Summary
This Chapter provides highlights on the mechanism of a photosystem II (PS II) damage and repair cycle in chloroplasts. Photo-oxidative damage to the PS II reaction center is a phenomenon that occurs in every organism of oxygenic photosynthesis. Through the process of evolution, an elaborate repair mechanism was devised, one that rectifies this presumably unavoidable and irreversible photoinhibition and restores the PS II charge separation activity. The repair process entails several enzymatic reactions for the selective removal and replacement of the inactivated D1/32 kD reaction center protein (the chloroplast-encoded psbAgene product) from the massive (>1,000 kD) H2O-oxidizing and O2-evolving PS II holocomplex. This repair process is unique in the annals of biology; nothing analogous in complexity and specificity has been reported in other biological systems. Elucidation of the repair mechanism may reveal the occurrence of hitherto unknown regulatory and catalytic reactions for the selective in situ replacement of specific proteins from within multi-protein complexes. This may not only have significant applications in photosynthesis and agriculture but also in medicine and other fields.
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References
Adam Z and Clarke AK (2002) Cutting edge of chloroplast proteolysis. Trends Plant Sci 7: 451–456
Adams WW III, Demmig-Adams B, Rosenstiel TN, Brightwell AK and Ebbert V (2002) Photosynthesis and photoprotection in overwintering plants. Plant Biology 4: 545–557
Adams WW III, Zarter CR, Ebbert V and Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens. BioScience 54: 41–49
Adamska I, Ohad I and Kloppstech K (1992) Synthesis of the early light-inducible protein is controlled by blue light and related to light stress. Proc Natl Acad Sci USA 89: 2610–2613
AdirN, Shochat S and Ohad I (1990) Light-dependent D1 protein synthesis and translocation is regulated by reaction center II: Reaction center II serves as an acceptor for the D1 precursor. J Biol Chem 265: 12563–12568
Allen JF (2003) State transitions—a question of balance. Science 299: 1530–1532
Allen JF and Nilsson A (1997) Redox signaling and the structural basis of regulation of photosynthesis by protein phosphorylation. Physiol Plant 100: 863–868
Anderson JM and Melis A (1983) Localization of different photosystems in separate regions of chloroplast membranes. Proc Natl Acad Sci USA 80: 745–749
Andreasson E and Melis A (1995) Localization and characterization of a novel 20 kDa polypeptide in the chloroplast of the green alga Dunaliella salina. Plant Cell Physiol 136: 1483– 1492
Aro E-M, Kettunen R and Tyystjärvi E (1992) ATP and light regulate D1 protein modification and degradation: role of D1 in photoinhibition. FEBS Lett 297: 29–33
Aro E-M, Virgin I and Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134
Baena-González E and Aro E-M (2002) Biogenesis, assembly and turnover of photosystem II units. Philos T Roy Soc B 357: 1451–1460
Banet G, Pick U and Zamir A (2000) Light-harvesting complex II pigments and proteins in association with Cbr, a homolog of higher-plant early light-inducible proteins in the unicellular green alga Dunaliella. Planta 210: 947–955
Barbato R, Friso G, Rigoni F, Frizzo A and Giacometti GM (1992) Characterization of a 41 kDa photoinhibition adduct in isolated photosystem II reaction centres. FEBS Lett 309: 165–169
Barber J (1989) Function and molecular biology of PS II. Oxford Surveys Plant Cell Biol 6: 115–162
Barber J (1994) Molecular basis of the vulnerability of PS II to damage by light. Aust J Plant Physiol 22: 201–208
