Three-Dimensional Organization of Higher-Plant Chloroplast Thylakoid Membranes Revealed by Electron Tomography

Abstract

The light-harvesting and energy-transducing functions of the chloroplast are performed within an intricate lamellar system of membranes, called thylakoid membranes, which are differentiated into granum and stroma lamellar domains. Using dualaxis electron microscope tomography, we determined the three-dimensional organization of the chloroplast thylakoid membranes within cryo-immobilized, freeze-substituted lettuce (Lactuca sativa) leaves. We found that the grana are built of repeating units that consist of paired layers formed by bifurcations of stroma lamellar sheets, which fuse within the granum body. These units are rotated relative to each other around the axis of the granum cylinder. One of the layers that makes up the pair bends upwards at its edge and fuses with the layer above it, whereas the other layer bends in the opposite direction and merges with the layer below. As a result, each unit in the granum is directly connected to its neighbors as well as to the surrounding stroma lamellae. This highly connected morphology has important consequences for the formation and function of the thylakoid membranes as well as for their stacking/unstacking response to variations in light conditions.

Assessment of the requirement for aquaporins in the thylakoid membrane of plant chloroplasts to sustain photosynthetic water oxidation

“…In land plants and green algae, PSII is restricted to cylindrical stacks of grana thylakoids, PSI and the ATP-synthase are only found in stroma-exposed regions of the thylakoid membrane, and cytochrome b 6 f is found in both types of membranes. Despite heterogeneity in organization and composition, the thylakoid network encloses a tiny but continuous aqueous space, named thylakoid lumen [4].…”

IM30 triggers membrane fusion in cyanobacteria and chloroplasts

“…Although it is clear that fusion proteins are essential for the formation and maintenance of TMs, surprisingly, not a single fusion-inducing protein has been identified in TM-containing organisms yet. Fusion of individual TM sheets and of the CM and TMs has previously been observed in chloroplasts and cyanobacteria 9,11 , and in chloroplasts, with changing light conditions the architecture of the TM network rearranges, involving membrane fission and fusion events 10 . As in chloroplasts, also in cyanobacteria, the TM network can be highly interconnected 41 , and it is thus likely that the TM system of cyanobacteria is as ARTICLE dynamic as in chloroplasts and undergoes remodelling under changing growth conditions or in the course of development 6 .…”

“…Regulated material transfer between the IE/CM and the TMs have been proposed to be mediated by vesicular transport or via direct connections between the membrane systems 6,7 . Direct connections between the IE and TM have been observed in chloroplasts 8,9 , and TM membrane reorganization is also suggested to involve dynamic fission and fusion events, as found in the membranes of the mitochondria, endoplasmic reticulum and the Golgi apparatus 10 . In the cyanobacterium Synechocystis sp.…”

Molecular Architecture of Plant Thylakoids under Physiological and Light Stress Conditions: A Study of Lipid-Light-Harvesting Complex II Model Membranes

“…This internal membrane system is laterally differentiated into densely stacked domains (grana) and unstacked regions (stroma lamellae) (Mustárdy and Garab, 2003;Shimoni et al, 2005;Mustárdy et al, 2008;Austin and Staehelin, 2011;Kouril et al, 2011). The thylakoid membrane is a highly dynamic system capable of adapting to changing environmental conditions.…”