Do Grana Margins of Thylakoid Membranes form a Functional Domain During Repair Cycle of Photosystem II ?

Kettunen, Reetta; Tyystjärvi, Esa; Aro, Eva‐Mari

doi:10.1007/978-94-009-0173-5_774

Cited by 4 publications

(4 citation statements)

References 2 publications

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“…The meaning of a limiting "lateral destacking threshold" remains to be elucidated, but points to structural and compositional differences within the grana, that is, between core grana and peripheral grana. This is in line with the hypothesis that grana margins form a functional domain for the PSII repair cycle (35), which allows for efficient contact between damaged PSII and its repair machinery.…”

Section: Discussionsupporting

confidence: 89%

Architectural switch in plant photosynthetic membranes induced by light stress

Herbstová

Tietz

Kinzel

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

143

113

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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...

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Section: Discussionsupporting

confidence: 89%

Architectural switch in plant photosynthetic membranes induced by light stress

Herbstová

Tietz

Kinzel

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

143

113

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“…The sublocalization analysis of components involved in PS II repair (Fig. 3) reveals a pronounced heterogeneity along the thylakoid membrane and highlights the pivotal role of grana margins (23,36). The heterogeneous distribution of PS II repair proteins leads to a division of labor between the different thylakoid subcompartments, constituting a specific order of events.…”

Section: Discussionmentioning

confidence: 98%

Compartmentalization of the protein repair machinery in photosynthetic membranes

Puthiyaveetil

Tsabari

Lowry

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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A crucial component of protein homeostasis in cells is the repair of damaged proteins. The repair of oxygen-evolving photosystem II (PS II) supercomplexes in plant chloroplasts is a prime example of a very efficient repair process that evolved in response to the high vulnerability of PS II to photooxidative damage, exacerbated by high-light (HL) stress. Significant progress in recent years has unraveled individual components and steps that constitute the PS II repair machinery, which is embedded in the thylakoid membrane system inside chloroplasts. However, an open question is how a certain order of these repair steps is established and how unwanted back-reactions that jeopardize the repair efficiency are avoided. Here, we report that spatial separation of key enzymes involved in PS II repair is realized by subcompartmentalization of the thylakoid membrane, accomplished by the formation of stacked grana membranes. The spatial segregation of kinases, phosphatases, proteases, and ribosomes ensures a certain order of events with minimal mutual interference. The margins of the grana turn out to be the site of protein degradation, well separated from active PS II in grana core and de novo protein synthesis in unstacked stroma lamellae. Furthermore, HL induces a partial conversion of stacked grana core to grana margin, which leads to a controlled access of proteases to PS II. Our study suggests that the origin of grana in evolution ensures high repair efficiency, which is essential for PS II homeostasis.photosynthesis | photoinhibition | PS II repair cycle | thylakoid membrane | grana margin R epair of damaged protein complexes is essential for the survival of all living organisms. One of nature's most efficient repair machineries is localized in photosynthetic thylakoid membranes of plants, which can turn over the total pool of the watersplitting photosystem II (PS II) supercomplex in less than 1 h (1). This remarkable potential for protein repair is crucial for the survival and fitness of plants because photodamage by reactive oxygen species is an inherent feature of PS II photochemistry. Significant knowledge gained over the past decade identifies individual steps involved in PS II repair. This progress has led to the formulation of a repair cycle that describes the life cycle of PS II, proceeding from its damage, disassembly, degradation, and resynthesis to its reassembly (2-4).To appreciate the challenges for repairing damaged PS II, it is essential to understand two structural features of the thylakoid membrane system. The first is that functional PS II is organized as a dimeric 1.4-MDa supercomplex in which each monomer consists of at least 28 subunits with two trimeric light harvesting complexes II (LHC II) attached to the core (5, 6). Within this huge supercomplex, the main target of photodamage is the central D1 subunit (7). The PS II repair cycle is therefore mainly designed for specific replacement of the damaged D1, which requires disassembly and reassembly of the whole supercomplex. The second characteri...

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“…So far, these considerations mainly addressed the relationship between grana core and stroma lamellae. The role of grana margins is unclear but as they are at the interface between the two other thylakoid regions, it is likely that they play a pivotal role for the PSII repair cycle [53]. More studies are required to unravel the function of grana margins for protein repair in thylakoid membranes.…”

Section: Psii Repair Cyclementioning

confidence: 99%

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

Kirchhoff

2014

Phil. Trans. R. Soc. B

104

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Land plants live in a challenging environment dominated by unpredictable changes. A particular problem is fluctuation in sunlight intensity that can cause irreversible damage of components of the photosynthetic apparatus in thylakoid membranes under high light conditions. Although a battery of photoprotective mechanisms minimize damage, photoinhibition of the photosystem II (PSII) complex occurs. Plants have evolved a multi-step PSII repair cycle that allows efficient recovery from photooxidative PSII damage. An important feature of the repair cycle is its subcompartmentalization to stacked grana thylakoids and unstacked thylakoid regions. Thus, understanding the crosstalk between stacked and unstacked thylakoid membranes is essential to understand the PSII repair cycle. This review summarizes recent progress in our understanding of high-light-induced structural changes of the thylakoid membrane system and correlates these changes to the efficiency of the PSII repair cycle. The role of reversible protein phosphorylation for structural alterations is discussed. It turns out that dynamic changes in thylakoid membrane architecture triggered by high light exposure are central for efficient repair of PSII.

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Do Grana Margins of Thylakoid Membranes form a Functional Domain During Repair Cycle of Photosystem II ?

Cited by 4 publications

References 2 publications

Architectural switch in plant photosynthetic membranes induced by light stress

Architectural switch in plant photosynthetic membranes induced by light stress

Compartmentalization of the protein repair machinery in photosynthetic membranes

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

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