallel stroma thylakoids. We postulate that the tremendous variability in size of the junctional slits may reflect a novel, active role of junctional slits in the regulation of photosynthetic function. In particular, by controlling the size of junctional slits, plants could regulate the flow of ions and membrane molecules between grana and stroma thylakoid membrane domains.

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Figures

Figure 1.
Figure 1.
Electron tomogram of a high-pressure-frozen and freeze-substituted chloroplast. Shown is a composite tomographic slice image (five superimposed serial 2.2-nm optical slices) of the interconnecting grana stacked thylakoids (gt) and stroma thylakoids (st).
Figure 2.
Figure 2.
An overview of grana and stroma thylakoid organization. A to C are three composite tomographic slice images (five superimposed 2.2-nm optical slices) showing views from the front (A), middle (B), and back (C) of a grana thylakoid stack. D and E are tomographic reconstructed models of the grana stack shown in A to C, with the grana thylakoids colored yellow and the stroma thylakoids colored green. Front view in D, and the model (E) is rotated 180° to show the back view. Note that for illustrative purposes the model does not display all of the thylakoids associated with the grana stacks.
Figure 3.
Figure 3.
Serial tomographic slice images through a grana thylakoid stack and reconstructed models of the stack. A is a tomographic model of a grana stack. Grana thylakoids are colored yellow, and interconnecting stoma thylakoids are colored and numbered so their position can be tracked in the serial tomographic slices B to K. B to K show serial 2.2-nm tomographic slice images at specific z intervals through the grana stack.
Figure 4.
Figure 4.
Electron tomogram serial sections illustrating the structure of the junctional connections between grana thylakoids and a helical stroma thylakoid. A to J show serial 2.2-nm tomographic slice images through grana-stroma thylakoid connections. The grana stack thylakoids are colored yellow and lettered A to D, and the stoma thylakoids are colored green. Also, the stroma-grana connections are marked with arrows. Note that in A the stroma thylakoid connects with the grana thylakoid marked C. In B to D the stroma thylakoid connect with grana thylakoids C and B. In E and F the stroma thylakoid is connected with grana thylakoid B only. In G to I the stroma thylakoid is connected with grana thylakoids B and A. Finally in J the stroma thylakoid is connected to grana A only.
Figure 5.
Figure 5.
Tomographic model of a granum with associated stroma thylakoid. A depicts an image composed of five superimposed 2.2-nm serial tomographic slices. Grana thylakoids are colored yellow with interconnected stroma thylakoids colored green. B, Rotated (x = −35, y = 49.1, and z = −4.23) tomographic slice image of A. Note the stroma thylakoid connects with seven grana thylakoid membranes (marked with arrows). C is a colored version of B, with grana thylakoids highlighted yellow and stroma thylakoids green. D shows a tomographic model of the grana stack and stoma thylakoid shown in A. The black arrowheads mark the smaller-size, slit-like stroma-grana connections, whereas the white arrowheads mark one stroma-grana connection that is approximately twice the length of the other stroma-grana connections. See histogram Figure 7 for quantitative information on the slit size dimensions.
Figure 6.
Figure 6.
Spatial distribution of differently sized grana-stroma connections on a grana stack. A is a tomographic model showing the top view of a grana stack (gt), with interconnected stroma thylakoids (st). B is a rotated (90°) tomographic model of A. C is a tomographic model of B where the stroma thylakoid has been partially cut away to reveal the connection site between the stroma and grana membranes (highlighted black). D is a tomographic model in which all of the stroma thylakoid membrane on the front side of the grana stack have been removed, revealing all of the stroma-grana connecting sites (highlighted in black). Note the white arrowheads pointing to a stroma-grana connecting site that is much longer than the others.
Figure 7.
Figure 7.
Histogram demonstrating the variation in junctional slit lengths between grana and stroma thylakoids.
Figure 8.
Figure 8.
Tomographic models showing the variation in stroma architecture. A shows a tomographic model with parallel, sheet-like stroma thylakoid membranes (st; colored green, pink, and red) that bridge the space between two grana thylakoid stacks (gt; colored yellow), but that are not connected to each other. B to D is the same model as A, but rotated 90° showing the sheet-like architecture of the individual stroma thylakoids; green (B), pink (C), and red (D) stroma thylakoids. E illustrates another tomographic model in which quasi-helical stroma thylakoids (st; colored green, red, turquoise, and pink) are seen to connect two grana stacks (gt; colored yellow). F and G, Same model as E, but F is rotated 60° to better demonstrate the 3D interconnectivity of the green (semitransparent) and the red stroma thylakoid membranes; G is rotated 45° and shows the interconnectivity between the red and turquoise stroma thylakoid membranes.
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