Photoinhibition and Recovery in Oxygenic Photosynthesis: Mechanism of a Photosystem II Damage and Repair Cycle

Yokthongwattana, Kittisak; Melis, Anastasios

doi:10.1007/1-4020-3579-9_12

Cited by 42 publications

(48 citation statements)

References 144 publications

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“…Phosphorylated polypeptides associated with the PSII core reaction center complex that undergo phosphorylation include the D1/D2 reaction center polypeptides as well as a 43-kD Chl a-binding protein (CP43; Hansson and Vener, 2003;Turkina et al, 2006;Vener, 2006Vener, , 2007Yokthongwattana and Melis, 2006;Edelman and Mattoo, 2008). The phosphorylation of D1/D2 and CP43 is associated with the disassembly, degradation, and resynthesis of the D1 protein during the PSII repair cycle in response to PSII chronic photoinhibition (Yokthongwattana and Melis, 2006;Edelman and Mattoo, 2008;Tikkanen et al, 2008;Fristedt et al, . Table II.…”

Section: Discussionmentioning

confidence: 99%

The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b₆/f Supercomplex

et al. 2015

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Chlamydomonas sp. UWO 241 (UWO 241) is a psychrophilic green alga isolated from Antarctica. A unique characteristic of this algal strain is its inability to undergo state transitions coupled with the absence of photosystem II (PSII) light-harvesting complex protein phosphorylation. We show that UWO 241 preferentially phosphorylates specific polypeptides associated with an approximately 1,000-kD pigment-protein supercomplex that contains components of both photosystem I (PSI) and the cytochrome b 6 /f (Cyt b 6 /f) complex. Liquid chromatography nano-tandem mass spectrometry was used to identify three major phosphorylated proteins associated with this PSI-Cyt b 6 /f supercomplex, two 17-kD PSII subunit P-like proteins and a 70-kD ATP-dependent zinc metalloprotease, FtsH. The PSII subunit P-like protein sequence exhibited 70.6% similarity to the authentic PSII subunit P protein associated with the oxygen-evolving complex of PSII in Chlamydomonas reinhardtii. Tyrosine-146 was identified as a unique phosphorylation site on the UWO 241 PSII subunit P-like polypeptide. Assessment of PSI cyclic electron transport by in vivo P700 photooxidation and the dark relaxation kinetics of P700 + indicated that UWO 241 exhibited PSI cyclic electron transport rates that were 3 times faster and more sensitive to antimycin A than the mesophile control, Chlamydomonas raudensis SAG 49.72. The stability of the PSI-Cyt b 6 /f supercomplex was dependent upon the phosphorylation status of the PsbP-like protein and the zinc metalloprotease FtsH as well as the presence of high salt. We suggest that adaptation of UWO 241 to its unique low-temperature and high-salt environment favors the phosphorylation of a PSI-Cyt b 6 /f supercomplex to regulate PSI cyclic electron transport rather than the regulation of state transitions through the phosphorylation of PSII light-harvesting complex proteins.

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Section: Discussionmentioning

confidence: 99%

The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b₆/f Supercomplex

et al. 2015

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“…The lightinduced damage to PSII, in particular to the D1 reaction center protein, requires PSII repair to sustain its photosynthetic function (Takahashi and Murata, 2008). Impairment and degradation of D1 increase with rising light intensities, and this protein has the fastest turnover rate among the photosynthetic proteins of plants, algae, and cyanobacteria (Yokthongwattana and Melis, 2006). However, in plants, the PSII is segregated in highly stacked membrane layers of very large thylakoid membranes (Andersson and Anderson, 1980;Kirchhoff et al, 2008), which are densely folded to fit inside chloroplasts (Mullineaux, 2005;Shimoni et al, 2005).…”

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Phosphorylation of Photosystem II Controls Functional Macroscopic Folding of Photosynthetic Membranes inArabidopsis

et al. 2009

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Photosynthetic thylakoid membranes in plants contain highly folded membrane layers enriched in photosystem II, which uses light energy to oxidize water and produce oxygen. The sunlight also causes quantitative phosphorylation of major photosystem II proteins. Analysis of the Arabidopsis thaliana stn7xstn8 double mutant deficient in thylakoid protein kinases STN7 and STN8 revealed light-independent phosphorylation of PsbH protein and greatly reduced N-terminal phosphorylation of D2 protein. The stn7xstn8 and stn8 mutants deficient in light-induced phosphorylation of photosystem II had increased thylakoid membrane folding compared with wild-type and stn7 plants. Significant enhancement in the size of stacked thylakoid membranes in stn7xstn8 and stn8 accelerated gravity-driven sedimentation of isolated thylakoids and was observed directly in plant leaves by transmission electron microscopy. Increased membrane folding, caused by the loss of light-induced protein phosphorylation, obstructed lateral migration of the photosystem II reaction center protein D1 and of processing protease FtsH between the stacked and unstacked membrane domains, suppressing turnover of damaged D1 in the leaves exposed to high light. These findings show that the high level of photosystem II phosphorylation in plants is required for adjustment of macroscopic folding of large photosynthetic membranes modulating lateral mobility of membrane proteins and sustained photosynthetic activity.The use of captured sunlight energy to split water and drive oxygenic photosynthesis by photosystem II (PSII) (Barber, 2006) inevitably generates reactive oxygen species and causes oxidative damage to the PSII protein pigment complex. The lightinduced damage to PSII, in particular to the D1 reaction center protein, requires PSII repair to sustain its photosynthetic function (Takahashi and Murata, 2008). Impairment and degradation of D1 increase with rising light intensities, and this protein has the fastest turnover rate among the photosynthetic proteins of plants, algae, and cyanobacteria (Yokthongwattana and Melis, 2006). However, in plants, the PSII is segregated in highly stacked membrane layers of very large thylakoid membranes (Andersson and Anderson, 1980;Kirchhoff et al., 2008), which are densely folded to fit inside chloroplasts (Mullineaux, 2005;Shimoni et al., 2005). As a consequence, the PSII repair cycle in plants is slower than in cyanobacteria (Yokthongwattana and Melis, 2006), and it includes migration of the PSII complex from the stacked membrane domains (grana) to the unstacked membranes (stroma lamellae), where proteolysis and insertion of a newly synthesized D1 protein occurs (Baena-Gonzalez and Aro, 2002;Yokthongwattana and Melis, 2006). High light also causes quantitative phosphorylation of the membrane surface-exposed regions of D1, D2, CP43, and PsbH proteins of PSII in plants (Rintamä ki et al., 1997;Vener et al., 2001), but the function of this phosphorylation is largely unknown and reports on its importance for the D1 protein turnover ...

