Singlet oxygen production in photosystem II and related protection mechanism

Photosynthesis Research - Tập 98 Số 1-3 - Trang 551-564 - 2008
Anja Krieger‐Liszkay1, Christian Fufezan2, Achim Trebst3
1CEA, Institut de Biologie et Technologies de Saclay, CNRS URA 2096, Service de Bioénergétique Biologie Structurale et Mécanisme, 91191, Gif-sur-Yvette Cedex, France
2Institut für Biochemie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Münster, Germany
3Plant Biochemistry, Ruhr-University Bochum, Bochum, Germany

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Tài liệu tham khảo

Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition—a historical perspective. Photosynth Res 76:343–370. doi: 10.1023/A:1024969518145

Anderson JM, Osmond CB (1987) Shade-sun responses: compromises between acclimation and photoinhibition. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elesevier, Amsterdam, pp 1–36

Andréasson LE, Vass I, Styring S (1995) Ca2+-depletion modifies the electron transfer on both donor and acceptor sides in photosystem II. Biochim Biophys Acta 1230:155–164. doi: 10.1016/0005-2728(95)00047-M

Andrée S, Weis E, Krieger A (1998) Heterogeneity and photoinhibition of photosystem II studied by thermoluminescence. Plant Physiol 116:1053–1061. doi: 10.1104/pp.116.3.1053

Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134. doi: 10.1016/0005-2728(93)90134-2

Beck CF (2005) Signaling pathways from the chloroplast to the nucleus. Planta 222:743–756. doi: 10.1007/s00425-005-0021-2

Briantais JM, Ducruet JM, Hodges M, Krause GH (1992) Effects of high light at chilling temperature on photosystem II in spinach leaves. Photosynth Res 31:1–10. doi: 10.1007/BF00049531

Clarke AK, Soitamo A, Gustafsson P, Öquist G (1993) Rapid interchange between two distinct forms of cyanobacterial photosystem II reaction-center protein D1 in response to photoinhibition. Proc Natl Acad Sci USA 90:9973–9977. doi: 10.1073/pnas.90.21.9973

Cser K, Vass I (2007) Radiative and non-radiative charge recombination pathways in photosystem II studied by thermoluminescence and chlorophyll fluorescence in the cyanobacterium Synechocystis 6803. Biochim Biophys Acta 1767:233–243. doi: 10.1016/j.bbabio.2007.01.022

Cuni A, Xiong L, Sayre RT, Rappaport F, Lavergne J (2004) Modification of the pheophytin midpoint potential in photosystem II: modulation of the quantum yield of charge separation and charge recombination pathways. Phys Chem Chem Phys 6:4825–4831. doi: 10.1039/b407511k

Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role of the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24. doi: 10.1016/0005-2728(90)90088-L

Depka B, Jahns P, Trebst A (1998) Beta-carotene to zeaxanthin conversion in the rapid turnover of the D1 protein of photosystem II. FEBS Lett 424:267–270. doi: 10.1016/S0014-5793(98)00188-4

Diner BA, Schlodder E, Nixon PJ, Coleman WJ, Rappaport F, Lavergne J et al (2001) Site-directed mutations at D1-His198 and D2-His197 of photosystem II in Synechocystis PCC 6803: sites of primary charge separation and cation and triplet stabilization. Biochemistry 40:9265–9281. doi: 10.1021/bi010121r

Dorlet P, Xiong L, Sayre RT, Un S (2001) High field EPR study of the pheophytin anion radical in wild type and D1-E130 mutants of photosystem II in Chlamydomonas reinhardtii. J Biol Chem 276:22313–22316. doi: 10.1074/jbc.M102475200

Durrant JR, Giorgi LB, Barber J, Klug DR, Porter G (1990) Characterization of triplet-states in isolated photosystem II reaction centres—oxygen quenching as a mechanism for photodamage. Biochim Biophys Acta 1017:175–176

Eckhardt U, Grimm B, Hörtensteiner S (2004) Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol Biol 56:1–14. doi: 10.1007/s11103-004-2331-3

Edge R, Truscott TG (1999) Carotenoid radicals and the interaction of carotenoids with active oxygen species. In: Frank HA, Young AJ, Britton D, Cogdell RJ (eds) Advances in photosynthesis: the photochemistry of carotenoids, vol 8. Kluwer, Dordrecht, pp 223–234

