Regulation of D1-protein degradation during photoinhibition of photosystem II in vivo: Phosphorylation of the D1 protein in various plant groups

Rintamäki, Eevi; Salo, Riitta; Lehtonen, Elina; Aro, Eva‐Mari

doi:10.1007/bf00202595

Cited by 77 publications

(46 citation statements)

References 45 publications

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“…PSII is a subject for photoinhibition (21,22), which is directly proportional to light intensity (23) and occurs because of inactivation of the D1 reaction center protein (24). This central functional subunit of PSII undergoes a very fast turnover (25,26) that necessitates the repair cycle of PSII and depends on the phosphorylation status of D1 (27)(28)(29). Phosphorylation of PSII proteins at high irradiances controls stability of the photosystem, whereas stepwise dephosphorylation of CP43, D2, and D1 proteins is part of a repair cycle during lateral migration of PSII in the membrane and with its disassembly followed by degradation of photodamaged D1, which occurs only after complete dephosphorylation of this protein (4,30).…”

mentioning

confidence: 99%

STN8 Protein Kinase in Arabidopsis thaliana Is Specific in Phosphorylation of Photosystem II Core Proteins

Vainonen¹,

Hansson

Vener

2005

Journal of Biological Chemistry

190

253

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light-exposed leaves of two Arabidopsis lines with T-DNA insertions in the stn8 gene was found significantly reduced in the assays with anti-phosphothreonine antibodies. Protein phosphorylation in each of the mutants was quantified comparatively to the wild type by mass spectrometric analyses of phosphopeptides released from the photosynthetic membranes and differentially labeled with stable isotopes. The lack of STN8 caused 50 -60% reduction in D1 and D2 phosphorylation, but did not change the phosphorylation level of two peptides that could correspond to light-harvesting proteins encoded by seven different genes in Arabidopsis. Phosphorylation of the PsbH protein at Thr-4 was completely abolished in the plants lacking STN8. Phosphorylation of Thr-4 in the wild type required both light and prior phosphorylation at Thr-2, indicating that STN8 is a light-activated kinase that phosphorylates Thr-4 only after another kinase phosphorylates Thr-2. Analysis of the STN8 catalytic domain suggests that selectivity of STN8 in phosphorylation of the very N-terminal residues in D1, D2, and CP43, and Thr-4 in PsbH pre-phosphorylated at Thr-2 may be explained by the long loops obstructing entrance into the kinase active site and seven additional basic residues in the vicinity of the catalytic site, as compared with the homologous STN7 kinase responsible for phosphorylation of light-harvesting proteins.Reversible protein phosphorylation is a key molecular mechanism regulating all aspects of physiology and development in eukaryotic cells. The genome sequencing of Arabidopsis thaliana has uncovered more than 1160 genes encoding for the protein kinases and phosphatases in this model plant (1), highlighting a new challenge in revealing of the substrates and functions for these catalysts of reversible protein phosphorylation. The task of identification of in vivo substrate specificities for individual protein kinases and phosphatases in Arabidopsis thaliana has recently became feasible because of two groundbreaking developments. First, the plant lines with knockouts of individual genes became public and commercially available (2). Second, new mass spectrometrybased analytical techniques permitted identification and mapping of in vivo phosphorylation sites in numerous proteins (as reviewed in Ref.3). For the first time these technical advancements provide the possibility of unraveling the complex protein phosphorylation network in plant photosynthetic membranes, which regulates the adaptation of the photosynthetic apparatus and efficient energy utilization in response to light quality and intensity, ambient temperature, circadian rhythm, nutrient deficiency, and other stresses (4 -6).The major proteins undergoing reversible phosphorylation in the photosynthetic thylakoid membranes belong to photosystem II (PSII) 3 and its light-harvesting antennae proteins LHCII (6 -11). Phosphorylation status of these proteins is differentially regulated by light (12), redox state of the membrane electron carriers (13-15), the ferredoxin-thioredoxi...

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mentioning

confidence: 99%

STN8 Protein Kinase in Arabidopsis thaliana Is Specific in Phosphorylation of Photosystem II Core Proteins

Vainonen¹,

Hansson

Vener

2005

Journal of Biological Chemistry

190

253

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“…Although in vitro (in isolated thylakoids) degradation of the damaged D1 protein and disassembly of the PSII complexes does occur in darkness [2,3], it is possible that in vivo degradation and disassembly are influenced by light through phosphorylation and dephosphorylation of the D1 protein [29]. We can therefore not exclude that the light dependence of D1 assembly, as observed in our experiments, resulted partially from a light control of degradation and disassembly of the PSII reaction center.…”

Section: Discussionmentioning

confidence: 70%

Light is required for efficient translation elongation and subsequent integration of the D1‐protein into Photosystem II

Wijk

Eichacker²

1996

FEBS Letters

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The light dependence of translation and successive assembly of the D1 reaction center protein into Photosystem II subcomplexes was followed in fully developed chloroplasts isolated from the dark phase of diurnally grown spinach. The incorporation of synthesized D1 protein into Photosystem II (PSII) was analyzed by fractionation of radiolabeled unassembled protein and PSII (sub)complexes on sucrose density gradients. The ribosomes with attached nascent chains were recovered as pellets in the same gradients, and nascent chains of the D1 protein were immunoprccipitated. The analysis showed that absence of light during translation leads to an increased accumulation of polysome-bound D1 translation intermediates, indicating that light is required for efficient elongation of the D1 protein. The accumulation of the D1 protein and CP43 decreased three-fold in darkness, whereas accumulation of the D2 reaction center protein was not affected by light. In addition, light was also required for efficient incorporation of the D1 protein into the PSII core complex. In darkness, the newly synthesized D1 protein accumulated predominantly as unassembled protein or in PSII subcomplexes smaller than 100 kDa.