Barber J, Chapman DJ and Telfer A (1987) Characterisation of a photosystem two reaction center isolated from Pisum sativum. FEBS Lett 220: 67–74
Barber J, Morris E and Buchel C (2000) Revealing the structure of the photosystem II chlorophyll binding proteins, CP43 and CP47. Biochim Biophys Acta 1459: 239–247
Baroli I and Melis A (1996) Photoinhibition and repair in Dunaliella salina acclimated to different growth irradiances. Planta 198: 640–646
Baroli I and Melis A (1998) Photoinhibitory damage is modulated by the rate of photosynthesis and by the photosystem II light-harvesting chlorophyll antenna size. Planta 205: 288– 296
Baroli I and Niyogi KK (2000) Molecular genetics of xanthophyll-dependent photoprotection in green algae and plants. Philos T Roy Soc B 355: 1385–1394
Baroli I, Do AD, Yamane T and Niyogi KK (2003) Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress. Plant Cell 15: 992–1008
Bassi R, Rigoni F and Giacometti GM (1990) Chlorophyll binding proteins with antenna function in higher plants and green algae. Photochem Photobiol 52: 1187–1206
Bennett J (1979) The protein kinase of the thylakoid membrane is light-dependent. FEBS Lett 103: 342–344
Bennett J (1991) Protein phosphorylation in green plant chloroplasts. Annu Rev Plant Physiol Plant Mol Biol 42: 281– 311
Black MT, Brearley TH and Horton P (1986) Heterogeneity in chloroplast PS II. Photosynth Res 8: 193–207
Booij-James IS, Swegle WM, Edelman M and Mattoo AK (2002) Phosphorylation of the D1 photosystem II reaction center protein is controlled by an endogenous circadian rhythm. Plant Physiol 130: 2069–2075
BottomleyW, SpencerDand Whitfeld PR (1974) Protein synthesis in isolated spinach chloroplasts: comparison of light-driven and ATP-driven synthesis. Arch Biochem Biophys 164: 106– 117
Bricker TM (1990) The structure and function of CPa-1 and CPa-2 in photosystem-II. Photosynth Res 24: 1–13
Callahan FE, Wergin WP, Nelson N, Edelman M and Mattoo AK (1989) Distribution of thylakoid proteins between stromal and granal lamellae in Spirodela. Plant Physiol 91: 629–635
Callahan FE, Ghirardi ML, Sopory SK, Mehta AM, Edelman M and Mattoo AK (1990) A novel metabolic formof the 32 kDa- D1 protein in the grana-localized reaction center of PS II. J Biol Chem 265: 15357–15360
Cao H, Zhang L and Melis A (2001) Bioenergetic and metabolic processes for the survival of sulfur-deprived Dunaliella salina (Chlorophyta). J Appl Phycol 13: 25–34
Chen H-C and Melis A (2002) Complete genomic DNA (bases 1 through 3873) and protein sequence (amino acids 1 through 411) for a putative chloroplast-envelope localized sulfate permease (CrcpSulP) in the unicellular green alga Chlamydomonas reinhardtii. GenBank Accession Number AF467891
Chen H-C, Yolthongwattana K and Melis A (2002) Chlamydomonas reinhardtii chloroplast sulfate transport system permease (SulP) mRNA, complete cds; nuclear gene for chloroplast product. GenBank Accession Number AF481828
Chen H-C, Yokthongwattana K, Newton AJ and Melis A (2003) SulP, a nuclear gene encoding a putative chloroplast-targeted sulfate permease in Chlamydomonas reinhardtii. Planta 218: 98–106
Chylla RA and Whitmarsh J (1989) Inactive photosystem-II complexes in leaves—turnover rate and quantitation. Plant Physiol 90: 765–772
Cinco RM, Rompel A, Visser H, Aromi G, Klein M and Sauer K (1999) Comparison of the manganese cluster in oxygenevolving photosystem II with distorted cubane manganese compounds through X-ray absorption spectroscopy. Inorg Chem 38: 5988–5998
Cleland RE and Melis A (1987) Probing the events of photoinhibition by altering electron-transport activity and lightharvesting capacity in chloroplast thylakoids. Plant Cell Environ 10: 747–752