Faller P, Fufezan C, Rutherford AW (2006) Side-path electron donors: cytochrome b559, chlorophyll Z and β-carotene. In: Wydrzynski T, Satoh K (eds) Photosystem II: the water/plastoquinone oxido-reductase in photosynthesis. Kluwer, Dordrecht chap. 15

Farineau J (1990) Photochemical alterations of photosystem II induced by two different photoinhibitory treatments in isolated chloroplasts in pea. A thermoluminescence study. Biochim Biophys Acta 1016:357–363. doi: 10.1016/0005-2728(90)90169-5

Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving centre. Science 303:1831–1838. doi: 10.1126/science.1093087

Fischer BB, Eggen RI, Trebst A, Krieger-Liszkay A (2006) The glutathione peroxidase homologous gene Gpxh in Chlamydomonas reinhardtii is upregulated by singlet oxygen produced in photosystem II. Planta 223:583–590. doi: 10.1007/s00425-005-0108-9

Fischer BB, Krieger-Liszkay A, Hideg E, Snyrychová I, Wiesendanger M, Eggen RI (2007) Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii. FEBS Lett 581:5555–5560. doi: 10.1016/j.febslet.2007.11.003

Fufezan C, Rutherford AW, Krieger-Liszkay A (2002) Singlet oxygen production in herbicide-treated photosystem II. FEBS Lett 532:407–410. doi: 10.1016/S0014-5793(02)03724-9

Fufezan C, Gross CM, Sjödin M, Rutherford AW, Krieger-Liszkay A, Kirilovsky D (2007) Influence of the redox potential of the primary quinone electron acceptor on photoinhibition in photosystem II. J Biol Chem 282:12492–12502. doi: 10.1074/jbc.M610951200

Golan T, Müller-Moulé P, Niyogi KK (2006) Photoprotection mutants of Arabidopsis thaliana acclimate to high light by increasing photosynthesis and specific antioxidants. Plant Cell Environ 29:879–887. doi: 10.1111/j.1365-3040.2005.01467.x

Goussias C, Boussac A, Rutherford AW (2002) Photosystem II and photosynthetic oxidation of water: an overview. Philos Trans R Soc Lond B 57:1369–1381. doi: 10.1098/rstb.2002.1134

Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. University Press, Oxford, UK

Hanley J, Deligiannakis Y, Pascal A, Faller P, Rutherford AW (1999) Carotenoid oxidation in photosystem II. Biochemistry 38:8189–8195. doi: 10.1021/bi990633u

Harel Y, Ohad I, Kaplan A (2004) Activation of photosynthesis and resistance to photoinhibition in cyanobacteria within biological desert crust. Plant Physiol 136:3070–3079. doi: 10.1104/pp.104.047712

Hatz S, Lambert JDC, Ogilby PR (2007) Measuring the lifetime of singlet oxygen in a single cell: addressing the issue of cell viability. Photochem Photobiol Sci 6:1106–1116. doi: 10.1039/b707313e

Havaux M, Bonfits J-P, Lütz C, Niyogi KK (2000) Photodamage of the photosynthetic apparatus and its dependence on the leaf development stage in the npq1 Arabidopsis mutant deficient in the xanthophylls cyle enzyme violaxanthin de-epoxidase. Plant Physiol 124:273–284. doi: 10.1104/pp.124.1.273

Heber U, Azarkovich M, Shuvalov V (2007) Activation of mechanisms of photoprotection by desiccation and by light: poikilohydric photoautotrophs. J Exp Bot 58:2745–2759. doi: 10.1093/jxb/erm139

Heddad M, Norén H, Reiser V, Dunaeva M, Andersson B, Adamska I (2006) Differential expression and localization of early light-induced proteins in Arabidopsis. Plant Physiol 142:75–87. doi: 10.1104/pp.106.081489

Hideg E, Spetea C, Vass I (1994) Singlet oxygen production in thylakoid membranes during photoinhibition as detected by EPR spectroscopy. Photosynth Res 39:191–199. doi: 10.1007/BF00029386

Hideg E, Ogawa K, Kalai T, Hideg K (2001) Singlet oxygen imaging in Arabidopsis thaliana leaves under photoinhibition by excess photosynthetically active radiation. Physiol Plant 112:10–14. doi: 10.1034/j.1399-3054.2001.1120102.x

Hideg E, Barta C, Kalai T, Vass I, Hideg K, Asada K (2002) Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol 43:1154–1164. doi: 10.1093/pcp/pcf145

Hideg E, Kós PB, Vass I (2007) Photosystem II damage induced by chemically generated singlet oxygen in tobacco leaves. Physiol Plant 131:33–40. doi: 10.1111/j.1399-3054.2007.00913.x