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“…Phosphorylation of D1 has never been observed in C. reinhardtii (31) despite a conserved Thr residue present at its N terminus (18). For these reasons, P33-34 is likely to result from structural modifications of D1 other than phosphorylation that might protect it from proteolytic attack in the same manner as the N-terminal phosphorylation of D1 does in higher plants (32). The discrepancy between P33-34 turnover and steady state levels in some of the mutants suggests that different forms of P33-34 with different half-lives might coexist in the thylakoid membrane.…”

Section: Changes At Ala 251 That Impair D1 Synthesis and Accumulationmentioning

confidence: 99%

Site-directed Mutations at Residue 251 of the Photosystem II D1 Protein of Chlamydomonas That Result in a Nonphotosynthetic Phenotype and Impair D1 Synthesis and Accumulation

Lardans

Gillham

Boynton

1997

Journal of Biological Chemistry

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In Cyanobacteria and Chlamydomonas reinhardtii, substitution of valine for alanine at position 251 of the photosystem II D1 protein in the loop between transmembrane helices IV and V confers resistance to herbicides that reduce photosystem II function and increases sensitivity to photoinhibition. Using site-directed mutagenesis and chloroplast transformation in Chlamydomonas we have examined further the role of residue 251 in relation to D1 structure, function, and photosynthetic performance. Of the 12 different amino acid substitutions for Ala 251 introduced at this position, five (Arg, Asp, Gln, Glu, and His) resulted in a nonphotosynthetic phenotype. Transformants with the Arg 251 substitution synthesize a normal sized 32-kDa D1 protein with greatly reduced stability. The Gln, Glu, His, and Asp transformants make a 33-34-kDa form of the D1 protein of varying stability as well as an immunologically related polypeptide of 24 -25 kDa corresponding to the N-terminal portion of D1 that is unstable and appears to be an aborted D1 translation product. All mutant forms of the D1 protein are intrinsic to the thylakoids. In contrast to previous studies in Cyanobacteria showing that residues in the IV-V loop can be mutated or deleted without loss of photosynthetic competence, our results suggest that Ala 251 has a key role in the structure and function of the IV-V loop region.In all oxygen-evolving organisms, the reaction center of the photosystem II (PSII) 1 complex consists of the D1 protein, the structurally related D2 protein, cytochrome b 559 , and at least two small proteins of unknown function (1). The rapidly turning over D1 protein continuously undergoes a cycle of damage, degradation, and replacement in response to photodamage from normal PSII photochemistry (2). The D1 protein, encoded by the chloroplast psbA gene, is synthesized as a membrane associated 33.5-kDa precursor with a C-terminal extension. After processing to the 32-kDa mature form, D1 undergoes several posttranslational modifications postulated to facilitate translocation and proper assembly into PSII centers in the lipid bilayer (3), where it binds chlorophyll, pheophytin, quinone, carotenoid, iron, and manganese (4). D1 is thought to have five hydrophobic membrane-spanning helices, with its N terminus facing the chloroplast stroma and its C terminus projecting into the thylakoid lumen (5, 6). One stromally exposed region of D1, extending from the C terminus of helix IV through the N terminus of helix V (IV-V loop), participates in binding both Q B , the second stable quinone acceptor in PSII, and several classes of herbicides that inhibit photosynthetic electron transport (6). The IV-V loop region includes a stromal helix thought to lie parallel to the membrane surface (6) that divides this loop into two parts, one thought to be involved in D1 degradation in vivo and the other functioning in herbicide and quinone binding (7,8).Phylogenetic conservation of the IV-V loop among Cyanobacteria, algae, and higher plants (9) suggests that most of thes...

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Regulation of D1-protein degradation during photoinhibition of photosystem II in vivo: Phosphorylation of the D1 protein in various plant groups

Cited by 77 publications

References 45 publications

STN8 Protein Kinase in Arabidopsis thaliana Is Specific in Phosphorylation of Photosystem II Core Proteins

STN8 Protein Kinase in Arabidopsis thaliana Is Specific in Phosphorylation of Photosystem II Core Proteins

Light is required for efficient translation elongation and subsequent integration of the D1‐protein into Photosystem II

Site-directed Mutations at Residue 251 of the Photosystem II D1 Protein of Chlamydomonas That Result in a Nonphotosynthetic Phenotype and Impair D1 Synthesis and Accumulation

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