Cleland RE, MelisAand Neale PJ (1986) Mechanism of photoinhibition: photochemical reaction center inactivation in system II of chloroplasts. Photosynth Res 9: 79–88
Cramer WA and Whitmarsh J (1977) Photosynthetic cytochromes. Annu Rev Plant Physiol 28: 133–172
Cramer WA, Theg SM and Widger WR (1986) On the structure and function of cytochrome b-559. Photosynth Res 10: 393– 403
Crofts AR and Wraight CA (1983) The electrochemical domain of photosynthesis. Biochim Biophys Acta 726: 149–185
Davies JP, Yildiz F and Grossman AR (1994) Mutants of Chlamydomonas with aberrant responses to sulfur deprivation. Plant Cell 6: 53–63
Davies JP, Yildiz F and Grossman AR (1996) Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J 15: 2150– 2159
Deisenhofer J and Michel H (1989) The photosynthetic reaction center from the purple bacterium Rhodopseudomonas viridis. EMBO J 8: 2149–2170
Demeter S, Neale PJ and Melis A (1987) Photoinhibition: impairment of the primary charge separation between P680 and pheophytin in photosystem II of chloroplasts. FEBS Lett 214: 370–374
Demmig B and Björkman O (1987) Comparison of the effect of excessive light on chlorophyll fluorescence (77K) and photon yield of O2 evolution in leaves of higher plants. Planta 171: 171–184
Demmig-Adams B, Moeller DL, Logan BA and AdamsWWIII (1998) Positive correlation between levels of retained zeaxanthin + antheraxanthin and degree of photoinhibition in shade leaves of Schefflera arboricola (Hayata) Merrill. Planta 205: 367–374
Depka B, Jahns P and Trebst A (1998) β-carotene to zeaxathin conversion in the rapid turnover of the D1 protein of photosytem II. FEBS Lett 424: 267–270
Drzymalla C, Schroda M and Beck CF (1996) Light-inducible gene hsp70B encodes a chloroplast-localized heat shock protein in Chlamydomonas reinhardtii. Plant Mol Biol 31: 1185– 1194
Duysens LN, Amesz J and Kamp BM (1961) Two photochemical systems in photosynthesis. Nature 190: 510–511
Eaglesham ARJ and Ellis RJ (1974) Protein synthesis in chloroplasts: II. Light-driven synthesis of membrane protein by isolated pea chloroplasts. Biochim Biophys Acta 335: 396– 407
Ebbert V and Godde D (1996) Phosphorylation of PS II polypeptides inhibits D1 protein-degradation and increases PS II stability. Photosynth Res 50: 257–269
Edelman M and Reisfeld A (1978) Characterization, translation and control of the 32,000 dalton chloroplast membrane protein in Spirodela. In: Akoyunoglou and Argyroudi-Akoyunoglou (eds) Chloroplast Development, pp 642–652. Elsevier/North Holland Biomedical Press, New York
Elich TD, Edelman M and Mattoo AK (1992) Identification, characterization, and resolution of the in vivo phosphorylated form of the D1 photosystem II reaction center protein. J Biol Chem 267: 3523–3529
Farchaus J and Dilley RA (1986) Purification and partial sequence of the Mr 10,000 phosphoprotein from spinach thylakoids. Arch Biochem Biophys 244: 94–101
Frank HA, Bautista JA, Josue JS and Young AJ (2000) Mechanism of non-photochemical quenching in green plants: energies of the lowest excited singlet states of violaxanthin and zeaxanthin. Biochemistry 39: 2831–2837
Ferreira KN, Tina M, Iverson TM, Maghlaoui K, Barber J and Iwata S (2004) Architecture of the photosynthetic oxygenevolving center. Science 303: 1831–1838
Ghanotakis DF and Yocum CF (1990) Photosystem-II and the oxygen-evolving complex. Annu Rev Plant Physiol Plant Mol Biol 41: 255–276
Glick RE and Melis A (1988) Minimum photosynthetic unit size in system I and system II of barley chloroplasts. Biochim Biophys Acta 934: 151–155