Holt NE, Fleming GR, Niyogi KK (2004) Towards an understanding of the mechanism of non-photochemical quenching in green plants. Biochemistry 43:8281–8289. doi: 10.1021/bi0494020

Horton P, Ruban A (2005) Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. J Exp Bot 56:365–373. doi: 10.1093/jxb/eri023

Horton P, Johnson MP, Perez-Bueno ML, Kiss AZ, Ruban AV (2008) Photosynthetic acclimation: does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J 275:1069–1079. doi: 10.1111/j.1742-4658.2008.06263.x

Hundal T, Forsmark-Andree P, Ernster L, Andersson B (1995) Antioxidant activity of reduced plastoquinone in chloroplast thyalkoid membranes. Arch Biochem Biophys 324:117–122. doi: 10.1006/abbi.1995.9920

Ishikita H, Knapp EW (2005) Control of quinone redox potentials in photosystem II: electron transfer and photoprotection. J Am Chem Soc 127:14714–21470. doi: 10.1021/ja052567r

Jansen MA, Depka B, Trebst A, Edelman M (1993) Engagement of specific sites in the plastoquinone niche regulates degradation of the D1 protein in photosystem II. J Biol Chem 268:21246–21252

Johnson G, Krieger A (1994) Thermoluminescence as a probe of photosystem II in intact leaves: non-photochemical fluorescence quenching in peas grown in an intermittent light regime. Photosynth Res 41:371–379. doi: 10.1007/BF02183039

Johnson GN, Boussac A, Rutherford AW (1994) The origin of the 40–50°C thermoluminescence bands in photosystem II. Biochim Biophys Acta 1184:85–92. doi: 10.1016/0005-2728(94)90157-0

Johnson G, Rutherford AW, Krieger A (1995) A change in the midpoint potential of the quinone QA in photosystem II associated with photoactivation of oxygen evolution. Biochim Biophys Acta 1229:202–207. doi: 10.1016/0005-2728(95)00003-2

Kamlowski A, Frankemöller I, van der Est A, Stehlik D, Holzwarth AR (1996) Evidence for the delocalization of the triplet state 3P680 in the D1D2cytb559-complex of photosystem II. Ber Bunsen-Ges 100:2045–2051

Kautsky H, de Bruijn (1931) Die Aufklärung der Photoluminescenztilgung fluorescierender Systeme durch Sauerstoff: Die Bildung aktiver, diffusionsfähiger Sauerstoffmoleküle durch Sensibilisierung. Naturwissenschaften 19:1043. doi: 10.1007/BF01516190

Keren N, Gong H, Ohad I (1995) Oscillations of reaction centre II-D1 protein degradation in vivo induced by repetitive flashes. J Biol Chem 270:806–814. doi: 10.1074/jbc.270.24.14611

Keren N, Berg A, van Kan PJM, Levanon H, Ohad I (1997) Mechanism of photosystem II inactivation and D1 protein degradation at low light intensities: the role of electron back flow. Proc Natl Acad Sci USA 94:1579–1584. doi: 10.1073/pnas.94.4.1579

Keren N, Ohad I, Drepper F, Rutherford AW, Krieger-Liszkay A (2000) Inhibition of photosystem II activity by saturating single turnover flashes in calcium-depleted and active photosystem II. Photosynth Res 63:209–216. doi: 10.1023/A:1006435530817

Kim C, Meskauskiene R, Apel K, Laloi C (2008) No single way to understand singlet oxygen signalling in plants. EMBO Rep 9:435–439. doi: 10.1038/embor.2008.57

Kirilovsky D, Vernotte C, Astier C, Etienne AL (1988) Reversible and irreversible photoinhibition in herbicide-resistant mutants of Synechocystis 6714. Biochim Biophys Acta 933:124–131. doi: 10.1016/0005-2728(88)90062-X

Kirilovsky D, Rutherford AW, Etienne AL (1994) Influence of DCMU and ferricyanide on photodamage in photosystem II. Biochemistry 33:3087–3095. doi: 10.1021/bi00176a043

Kós PB, Deák Z, Cheregi O, Vass I (2008) Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim Biophys Acta 1777:74–83. doi: 10.1016/j.bbabio.2007.10.015

Krieger A, Rutherford AW (1997) Comparison of chloride-depleted and calcium-depleted PSII: the midpoint potential of QA and susceptibility to photodamage. Biochim Biophys Acta 1319:91–98. doi: 10.1016/S0005-2728(96)00117-X