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“…Despite these advances, the assembly and stabilization of the D1 protein in PSII and its regulation mechanism remain poorly understood (Aro et al, 1993;Yokthongwattana and Melis, 2006). Screening mutants with altered chlorophyll fluorescence has proved to be a specific and efficient way to dissect the molecular mechanisms underlying the biogenesis of photosystems (Peng et al, 2006), since alterations in chlorophyll fluorescence indicate defects in the photosynthetic electron transport chain, which may result from changes in the structure or function of the thylakoid membrane (Miles, 1994).…”

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HCF243 Encodes a Chloroplast-Localized Protein Involved in the D1 Protein Stability of the Arabidopsis Photosystem II Complex

et al. 2011

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Numerous auxiliary nuclear factors have been identified to be involved in the dynamics of the photosystem II (PSII) complex. In this study, we characterized the high chlorophyll fluorescence243 (hcf243) mutant of Arabidopsis (Arabidopsis thaliana), which shows higher chlorophyll fluorescence and is severely deficient in the accumulation of PSII supercomplexes compared with the wild type. The amount of core subunits was greatly decreased, while the outer antenna subunits and other subunits were hardly affected in hcf243. In vivo protein-labeling experiments indicated that the synthesis rate of both D1 and D2 proteins decreased severely in hcf243, whereas no change was found in the rate of other plastid-encoded proteins. Furthermore, the degradation rate of the PSII core subunit D1 protein is higher in hcf243 than in the wild type, and the assembly of PSII is retarded significantly in the hcf243 mutant. HCF243, a nuclear gene, encodes a chloroplast protein that interacts with the D1 protein. HCF243 homologs were identified in angiosperms with one or two copies but were not found in lower plants and prokaryotes. These results suggest that HCF243, which arose after the origin of the higher plants, may act as a cofactor to maintain the stability of D1 protein and to promote the subsequent assembly of the PSII complex.PSII is a multisubunit protein-pigment complex embedded in the thylakoid membrane that harnesses light energy to split water into oxygen, protons, and electrons. It comprises more than 20 different subunits, most of which are integral membrane proteins and bind numerous cofactors (Wollman et al., 1999;Iwata and Barber, 2004;Nelson and Yocum, 2006). The PSII reaction center complex is composed of the D1 and D2 proteins, the a-and b-subunits of cytochrome b 559 , and the PsbI protein. The D1 and D2 heterodimers bind all the essential redox components of PSII required for primary charge separation and subsequent electron transfer (Nanba and Satoh, 1987). In addition, PSII core complexes also contain the intrinsic chlorophyll a-binding proteins (CP43 and CP47), the extrinsic oxygen-evolving complex (33-, 23-, and 17-kD proteins), and the other low-molecular-mass proteins (Bricker and Ghanotakis, 1996). The functional form of PSII in the thylakoid membrane consists of the PSII core and the associated light-harvesting complex (Nelson and Yocum, 2006).Despite considerable advances in the elucidation of the structure and function of PSII, knowledge of the assembly of this multiprotein complex is only in its infancy. A number of studies have proved that this assembly is likely to involve multistep processes (Rokka et al., 2005). The first step is formation of the PSII reaction center, in which the D1 protein is incorporated into a precomplex, probably consisting of the D2, cytochrome b 559 , and PsbI proteins (Adir et al., 1990;van Wijk et al., 1997;Mü ller and Eichacker, 1999;Zhang et al., 1999). Subsequently, CP47 and CP43, core antenna subunits that bind chlorophyll a, are recruited to form the PSII core compl...

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Photoinhibition and Recovery in Oxygenic Photosynthesis: Mechanism of a Photosystem II Damage and Repair Cycle

Cited by 42 publications

References 144 publications

The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b₆/f Supercomplex

The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b₆/f Supercomplex

Phosphorylation of Photosystem II Controls Functional Macroscopic Folding of Photosynthetic Membranes inArabidopsis

HCF243 Encodes a Chloroplast-Localized Protein Involved in the D1 Protein Stability of the Arabidopsis Photosystem II Complex

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Photoinhibition and Recovery in Oxygenic Photosynthesis: Mechanism of a Photosystem II Damage and Repair Cycle

Cited by 42 publications

References 144 publications

The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b6/f Supercomplex

The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b6/f Supercomplex

Phosphorylation of Photosystem II Controls Functional Macroscopic Folding of Photosynthetic Membranes inArabidopsis

HCF243 Encodes a Chloroplast-Localized Protein Involved in the D1 Protein Stability of the Arabidopsis Photosystem II Complex

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The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b₆/f Supercomplex

The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b₆/f Supercomplex