Gong H, Nilsen S and Allen JF (1993) Photoinhibition of photosynthesis. In-vivo involvement of multiple sites in a photodamage process under carbon dioxide and oxygen-free conditions. Biochim Biophys Acta 1142: 115–122
Graan T and Ort DR (1986) Detection of oxygen-evolving photosystem-II centers inactive in plastoquinone reduction. Biochim Biophys Acta 852: 320–330
Green BR (1988) The chlorophyll-protein complexes of higher plant photosynthetic membranes or just what green band is that? Photosynth Res 15: 3–32
Green BR and Camm EL (1981) A model of the relationship of the chlorophyll-protein complexes associated with photosystem-II. In: Akoyunoglou G (ed) Photosynthesis, Proceedings of 5th International Congress, Vol III, pp 675–681. Balaban International Science Services, Philadelphia
Green BR and Kühlbrandt W (1995) Sequence conservation of light-harvesting and stress-response proteins in relation to the three-dimensional molecular structure of LHCII. Photosynth Res 44: 139–148
Greenberg BM, Gaba V, Mattoo AK and Edelman M (1987) Identification of a primary in vivo degradation product of the rapidly-turning-over 32 kD protein of photosystem II. EMBO J 6: 2865–2869
Greer DM, Berry JA and Björkman O (1986) Photoinhibition of photosynthesis in intact bean leaves: role of light and temperature, and requirement for chloroplast-encoded protein synthesis during recovery. Planta 168: 253–260
Guenther JE and Melis A (1990) The physiological significance of photosystem II heterogeneity in chloroplasts. Photosynth Res 23: 105–110
Guenther JE, Nemson JA and Melis A (1990) Development of PS II in dark grown Chlamydomonas reinhardtii. A lightdependent conversion of PS IIβ, QB-nonreducing centers to the PS IIα, QB-reducing form. Photosynth Res 24: 35– 46
Gumpel NJ and Purton S (1994) Playing tag with Chlamydomonas. Trends Cell Biol 4: 299–301
Hallick RB (1989) Proposals for the naming of chloroplast genes. II. Update to the nomenclature of genes for thylakoid membrane polypeptides. Plant Mol Biol Rep 7: 266–275
Hankamer B, Barber J and Boekema EJ (1997) Structure and membrane organization of photosystem II in green plants. Annu Rev Plant Physiol Plant Mol Biol 48: 641– 671
Hauβühl K, Andersson B and Adamska I (2001) A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. EMBO J 20: 713–722
Hell R (1997) Molecular physiology of plant sulfur metabolism. Planta 202: 138–148
HillRand Bendall F (1960) Function of the two cytochrome components in chloroplasts: a working hypothesis. Nature 186: 136–137
Huner NPA, Maxwell DP, Gray GR and Savitch LV (1996) Sensing environmental temperature change through imbalances between energy supply and energy consumption—redox state of photosystem II. Physiol Plant 98: 358–364
Hurry VM, Anderson JM, Badger MR and Price GD (1996) Reduced levels of cytochrome b - f in transgenic tobacco increases the excitation pressure on photosystem II without increasing sensitivity to photoinhibition in vivo. Photosynth Res 50: 159–169
Ishikawa Y, Nakatani E, Henmi T, Ferjani A, Harada Y, Tamura N and Yamamoto Y (1999) Turnover of the aggregates and cross-linked products of the D1 protein generated by acceptorside photoinhibition of photosystem II. Biochim Biophys Acta 1413: 147–158
Jahns P and Miehe B (1996) Kinetic correlation of recovery from photoinhibition and zeaxanthin epoxidation. Planta 198: 202– 210
Jahns P, Depka B and Trebst A (2000) Xanthopyll cycle mutants from Chlamydomonas reinhardtii indicate a role for zeaxanthin in the D1 protein turn over. Plant Physiol Biochem 38: 371–376
Jansen MAK, Mattoo AK and Edelman M (1999) D1-D2 protein degradation in the chloroplast. Complex light saturation kinetics. Eur J Biochem 260: 527–532