Krieger A, Weis E (1992) Energy-dependent quenching of chlorophyll-a-fluorescence: the involvement of a proton-calcium exchange at photosystem II. Photosynthetica 27:89–98

Krieger A, Weis E (1993) The role of calcium in the pH-dependent control of photosystem II. Photosynth Res 37:117–130. doi: 10.1007/BF02187470

Krieger A, Weis E, Demeter S (1993) Low pH-induced Ca ion release in the water-splitting system is accompanied by a shift in the midpoint redox potential of the primary quinone acceptor QA. Biochim Biophys Acta 1144:411–418. doi: 10.1016/0005-2728(93)90128-3

Krieger A, Rutherford AW, Johnson GN (1995) On the determination of the redox mid-point potential of the primary quinone acceptor, QA, in photosystem II. Biochim Biophys Acta 1229:193–201. doi: 10.1016/0005-2728(95)00002-Z

Krieger A, Rutherford AW, Vass I, Hideg E (1998a) Relationship between activity, D1 loss, and Mn binding in photoinhibition of photosystem II. Biochemistry 37:16262–16269. doi: 10.1021/bi981243v

Krieger A, Rutherford AW, Jegerschöld C (1998b) Thermoluminescence measurements on chloride-depleted and calcium-depleted photosystem II. Biochim Biophys Acta 1364:46–54. doi: 10.1016/S0005-2728(98)00009-7

Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346. doi: 10.1093/jxb/erh237

Krieger-Liszkay A, Rutherford AW (1998) Influence of herbicide binding on the redox potential of the quinone acceptor in photosystem II: relevance to photodamage and phytotoxicity. Biochemistry 37:17339–17344. doi: 10.1021/bi9822628

Krieger-Liszkay A, Trebst A (2006) Tocopherol is the scavenger of singlet oxygen produced by the triplet state of chlorophyll in the PSII reaction centre. J Exp Bot 57:1677–1684. doi: 10.1093/jxb/erl002

Kruk J, Trebst A (2008) Plastoquinol as a singlet oxygen scavenger in photosystem II. Biochim Biophys Acta 1777:154–162. doi: 10.1016/j.bbabio.2007.10.008

Kruk J, Strzałka, Schmid GH (1994) Antioxidant properties of plastoquinol and other biological prenylquinols in liposomes qnd solution. Free Radic Res 21:409–416. doi: 10.3109/10715769409056593

Kruk J, Holländer-Czytko H, Oettmeier W, Trebst A (2005) Tocopherol as singlet oxygen scavenger in photosystem II. J Plant Physiol 162:749–757. doi: 10.1016/j.jplph.2005.04.020

Laloi C, Przybyla D, Apel K (2006) A genetic approach towards elucidating the biological activity of different reactive oxygen species in Arabidopsis thaliana. J Exp Bot 57:1719–1724. doi: 10.1093/jxb/erj183

Laloi C, Stachowiak M, Pers-Kamczyc E, Warzych E, Murgia I, Apel K (2007) Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:672–677. doi: 10.1073/pnas.0609063103

Ledford HK, Chin BL, Niyogi KN (2007) Acclimation to singlet oxygen stress in Chlamydomonas reinhardtii. Eukaryot Cell 6:919–930. doi: 10.1128/EC.00207-06

Lee KP, Kim C, Landgraf F, Apel K (2007) EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci USA 104:10270–10275. doi: 10.1073/pnas.0702061104

Leisinger U, Rüfenacht K, Fischer B, Pesaro M, Spengler A, Zehnder AJB et al (2001) The glutathione peroxidase homologous gene from Chlamydomonas reinhardtii is transcriptionally upregulated by singlet oxygen. Plant Mol Biol 46:395–408. doi: 10.1023/A:1010601424452

Loll B, Kern J, Saenger W, Zouni A, Biesieadka J (2005) Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II. Nature 438:1040–1044. doi: 10.1038/nature04224

Macpherson AN, Telfer A, Truscott TG, Barber J (1993) Direct detection of singlet oxygen from isolated photosystem II reaction centres. Biochim Biophys Acta 1143:301–309. doi: 10.1016/0005-2728(93)90201-P

Matile P, Hortensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Physiol Plant Mol Biol 50:67–95. doi: 10.1146/annurev.arplant.50.1.67

