Protein kinases and phosphatases involved in the acclimation of the photosynthetic apparatus to a changing light environment (original) (raw)
Related papers
Thylakoid Protein Phosphorylation in Chloroplasts
Plant and Cell Physiology, 2021
Because of their abundance and extensive phosphorylation, numerous thylakoid proteins stand out amongst the phosphoproteins of plants and algae. In particular, subunits of light-harvesting complex II (LHCII) and of photosystem II (PSII) are dynamically phosphorylated and dephosphorylated in response to light conditions and metabolic demands. These phosphorylations are controlled by evolutionarily conserved thylakoid protein kinases and counteracting protein phosphatases, which have distinct but partially overlapping substrate specificities. The best characterized are the kinases STATE TRANSITION 7 (STN7/STT7) and STATE TRANSITION 8 (STN8), and the antagonistic phosphatases PROTEIN PHOSPHATASE 1/THYLAKOID-ASSOCIATED PHOSPHATASE 38 (PPH1/TAP38) and PHOTOSYSTEM II CORE PHOSPHATASE (PBCP). The phosphorylation of LHCII is mainly governed by STN7 and PPH1/TAP38 in plants. LHCII phosphorylation is essential for state transitions, a regulatory feedback mechanism that controls the allocation...
Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1994
Regulation of thylakoid protein phosphorylation from saturating up to photoinhibitory light conditions was studied in intact chloroplasts with high rates of CO2 fixation and functioning protein biosynthesis. Comparing steady-state level phosphorylation with the phosphorylation in the presence of the phosphatase inhibitor NaF, evidence was found that phosphorylation of light harvesting chlorophyll-protein complex II (LHC II) and Photosystem II (PS II) polypeptides was catalysed by at least two different kinase/phosphatase systems. Whereas the steady-state level of LHC II phosphorylation declined with increasing light intensity, the phosphorylation level of PS II polypeptides remained stable even at photoinhibitory conditions. Decrease of steady-state level of LHC II phosphorylation at higher light intensities was partially due to an inhibition of the phosphorylation reaction. Its inactivation was observed before any significant loss of PS II electron transfer activity occurred. Quenching analysis of chlorophyll fluorescence revealed that the high light inhibition of the LHC II phosphorylation reaction was caused by an increased membrane energetisation, and not by an oxidation of the plastoquinone pool. In contrast, the kinase activity responsible for the phosphorylation of the PS II polypeptides seemed to be exclusively under the redox control of the plastoquinone pool and was not influenced by membrane energetisation. Evidence was found that also the phosphatase activities specific for LHC II and PS II proteins were different. As indicated by the high turnover of phosphate groups bound to LHC II, the LHC II specific phosphatase showed a high activity. Its activity was stimulated at higher light intensities and determined to a main extent the steady state level of LHC II phosphorylation. The phosphatase specific for the PS II phosphoproteins showed almost no activity in the light as indicated by the absence of a phosphate group turnover in the light. Dephosphorylation of PS II could only be observed in the dark and in contrast to LHC II dephosphorylation could not be inhibited by NaF. Even the increased turnover of the D1 protein at higher light intensities, which was followed by the light-dependent incorporation of [14C]leucine into the protein, did not accelerate the D1 protein phosphorylation. The steady-state level of PS II protein phosphorylation was therefore in principle determined by its kinase activity.