Jin E, Polle J and Melis A (2001) Involvement of zeaxanthin and of the Cbr protein in the repair of photosystem-II from photoinhibition in the green alga Dunaliella salina. Biochim Biophys Acta 1506: 244–259
Jin E, Yokthongwattana K, Polle JEW and Melis A (2003) Role of the reversible xanthophyll cycle in the photosystem-II damage and repair cycle in Dunaliella salina (green alga). Plant Physiol 132: 352–364
Kaplan A (1981) Photoinhibition in Spirulina platensis: response of photosynthesis andHCO3-uptake capability toCO2- depleted conditions. J Exp Bot 32: 669–677
Kim J, Klein PG and Mullet JE (1994) Synthesis and turnover of photosystem II reaction center protein D1. Ribosome pausing increases during chloroplast development. J Biol Chem 269: 17918–17923
Kim JH, Nemson JA and Melis A (1993) Photosystem-II reaction center damage and repair in the green alga Dunaliella salina: analysis under physiological and adverse irradiance conditions. Plant Physiol 103: 181–189
Kindle KL (1990) High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 87: 1228–1232
Koivuniemi A, Aro E-M and Andersson B (1995) Degradation of the D1- and D2-proteins of photosystem II in higher plants is regulated by reversible phosphorylation. Biochemistry 34: 16022–16029
Königer M and Winter K (1993) Reduction of photosynthesis in sun leaves of Gossypium hirsutum L. under conditions of high light intensities and suboptimal leaf temperatures. Agronomie 13: 659–668
Kruse O, Zheleva D and Barber J (1997) Stabilization of photosystem two dimers by phosphorylation: implication for the regulation of the turnover of D1 protein. FEBS Lett 408: 276– 280
Kyle DJ, Ohad I and Arntzen CJ (1984) Membrane protein damage and repair: selective loss of a quinone-protein function in chloroplast membranes. Proc Natl Acad Sci USA 81: 4070– 4074
Lam E, Baltimore B, Ortiz W, Chollar S, Melis A and Malkin R (1983) Characterization of a resolved oxygen-evolving photosystem II preparation from spinach thylakoids. Biochim Biophys Acta 724: 201–211
Lavergne J (1982) Two types of primary acceptors in chloroplast PS II. Photobiochem Photobiophys 3: 257–285
Lavergne J and Briantais J-M (1996) Photosystem-II heterogeneity. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions, pp 265–287. Kluwer Academic Publishers, Dordrecht, The Netherlands
Levy H, Tal T, Shaish A and Zamir A (1993) Cbr, an algal homolog of plant early light-induced proteins, is a putative zeaxanthin binding protein. J Biol Chem 268: 20892–20896
Lindahl M, Spetea C, Hundal T, Oppenheim AB and Andersson B (2000) The thylakoid FtsH protease plays a role in the lightinduced turnover of the photosystem II D1 protein. Plant Cell 12: 419–431
Lorkovic ZJ, Schroder WP, Pakrasi HB, Irrgang K, Herrmann RG and Oelmuller R (1995) Molecular characterization of psbW, a nuclear-encoded component of the photosystem II reaction center complex in spinach. Proc Natl Acad Sci USA 92: 8930– 8934
Ma Y-Z, Holt NE, Li X-P, Niyogi KK and Fleming GR (2003) Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting. Proc Natl Acad Sci USA 100: 4377–4382
Mäenpää P, Andersson B and Sundby C (1987) Difference in sensitivity to photoinhibition between photosystem II in the appressed and non-appressed thylakoid regions. FEBS Lett 215: 31–36
Mattoo AK, Hoffman-Falk H, Marder J and Edelman M (1984) Regulation of protein metabolism: coupling of photosynthetic electron-transport to in vivo degradation of the rapidly metabolized 32-kDa protein of the chloroplast membranes. Proc Natl Acad Sci USA 81: 1380–1384