Merry SAP, Nixon PJ, Barter LMC, Schilstra MJ, Porter G, Barber J et al (1998) Modulation of quantum yield of primary radical formation in photosystem II by site-directed mutagenesis affecting radical cations and anions. Biochemistry 37:17439–17447. doi: 10.1021/bi980502d

Mizusawa N, Miyao M, Yamashita T (1997) Restoration of the high potential from of cytochrome b559 of photosystem II occurs via a two-step mechanism under illumination in the presence of manganese ions. Biochim Biophys Acta 1318:145–148. doi: 10.1016/S0005-2728(96)00130-2

Murchie EH, Hubbart S, Peng S, Horton P (2005) Acclimation of photosynthesis to high irradiance in rice: gene expression and interactions with leaf development. J Exp Bot 56:449–460. doi: 10.1093/jxb/eri100

Nakajima Y, Yoshida S, Ono T (1996) Differential effects of urea/triazine-type and phenol-type photosystem II inhibitors on inactivation of the electron transport and degradation of the D1 protein during photoinhibition. Plant Cell Physiol 37:673–680

Neely WC, Martin M, Barker SA (1988) Products and relative reaction rates of the oxidation of tocopherols with singlet molecular oxygen. Photochem Photobiol 48:423–428. doi: 10.1111/j.1751-1097.1988.tb02840.x

Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H, Murata N (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43:11321–11330. doi: 10.1021/bi036178q

Nixon PJ, Barker M, Boehm M, de Vries R, Komenda J (2005) FtsH-mediated repair of the photosystem II complex in response to light stress. J Exp Bot 56:357–363. doi: 10.1093/jxb/eri021

Noguchi T, Tomo T, Kato C (2001) Fourier transform infrared study of the cation radical of P680 in the photosystem II reaction center: evidence for charge delocalization on the chlorophyll dimer. Biochemistry 40:2176–2185. doi: 10.1021/bi0019848

Ohad I, Koike H, Shochat S, Inoue Y (1988) Changes in the properties of reaction center II during the initial stages of photoinhibition as revealed by thermoluminescence measurements. Biochim Biophys Acta 933:288–298. doi: 10.1016/0005-2728(88)90036-9

op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Göbel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332

Pallet KE, Dodge AD (1980) Studies into the action of some photosynthetic inhibitor herbicides. J Exp Bot 31:1051–1066

Prasil O, Adir N, Ohad I (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery process. In: Barber J (ed) Topics in photosynthesis, the photosystems: structure, function and molecular biology. Elsevier, Amsterdam, pp 220–250

Rappaport F, Diner BA (2008) Primary photochemistry and energetics leading to the oxidation of the (Mn)4Ca cluster and to the evolution of molecular oxygen in photosystem II. Coord Chem Rev 252:259–272

Rappaport F, Guergova-Kuras M, Nixon PJ, Diner BA, Lavergne J (2002) Kinetics and pathways of charge recombination in photosystem II. Biochemistry 41:8518–8527

Rappaport F, Cuni A, Xiong L, Sayre R, Lavergne J (2005) Charge recombination and thermoluminescence in photosystem II. Biophys J 88:1948–1958

Renger G (2008) Functional pattern of photosystem II. In: Renger G (ed) Primary processes in photosynthesis. RSC Publishing, Cambridge, UK, pp 237–290 part 2

Roberts AG, Gregor W, Britt RD, Kramer DM (2003) Acceptor and donor-side interactions of phenolic inhibitors in photosystem II. Biochim Biophys Acta 1604:23–32

Rochaix JD (2007) Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett 581:2768–2775

Rutherford AW, Krieger-Liszkay A (2001) Herbicide-induced oxidative stress in photosystem II. Trends Biochem Sci 26:648–653

Rutherford AW, Crofts AR, Inoue Y (1982) Thermoluminescence as a probe of photosystem II photochemistry: the origin of the flash-induced glow peaks. Biochim Biophys Acta 682:457–465

Sane PV, Ivanov AG, Hurry V, Huner NPA, Öquist G (2003) Changes in the redox potential of primary and secondary electron-accepting quinones in photosystem II confer increased resistance to photoinhibition in low-temperature-acclimated Arabidopsis. Plant Phys 132:2144–2151

Schatz GH, Brock H, Holzwarth AR (1988) Kinetic and energetic model for the primary processes in photosystem II. Biophys J 54:397–405

Schmidt K, Fufezan C, Krieger-Liszkay A, Satoh H, Paulsen H (2003) Recombinant water-soluble chlorophyll protein from Brassica oleracea var. botrys binds various chlorophyll derivatives. Biochemistry 42:7427–7433

