Significance of the Photosystem II Core Phosphatase PBCP for Plant Viability and Protein Repair in Thylakoid Membranes

Puthiyaveetil, Sujith; Woodiwiss, Timothy; Knoerdel, Ryan; Zia, Ahmad; Wood, Magnus; Hoehner, Ricarda; Kirchhoff, Helmut

doi:10.1093/pcp/pcu062

Cited by 39 publications

(28 citation statements)

References 48 publications

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“…Chl a/b ratio in our growth condition is about 3.5 for unknown reasons (see stn7 above). pbcp Lack of the PBCP phosphatase pbcp has impaired dephosphorylation of PSII core proteins in state 1 condition and slightly increased phosphorylation of PSII core proteins in GL and darkness as well as in photoinhibitory light condition (Puthiyaveetil et al, 2014); reported to have minor modulations in the thylakoid structure , thylakoid protein composition, and PSII function (Puthiyaveetil et al, 2014); delayed D1 degradation in photoinhibitory conditions (Puthiyaveetil et al, 2014). Chl a/b ratio in our growth condition is about 3.3. pgr5…”

Section: Dph Across the Thylakoid Membrane Has A Strong Influence On mentioning

confidence: 68%

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Plants Actively Avoid State Transitions upon Changes in Light Intensity: Role of Light-Harvesting Complex II Protein Dephosphorylation in High Light

et al. 2015

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ORCID IDs: 0000-0002-6309-5532 (N.R.M.); 0000-0002-2753-9597 (M.T.).Photosystem II (PSII) core and light-harvesting complex II (LHCII) proteins in plant chloroplasts undergo reversible phosphorylation upon changes in light intensity (being under control of redox-regulated STN7 and STN8 kinases and TAP38/PPH1 and PSII core phosphatases). Shift of plants from growth light to high light results in an increase of PSII core phosphorylation, whereas LHCII phosphorylation concomitantly decreases. Exactly the opposite takes place when plants are shifted to lower light intensity. Despite distinct changes occurring in thylakoid protein phosphorylation upon light intensity changes, the excitation balance between PSII and photosystem I remains unchanged. This differs drastically from the canonical-state transition model induced by artificial states 1 and 2 lights that concomitantly either dephosphorylate or phosphorylate, respectively, both the PSII core and LHCII phosphoproteins. Analysis of the kinase and phosphatase mutants revealed that TAP38/PPH1 phosphatase is crucial in preventing state transition upon increase in light intensity. Indeed, tap38/pph1 mutant revealed strong concomitant phosphorylation of both the PSII core and LHCII proteins upon transfer to high light, thus resembling the wild type under state 2 light. Coordinated function of thylakoid protein kinases and phosphatases is shown to secure balanced excitation energy for both photosystems by preventing state transitions upon changes in light intensity. Moreover, PROTON GRADIENT REGULATION5 (PGR5) is required for proper regulation of thylakoid protein kinases and phosphatases, and the pgr5 mutant mimics phenotypes of tap38/pph1. This shows that there is a close cooperation between the redox-and proton gradient-dependent regulatory mechanisms for proper function of the photosynthetic machinery.

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Section: Dph Across the Thylakoid Membrane Has A Strong Influence On mentioning

confidence: 68%

“…2). Moreover, PBCP is required to dephosphorylate PSII core protein in traditional state 1 and has also been linked to dephosphorylation of PSII core protein in photoinhibitory conditions (Puthiyaveetil et al, 2014). Despite such an obvious role of PBCP phosphatase in dephosphorylation of PSII core proteins Puthiyaveetil et al, 2014;Fig.…”

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confidence: 99%

Plants Actively Avoid State Transitions upon Changes in Light Intensity: Role of Light-Harvesting Complex II Protein Dephosphorylation in High Light

et al. 2015

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“…This implies that the constant dephosphorylated status of the potential substrate of these PP2Cs acts in a physiological or physical negative manner with regard to defence. Although no visible phenotype change was observed in the experiment, the atpp2c26 single mutant has been reported to show a concomitant reduction in the number of layers in the grana stacks (Samol et al ., ), and further analysis of the thylakoid membrane protein composition of this mutant characterized its smaller PSII antenna, whereas cytochrome (Cyt) b 6 f complexes and PSI were similar to those of the wild‐type (Puthiyaveetil et al ., ). Thus, the attenuation of the PSII antenna may lead to the enhancement of the basal defence system.…”

Section: Discussionmentioning

confidence: 97%

Loss of chloroplast‐localized protein phosphatase 2Cs in Arabidopsis thaliana leads to enhancement of plant immunity and resistance to Xanthomonas campestris pv. campestris infection

Akimoto-Tomiyama

Tanabe

Kajiwara

et al. 2017

Molecular Plant Pathology

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Protein phosphatases (PPs) counteract kinases in reversible phosphorylation events during numerous signal transduction pathways in eukaryotes. PP2Cs, one of the four major classes of the serine/threonine-specific PP family, are greatly expanded in plants. Thus, PP2Cs are thought to play a specific role in signal transduction pathways. Some rice PP2Cs classified in subgroup K are responsive to infection by the compatible Xanthomonas oryzae pv. oryzae, the causal agent of bacterial blight. In Arabidopsis thaliana, orthologous PP2C genes (AtPP2C62 and AtPP2C26) classified to subgroup K are also responsive to Xanthomonas campestris pv. campestris (Xcc, causal agent of black rot) infection. To elucidate the function of these subgroup K PP2Cs, atpp2c62- and atpp2c26-deficient A. thaliana mutants were characterized. A double mutant plant which was inoculated with a compatible Xcc showed reduced lesion development, as well as the suppression of bacterial multiplication. AtPP2C62 and AtPP2C26 localized to the chloroplast. Furthermore, the photosynthesis-related protein, chaperonin-60, was indicated as the potential candidate for the dephosphorylated substrate catalysed by AtPP2C62 and AtPP2C26 using two-dimensional isoelectric focusing sodium dodecylsulfate-polyacrylamide gel electrophoresis (2D-IDF-SDS-PAGE). Taken together, AtPP2C62 and AtPP2C26 are suggested to be involved in both photosynthesis and suppression of the plant immune system. These results imply the occurrence of crosstalk between photosynthesis and the plant defence system to control productivity under pathogen infection.

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“…Phosphorylation levels of PS II core proteins D1, D2, and CP43 in membrane fractions were estimated with an antiphosphothreonine antibody (Cell Signaling) essentially as described by Puthiyaveetil et al (38). Samples were loaded on an equal cyt b 559 basis.…”

Section: Stn8mentioning

confidence: 99%

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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Significance of the Photosystem II Core Phosphatase PBCP for Plant Viability and Protein Repair in Thylakoid Membranes

Cited by 39 publications

References 48 publications

Plants Actively Avoid State Transitions upon Changes in Light Intensity: Role of Light-Harvesting Complex II Protein Dephosphorylation in High Light

Plants Actively Avoid State Transitions upon Changes in Light Intensity: Role of Light-Harvesting Complex II Protein Dephosphorylation in High Light

Loss of chloroplast‐localized protein phosphatase 2Cs in Arabidopsis thaliana leads to enhancement of plant immunity and resistance to Xanthomonas campestris pv. campestris infection

Compartmentalization of the protein repair machinery in photosynthetic membranes

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