Mattoo AK and Edelman M (1987) Intramembrane translocation and posttranslational palmitoylation of the chloroplast 32-kDa herbicide-binding protein. Proc Natl Acad Sci USA 84: 1497– 1501
Maxwell DP, Falk S and Huner NPA (1995) Photosystem II excitation pressure and development of resistance to photoinhibition. 1. Light harvesting complex II abundance and zeaxanthin content in Chlorella vulgaris. Plant Physiol 107: 687–694
McKersie BD, Bowley SR, Harjanto E and Leprince O (1996) Water-deficit tolerance and field performance of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 111: 1177–1181
Meetam M, Keren N, Ohad I and Pakrasi HB (1999) The PsbY protein is not essential for oxygenic photosynthesis in the cyanobacterium Synechocystis sp PCC 6803. Plant Physiol 121: 1267–1272
Melis A (1985) Functional properties of PS IIβ in spinach chloroplasts. Biochim Biophys Acta 808: 334–342
Melis A (1989) Spectroscopic methods in photosynthesis: photosystem stoichiometry and chlorophyll antenna size. Philos T Roy Soc B 323: 397–409
Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058: 87–106
Melis A (1996) Excitation energy transfer: functional and dynamic aspects of Lhc (cab) proteins. In: Ort DR and Yocum CF (eds), Oxygenic Photosynthesis: The Light Reactions, pp 523– 538. Kluwer Academic Publishers, Dordrecht, The Netherlands
Melis A (1998) Photostasis in plants: mechanisms and regulation. In: Williams TP and Thistle A (eds) Photostasis and Related Phenomena, pp 207–221. Plenum Publishing Corporation, New York
Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts:what modulates the rate of photodamage in vivo? Trends Plant Sci 4: 130–135
Melis A and Anderson JM (1983) Structural and functional organization of the photosystems in spinach chloroplasts: Antenna size, relative electron transport capacity, and chlorophyll composition. Biochim Biophys Acta 724: 473–484
Melis A and Duysens LNM (1979) Biphasic energy conversion kinetics and absorbance difference spectra of PS II of chloroplasts. Evidence for two different system II reaction centers. Photochem Photobiol 29: 373–382
Melis A and Homann PH (1976) Heterogeneity of the photochemical centers in system II of chloroplasts. Photochem Photobiol 23: 343–350
Melis A and Nemson JA (1995) Characterization of a 160 kD photosystem-II reaction center complex isolated from photoinhibited Dunaliella salina thylakoids. Photosynth Res 46: 207–211
Melis A, Zhang L, Forestier M, Ghirardi ML and Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122: 127– 136
Michel H, Hunt DF, Shabanowitz J and Bennett J (1988) Tandem mass spectrometry reveals that three photosystem II protein of spinach chloroplasts contain N-acetyl-o-phosphothreonine at their NH2 termini. J Biol Chem 263: 1123–1130
Millner PA, Marder JB, Gounaris K and Barber J (1986) Localization and identification of phosphoproteins within the photosystem-II core of higher-plant thylakoid membranes. Biochim Biophys Acta 852: 30–37
Miyazaki A, Shina T, Toyoshima Y, Gounaris K and Barber J (1989) Stoichiometry of cytochrome b-559 in photosystem-II. Biochim Biophys Acta 975: 142–147
Murata N, Miyao M, Omata T, Matsunami H and Kuwabara T (1984) Stoichiometry of components in the photosynthetic oxygen evolution system of photosystem-II particles prepared with Triton X-100 from spinach chloroplasts. Biochim Biophys Acta 765: 363–369
Nanba O and Satoh K (1987) Isolation of a photosystem-II reaction center containing D1 and D2 polypeptides and cytochrome b-559. Proc Natl Acad Sci USA 84: 109–112
Neale PJ and Melis A (1990) Activation of a reserve pool of photosystem II in Chlamydomonas reinhardtii counteracts photoinhibition. Plant Physiol 92: 1196–1204