Nature, 2005
Illumination changes elicit modifications of thylakoid proteins and reorganization of the photosynthetic machinery. This involves, in the short term, phosphorylation of photosystem II (PSII) and light-harvesting (LHCII) proteins. PSII phosphorylation is thought to be relevant for PSII turnover 1,2 , whereas LHCII phosphorylation is associated with the relocation of LHCII and the redistribution of excitation energy (state transitions) between photosystems 3,4 . In the long term, imbalances in energy distribution between photosystems are counteracted by adjusting photosystem stoichiometry 5,6 . In the green alga Chlamydomonas and the plant Arabidopsis, state transitions require the orthologous protein kinases STT7 and STN7, respectively 7,8 . Here we show that in Arabidopsis a second protein kinase, STN8, is required for the quantitative phosphorylation of PSII core proteins. However, PSII activity under high-intensity light is affected only slightly in stn8 mutants, and D1 turnover is indistinguishable from the wild type, implying that reversible protein phosphorylation is not essential for PSII repair. Acclimation to changes in light quality is defective in stn7 but not in stn8 mutants, indicating that short-term and long-term photosynthetic adaptations are coupled. Therefore the phosphorylation of LHCII, or of an unknown substrate of STN7, is also crucial for the control of photosynthetic gene expression.
Photosynthesis research, 2002
Chloroplast thylakoid protein phosphorylation was discovered, and the most conspicuous phosphoproteins identified, by John Bennett at Warwick University. His initial findings were published in 1977. The phosphoproteins included apoproteins of chloroplast light harvesting complex II. Thylakoid protein phosphorylation was shown to influence distribution of excitation energy between Photosystems I and II in 1979, during a visit by Bennett to the laboratory of Charles J. Arntzen at the University of Illinois at Urbana-Champaign. That work was published by Bennett, Katherine E. Steinback and Arntzen in 1980. Control of both protein phosphorylation and excitation energy distribution by the redox state of the plastoquinone pool was first established in 1980 during the author's visit to Arntzen's laboratory. The experiments were prompted by the realization that coupling between redox state of an inter-photosystem electron carrier and excitation energy distribution provides a concret...
Frontiers in Plant Science, 2019
Phosphorylation of the light-harvesting complex II (LHCII) is a central trigger for the reorganization of the photosynthetic complexes in the thylakoid membrane during short-term light acclimation. The major kinase involved in LHCII phosphorylation is STATE TRANSITION 7 (STN7), and its activity is mostly counteracted by a thylakoidassociated phosphatase, PROTEIN PHOSPHATASE 1/THYLAKOID ASSOCIATED PHOSPHATASE 38 (PPH1/TAP38). This kinase/phosphatase pair responds to the redox status of the photosynthetic electron transport chain. In Arabidopsis thaliana, Lhcb1 and Lhcb2 subunits of the LHCII trimers are the major targets of phosphorylation and have different roles in the acclimation of the photosynthetic machinery. Another antagonistic kinase and phosphatase pair, STATE TRANSITION 8 (STN8) and PHOTOSYSTEM II PHOSPHATASE (PBCP) target a different set of thylakoid proteins. Here, we analyzed double, triple, and quadruple knockout mutants of these kinases and phosphatases. In multiple mutants, lacking STN7, in combination with one or both phosphatases, but not STN8, the phosphorylation of LHCII was partially restored. The recovered phosphorylation favors Lhcb1 over Lhcb2 and results in a better adaptation of the photosynthetic apparatus and increased plant growth under fluctuating light. This set of mutants allowed to unveil a contribution of STN8-dependent phosphorylation in the acclimation to rapid light variations.
Planta, 2008
Reduction of the plastoquinone (PQ) pool is known to activate phosphorylation of thylakoid proteins. In the Arabidopsis thaliana mutants psad1-1 and psae1-3, oxidation of photosystem I (PSI) is impaired, and the PQ pool is correspondingly over-reduced. We show here that, under these conditions, the antenna protein Lhca4 of PSI becomes a target for phosphorylation. Phosphorylation of the mature Lhca4 protein at Thr16 is suppressed in stn7 psad1 and stn7 psae1 double mutants. Thus, under extreme redox conditions, hyperactivation of thylakoid protein kinases and/or reorganization of thylakoid protein complex distribution increase the susceptibility of PSI to phosphorylation.
