Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light

Tikkanen, Mikko; Nurmi, Markus; Kangasjärvi, Saijaliisa; Aro, Eva‐Mari

doi:10.1016/j.bbabio.2008.08.004

Cited by 189 publications

(265 citation statements)

References 28 publications

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“…The unchanged D1 level without lincomycin is the result of a balanced D1 degradation and de novo synthesis by the PSII repair cycle. Overall, the characteristics of HL-induced PSII inactivation and D1 degradation in protoplasts were similar to those seen in leaves (24).…”

Section: Resultssupporting

confidence: 52%

“…One of these factors is disassembly of the dimeric holocomplex to a smaller monomeric unit. Although evidence indicates that PI leads to phosphorylation-dependent dismantling of the PSII holocomplex (23,24), the consequences for PSII mobility are less clear. For example, the correlation between particle size and particle mobility in crowded grana is difficult to predict.…”

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confidence: 99%

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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: Resultssupporting

confidence: 52%

mentioning

confidence: 99%

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

View full text Add to dashboard Cite

show abstract

“…Therefore, disassembly of the holocomplex is required to make the damaged D1 subunit accessible to proteases and to allow insertion of the newly synthesized copy [27,33]. Consequently, an important step in the PSII repair cycle is the disassembly of the PSII holocomplex.…”

Section: Psii Repair Cyclementioning

confidence: 99%

“…The mainstream model is that after high-light-induced damage, the PSII subunits D1, D2, CP43 and psbH are phosphorylated (figure 1(2)), catalysed mainly by the STN8 kinase [34,35] and possibly by the STN7 kinase [36][37][38]. As evidence exists that in STN7/STN8 double mutants, the disassembly of the PSII holocomplex is inhibited [33,[39][40][41], it was hypothesized that phosphorylation of core subunits triggers disassembly ( figure 1(3)). It is further assumed that the stripped down and phosphorylated PSII complex is the form that diffuses from stacked to unstacked thylakoid regions ( figure 1(4)) where the repair machinery is localized.…”

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

107

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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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“…The functional PSII complex in vascular plants is predominantly localized in the grana regions of the thylakoid membrane, whereas insertion of newly synthesized D1, de novo PSII biogenesis, and assembly processes during the repair cycle are suggested to occur mainly in nonappressed stroma lamellar sheets (Danielsson et al, 2006;Tikkanen et al, 2008). This is supported by the localization of the PSII assembly factor HCF136 in stroma lamellae, polysome binding to exposed thylakoids, cotranslational assembly of D1, and the preferential appearance of distinct smaller PSII subcomplexes in stroma lamellae (Yamamoto et al, 1981;Meurer et al, 1998;Zhang et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

PsbN Is Required for Assembly of the Photosystem II Reaction Center in Nicotiana tabacum

et al. 2014

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ORCID ID: 0000-0003-2973-9514 (J.M.)The chloroplast-encoded low molecular weight protein PsbN is annotated as a photosystem II (PSII) subunit. To elucidate the localization and function of PsbN, encoded on the opposite strand to the psbB gene cluster, we raised antibodies and inserted a resistance cassette into PsbN in both directions. Both homoplastomic tobacco (Nicotiana tabacum) mutants ΔpsbN-F and ΔpsbN-R show essentially the same PSII deficiencies. The mutants are extremely light sensitive and failed to recover from photoinhibition. Although synthesis of PSII proteins was not altered significantly, both mutants accumulated only ;25% of PSII proteins compared with the wild type. Assembly of PSII precomplexes occurred at normal rates, but heterodimeric PSII reaction centers (RCs) and higher order PSII assemblies were not formed efficiently in the mutants. The ΔpsbN-R mutant was complemented by allotopic expression of the PsbN gene fused to the sequence of a chloroplast transit peptide in the nuclear genome. PsbN represents a bitopic trans-membrane peptide localized in stroma lamellae with its highly conserved C terminus exposed to the stroma. Significant amounts of PsbN were already present in dark-grown seedling. Our data prove that PsbN is not a constituent subunit of PSII but is required for repair from photoinhibition and efficient assembly of the PSII RC.

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Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light

Cited by 189 publications

References 28 publications

Architectural switch in plant photosynthetic membranes induced by light stress

Architectural switch in plant photosynthetic membranes induced by light stress

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

PsbN Is Required for Assembly of the Photosystem II Reaction Center in Nicotiana tabacum

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