Neale PJ and Melis A (1991) Dynamics of photosystem II heterogeneity during photoinhibition: depletion of PS IIβ from the non-appressed thylakoids during strong-irradiance exposure of Chlamydomonas reinhardtii. Biochim Biophys Acta 1056: 195–203
Nedbal L, Samson G and Whitmarsh J (1992) Redox state of a one-electron component controls the rate of photoinhibition of photosystem-II. Proc Natl Acad Sci USA 89: 7929–7933
Nield J, Kruse O, Ruprecht J, da Fonseca P and Barber J (2000) Three-dimensional structure of Chlamydomonas reinhardtii and Synechococcus elongatus photosystem II complexes allows for comparison of their oxygen-evolving complex organization. J Biol Chem 275: 27940–27946
Ohad I, Kyle DJ and Arntzen CJ (1984) Membrane protein damage and repair: removal and replacement of inactivated 32- kilodalton polypeptides in chloroplast membranes. J Cell Biol 99: 481–485
Ohnishi N and Takahashi Y (2001) PsbT polypeptide is required for efficient repair of photodamaged photosystem II reaction center. J Biol Chem 276: 33798–33804
Park YI, Chow WS, Osmond CB and Anderson JM (1996) Electron transport to oxygen mitigates against the photoinactivation of Photosystem II in vivo. Photosynth Res 50: 23–32
Park YI, Chow WS and Anderson JM (1997) Antenna size dependency of photoinactivation of photosystem II in lightacclimated pea leaves. Plant Physiol 115: 151–157
Payton P, Allen RD, Trolinder N and Holaday AS (1998) Overexpression of chloroplast-targeted Mn superoxide dismutase in cotton (Gossypium hirsutum L.) does not alter the reduction of photosynthesis after short exposures to lowtemperature and high light intensity. Photosynth Res 52: 233–244
Polle JEW and Melis A (1999) Recovery of the photosynthetic apparatus from photoinhibition during dark incubation of the green alga Dunaliella salina. Aust J Plant Physiol 26: 679–686
Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35: 15–44
Pursiheimo S, Rintamäki E, Baena-González E and Aro E-M (1998) Thylakoid protein phosphorylation in evolutionally divergent species with oxygenic photosynthesis. FEBS Lett 423: 178–182
Rhee K-H, Morriss EP, Barber J and Kuhlbrandt W (1998) Threedimensional structure of the plant photosystem II reaction centre at 8 angstrom resolution. Nature 396: 283–286
Rintamäki E, Kettunen R and Aro E-M (1996) Differential D1 phosphorylation in functional and photodamaged photosystem II centers: dephosphorylation is a prerequisite for degradation of damaged D1. J Biol Chem 271: 14870–14875
Schroda M, Vallon O, Wollman FA and Beck CF (1999) A chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of PS II during and after photoinhibition. Plant Cell 11: 1165–1178
Seibert M, Picorel R, Rubin AB and Connolly JS (1988) Spectral, photophysical, and stability properties of isolated photosystem-II reaction center. Plant Physiol 87: 303– 306
Shi LX, Kim SJ, Marchant A, Robinson C and others (1999) Characterisation of the PsbX protein from Photosystem II and light regulation of its gene expression in higher plants. Plant Mol Biol 40: 737–744
Silva P, Choi YJ, Hassan HAG and Nixon PJ (2002) Involvement of the HtrA family of proteases in the protection of the cyanobacterium Synechocystis PCC 6803 from light stress and in the repair of photosystem II. Philos T Roy Soc B 357: 1461– 1467
Smirnoff N (1995) Antioxidant systems and plant responses to the environment. In: Smirnoff N (ed) Environment and Plant Metabolism, pp 217–242. BIOS Scientific Publishers Ltd, Oxford, UK
Smith BM, Morrissey PJ, Guenther JE, Nemson JA, Harrison MA, Allen JF and Melis A (1990) Response of the photosynthetic apparatus in Dunaliella salina (green algae) to irradiance stress. Plant Physiol 93: 1433–1440