Shao N, Krieger-Liszkay A, Schroda M, Beck CF (2007) A reporter system for the individual detection of hydrogen peroxide and singlet oxygen: its use for the assay of reactive oxygen species produced in vivo. Plant J 50:475–487

Sharma J, Panico M, Barber J, Morris HR (1997) Characterization of the low molecular weight photosystem II reaction center subunits and their light-induced modifications by mass spectrometry. J Biol Chem 272:3935–3943

Skovsen E, Snyder JW, Lambert JDC, Ogilby PR (2005) Lifetime and diffusion of singlet oxygen in a cell. J Phys Chem B 109:8570–8573

Szilard A, Sass L, Hideg E, Vass I (2005) Photoinactivation of photosystem II by flashing light. Photosynth Res 84:15–20

Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182

Takano A, Takahashi R, Suzuki H, Noguchi T (2008) Herbicide effect on the hydrogen-bonding interaction of the primary quinone electron acceptor QA in photosystem II as studied by Fourier transform infrared spectroscopy. Photosynth Res. doi: 10.1007/s11120-008-9302-5

Telfer A (2002) What is β-carotene doing in the photosystem II reaction centre? Phil Trans R Soc Lond B 357:1431–1440

Telfer A (2005) Too much light? How beta-carotene protects the photosystem II reaction centre. Photochem Photobiol Sci 4:950–956

Tichý M, Lupínková L, Sicora C, Vass I, Kuviková S, Prásil O, Komenda J (2003) Synechocystis 6803 mutants expressing distinct forms of the photosystem II D1 protein from Synechococcus 7942: relationship between the psbA coding region and sensitivity to visible and UV-B radiation. Biochim Biophys Acta 1605:55–66

Trebst A (2003) Function of beta-carotene and tocopherol in photosystem II. Z Naturforsch C 58:609–620

Trebst A, Depka B (1997) Role of carotene in the rapid turnover and assembly of photosystem II in Chlamydomonas reinhardtii. FEBS Lett 400:359–362

Trebst A, Depka B, Hollander-Czytko H (2002) A specific role for tocopherol and of chemical singlet oxygen quenchers in the maintenance of photosystem II structure and function in Chlamydomonas reinhartii. FEBS Lett 516:156–160

Tyystjärvi E (2008) Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coord Chem Rev 252:361–376

van Gorkom HJ (1985) Electron transfer in photosystem II. Photosynth Res 6:97–112

van Mieghem FJE, Satoh K, Rutherford AW (1991) A chlorophyll tilted 30 relative to the membrane in the photosystem II reaction center. Biochim Biophys Acta 1058:379–385

Vass I, Aro EM (2007) Photoinhibition of photosynthetic electron transport. In: Renger G (ed) Primary processes in photosynthesis, comprehensive series in photochemical and photobiological sciences. RSC Publishing, The Royal Society of Chemistry, Cambridge, UK, pp 393–425 part 1

Vass I, Mohanty N, Demeter S (1988) Photoinhibition of electron transport activity of photosystem II in isolated thylakoids studied by thermoluminescence and delayed luminescence. Z Naturforsch 43c:871–876

Vass I, Styring S, Hundal T, Koivuniemi A, Aro EM, Andersson B (1992) Reversible and irreversible intermeidates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89:1408–1412

Vass I, Sass L, Spetea C, Bakou A, Ghanotakis DF, Petrouleas V (1996) UV-B-induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence. Impairment of donor and acceptor side components. Biochemistry 35:8964–8973

Vavilin DV, Vermaas WFJ (2000) Mutations in the CD-loop region of the D2 protein in Synechocystis sp. PCC 6803 modify charge recombination reaction pathways in photosystem II in vivo. Biochemistry 39:14831–14838

Vavilin D, Vermaas W (2007) Continuous chlorophyll degradation accompanied by chlorophyllide and phytol reutilization for chlorophyll synthesis in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1767:920–929

von Gromoff ED, Alawady A, Meinecke L, Grimm B, Beck CF (2008) Heme, a plastid-derived regulator of nuclear gene expression in Chlamydomonas. Plant Cell 20:552–567

Vrettos JS, Stewart DH, dePaula JC, Brudvig GW (1999) Low-temperature optical and resonance Raman of carotenoid cation radical in photosystem II. J Phys Chem B 103:6403–6406

Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447

Wilson A, Ajlani G, Verbavatz JM, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992–1007