Architectural switch in plant photosynthetic membranes induced by light stress

Abstract

Unavoidable side reactions of photosynthetic energy conversion can damage the water-splitting photosystem II (PSII) holocomplex embedded in the thylakoid membrane system inside chloroplasts. Plant survival is crucially dependent on an efficient molecular repair of damaged PSII realized by a multistep repair cycle. The PSII repair cycle requires a brisk lateral protein traffic between stacked grana thylakoids and unstacked stroma lamellae that is challenged by the tight stacking and low protein mobility in grana. We demonstrated that high light stress induced two main structural changes that work synergistically to improve the accessibility between damaged PSII in grana and its repair machinery in stroma lamellae: lateral shrinkage of grana diameter and increased protein mobility in grana thylakoids. It follows that high light stress triggers an architectural switch of the thylakoid network that is advantageous for swift protein repair. Studies of the thylakoid kinase mutant stn8 and the double mutant stn7/8 demonstrate the central role of protein phosphorylation for the structural alterations. These findings are based on the elaboration of mathematical tools for analyzing confocal laser-scanning microscopic images to study changes in the sophisticated thylakoid architecture in intact protoplasts.confocal microscopy | macromolecular crowding | photosynthesis P hotosynthetic transformation of sunlight into metabolic energy equivalents is a dangerous venture, because toxic side products of the primary photochemical processes can lead to uncontrolled damage. Harmful photosynthetic side reactions cannot be avoided completely and become a serious problem under stress (e.g., high light stress). The main target of photoinhibition (PI) is the D1 subunit of the water-splitting photosystem II (PSII) (1, 2). The D1 subunit is buried in the massive (1,400 kDa) PSII holocomplex that is organized as a dimer and binds between two and four trimeric light-harvesting complex IIs (LHCIIs) (3, 4). Estimates predict that without repair of damaged PSII, the efficiency for photosynthetic energy conversion would drop below 5% (5). Consequently, plants would not survive in a highly dynamic and competitive natural environment. Plants address this challenge through the evolutionary invention of one of the fastest and most efficient molecular repair mechanisms in nature, the PSII repair cycle (5-7).The PSII repair cycle consist of a series of events, including phosphorylation/ dephosphorylation of PSII subunits, holocomplex disassembly/reassembly, and D1 degradation/de novo synthesis (8-10). All of these reactions are harbored in or at the thylakoid membrane system inside the chloroplast. The complex folding of the thylakoid membrane leads to a structural differentiation into stacked grana regions interconnected by unstacked stroma lamellae (11)(12)(13). This structural heterogeneity is accompanied by, and partly driven by, differential protein distributions. PSII and LHCII are concentrated in grana stacks, photosystem I (PSI) and the ATPas...

Differential Mobility of Pigment-Protein Complexes in Granal and Agranal Thylakoid Membranes of C3 and C4 Plants

“…It is important to note that although 70% to 80% of the protein complexes in grana are virtually immobile, the remaining protein complexes are very mobile . It is likely that the mobile fraction increases under environmental conditions that require brisk lateral protein transport through the crowded grana (Herbstová et al, 2012). In unstacked thylakoid membranes, the need to pack protein complexes tightly is not required because of the nonmodular organization of the PSI/LHCI system.…”

“…The situation in native membranes of C 3 plants is more complex than in the computer simulations. For example, phosphorylation of damaged PSII subunits causes a slight overall increase in protein mobility (Goral et al, 2010;Herbstová et al, 2012) and disassembly of the supercomplex (Pesaresi et al, 2011;Tikkanen and Aro, 2012). Both could speed up lateral diffusion of damaged PSII out of the grana.…”

Structural changes of the thylakoid membrane network induced by high light stress in plant chloroplasts

“…Therefore, the structural relationship of grana core, grana margins and stroma lamellae is relevant for efficient PSII repair. In recent years, it has come into focus that high light stress is accompanied by changes in macroscopic thylakoid folding [39,48,49]. From these studies, a partial destacking of grana was concluded, i.e.…”

“…By using fluorescence recovery after photobleaching (FRAP), it was measured that high light treatment increases the rate of protein exchange between different grana discs [60] and the mobility within isolated grana membranes [49]. The significance for the PSII repair cycle is given by the fact that under non-stressed conditions, protein (PSII) mobility in stacked grana is very low [60][61][62].…”

TEF30 Interacts with Photosystem II Monomers and Is Involved in the Repair of Photodamaged Photosystem II in Chlamydomonas reinhardtii

“…Lateral migration of damaged PSII complexes is facilitated by thylakoid membrane unfolding and PSII supercomplex disassembly. Both processes are enhanced by the phosphorylation of the PSII core subunits D1, D2, CP43, and PsbH, which is mainly mediated by the protein kinase STATE TRANSITION8 (STN8; Tikkanen et al, 2008;Fristedt et al, 2009;Herbstová et al, 2012;Nath et al, 2013b;Wunder et al, 2013). Efficient PSII supercomplex disassembly also requires the THYLAKOID FORMATION1 (THF1)/NON-YELLOW COLORING4 (NYC4)/Psb29 protein Yamatani et al, 2013).…”