Sundby C, McCaffery S and Anderson JM (1993) Turnover of the photosystem II D1 protein in higher plants under photoinhibitory and nonphotoinhibitory irradiance. J Biol Chem 268: 25476–25482
Tam L-W and Lefebvre PA (1993) Cloning of flagellar genes in Chlamydomonas reinhardtii byDNAinsertional mutagenesis. Genetics 135: 375–384
Thielen APGM and VanGorkom HJ (1981) Electron transport properties of the photosystems IIα and IIβ. In: Akoyunoglou G (ed) Photosynthesis, Proceedings of 5th International Congress, Vol II, pp 57–64. Balaban International Science Services, Philadelphia
Thornber JP (1986) Biochemical characterization and structure of pigment-proteins of photosynthetic organisms. In: Staehelin LA and Arntzen CJ (eds) Encyclopedia of Plant Physiology, Vol 19, pp 98—115. Springer Verlag, New York
Tyystjärvi E and Aro E-M (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci USA 93: 2213–2218
Tyystjärvi E, Koivuniemi A, Kettunen R and Aro E-M (1991) Small light-harvesting antenna does not protect from photoinhibition. Plant Physiol 97: 477–483
Tyystjärvi E, Kettunen R and Aro E-M (1994) The rate constant of photoinhibition in vitro is independent of the antenna size of photosystem II but depends on temperature. Biochim Biophys Acta 1186: 177–185
Vallon O, Wollman FA and Olive J (1986) Lateral distribution of the main protein complexes of the photosynthetic apparatus in Chlamydomonas reinhardtii and in spinach: an immunocytochemical study using intact thylakoid membranes and a PS II-enriched membrane preparation. Photobiochem Photobiophys 12: 203–220
VallonO, Hoyer-HansenGand Simpson DJ (1987) Photosystem- II and cytochrome b-559 in the stroma lamellae of barley chloroplasts. Carlsberg Res Commun 52: 405– 421
Van Gorkom HJ (1985) Electron transfer in photosystem-II. Photosynth Res 6: 97–112
Vasilikiotis C and Melis A (1994) Photosystem-II reaction center damage and repair cycle—chloroplast acclimation strategy to irradiance stress. Proc Natl Acad Sci USA 91: 7222–7226
Wettern M (1986) Localization of 32,000 dalton chloroplast protein pools in thylakoids: significance in atrazine binding. Plant Sci 43: 173–177
Wykoff DD, Davies JP, Melis A and Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117: 129–139
Xu CC, Lee H-Y and Lee C-H (1999) Recovery from lowtemperature photoinhibition is not governed by changes in the level of zeaxanthin in rice (Oryza sativa L.) leaves. J Plant Physiol 155: 755–761
Yamamoto Y (2001) Quality control of photosystem II. Plant Cell Physiol 42: 121–128
Yokthongwattana K, ChrostB, Behrman S, Casper-Lindley C and Melis A (2001) Photosystem II damage and repair cycle in the green alga Dunaliella salina: involvement of a chloroplastlocalized HSP70. Plant Cell Physiol 42: 1389–1397
Zhang L, Niyogi KK, Baroli I, Nemson JA, Grossman A and Melis A (1997) DNA insertional mutagenesis for the elucidation of a PS II repair process in the green alga Chlamydomonas reinhardtii. Photosynth Res 53: 173–184
Zouni A, Witt HT, Kern J, Fromme P, Krauss, N, Saenger W and Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409: 739– 743
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Yokthongwattana, K., Melis, A. (2008). Photoinhibition and Recovery in Oxygenic Photosynthesis: Mechanism of a Photosystem II Damage and Repair Cycle. In: Demmig-Adams, B., Adams, W.W., Mattoo, A.K. (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment. Advances in Photosynthesis and Respiration, vol 21. Springer, Dordrecht. https://doi.org/10.1007/1-4020-3579-9_12
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