Plant, Cell & Environment, 2012
State transitions and photosystem stoichiometry adjustment are two oxidation–reduction (redox)-regulated acclimatory responses in photosynthesis. State transitions are short-term adaptations that, in chloroplasts, involve reversible post-translational modification by phosphorylation of light-harvesting complex II (LHC II). Photosystem stoichiometry adjustments are long-term responses involving transcriptional regulation of reaction centre genes. Both responses are initiated by changes in light quality and are regulated by the redox state of plastoquinone (PQ). The LHC II kinase involved in the state 2 transition is a serine/threonine kinase known as STT7 in Chlamydomonas, and as STN7 in Arabidopsis. The phospho-LHC II phosphatase that produces the state 1 transition is a PP2C-type protein phosphatase currently termed both TAP38 and PPH1. In plants and algae, photosystem stoichiometry adjustment is governed by a modified two-component sensor kinase of cyanobacterial origin – chloroplast sensor kinase (CSK). CSK is a sensor of the PQ redox state. Chloroplast sigma factor 1 (SIG1) and plastid transcription kinase (PTK) are the functional partners of CSK in chloroplast gene regulation. We suggest a signalling pathway for photosystem stoichiometry adjustment. The signalling pathways of state transitions and photosystem stoichiometry adjustments are proposed to be distinct, with the two pathways sensing PQ redox state independently of each other.
Journal of Biological Chemistry, 2001
Photosynthetic organisms acclimate to long term changes in the environmental light quality by an adjustment of their photosystem stoichiometry to maintain photosynthetic efficiency. By using light sources that predominantly excite either photosystem I (PSI) or photosystem II (PSII), we studied the effects of excitation imbalances between both photosystems on nuclear PSI gene transcription in transgenic tobacco seedlings with promoter::-glucuronidase gene fusions. Shifts from PSI to PSII light sources (and vice versa) induced changes in the reduction/oxidation state of intersystem redox components, and acclimation of tobacco seedlings to such changes were monitored by changes in chlorophyll a/b ratios and in vivo chlorophyll a fluorescence. The ferredoxin-NADP ؉oxidoreductase gene promoter did not respond to these treatments, those from the genes for subunits PsaD and PsaF of PSI are activated by a reduction signal, and the plastocyanin promoter responded to both reduction and oxidation signals. Additional experiments with photosynthetic electron transport inhibitors 3-(3,4-dichlorophenyl)-1,1-dimethyl urea and 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone demonstrated that the redox state of the plastoquinone pool controls the activity of the plastocyanin promoter, whereas subunit PsaD and PsaF gene transcription is regulated by other photosynthesis-derived signals. Thus, the expression of nuclear-encoded PSI genes is controlled by diverse light quality-dependent redox signals from the plastids during photosystem stoichiometry adjustment.
Analysis of the Chloroplast Protein Kinase Stt7 during State Transitions
PLoS Biology, 2009
State transitions allow for the balancing of the light excitation energy between photosystem I and photosystem II and for optimal photosynthetic activity when photosynthetic organisms are subjected to changing light conditions. This process is regulated by the redox state of the plastoquinone pool through the Stt7/STN7 protein kinase required for phosphorylation of the light-harvesting complex LHCII and for the reversible displacement of the mobile LHCII between the photosystems. We show that Stt7 is associated with photosynthetic complexes including LHCII, photosystem I, and the cytochrome b 6 f complex. Our data reveal that Stt7 acts in catalytic amounts. We also provide evidence that Stt7 contains a transmembrane region that separates its catalytic kinase domain on the stromal side from its N-terminal end in the thylakoid lumen with two conserved Cys that are critical for its activity and state transitions. On the basis of these data, we propose that the activity of Stt7 is regulated through its transmembrane domain and that a disulfide bond between the two lumen Cys is essential for its activity. The high-light-induced reduction of this bond may occur through a transthylakoid thiol-reducing pathway driven by the ferredoxinthioredoxin system which is also required for cytochrome b 6 f assembly and heme biogenesis. Citation: Lemeille S, Willig A, Depège-Fargeix N, Delessert C, Bassi R, et al. (2009) Analysis of the chloroplast protein kinase Stt7 during state transitions. PLoS Biol 7(3): e1000045.