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Reaction centre quenching of excess light energy and photoprotection of photosystem II

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Abstract

In addition to the energy dissipation of excess light occurring in PSII antenna via the xanthophyll cycle, there is mounting evidence of a zeaxanthin-independent pathway for non-photochemical quenching based within the PSII reaction centre (reaction centre quenching) that may also play a significant role in photoprotection. It has been demonstrated that acclimation of higher plants, green algae and cyanobacteria to low temperature or high light conditions which potentially induce an imbalance between energy supply and energy utilization is accompanied by the development of higher reduction state of QA and higher resistance to photoinhibition (Huner et al., 1998). Although this is a fundamental feature of all photoautotrophs, and the acquisition of increased tolerance to photoinhibition has been ascribed to growth and development under high PSII excitation pressure, the precise mechanism controlling the redox state of QA and its physiological significance in developing higher resistance to photoinhibition has not been fully elucidated. In this review we summarize recent data indicating that the increased resistance to high light in a broad spectrum of photosynthetic organisms acclimated to high excitation pressure conditions is associated with an increase probability for alternative non-radiative P680+QA - radical pair recombination pathway for energy dissipation within the reaction centre of PSII. The various molecular mechanisms that could account for non-photochemical quenching through PSII reaction centre are also discussed.

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Abbreviations

Cytb 559 :

cytochromeb 559

D1:

photosystem II reaction centre polypeptide

D2:

photosystem II reaction centre polypeptide

Fo :

minimum yield of chlorophyll fluorescence at open PSII centres in dark-adapted leaves

Fm :

maximum yield of fluorescence at closed PSII reaction centres in dark adapted leaves

Fimv :

variable yield of fluorescence in dark adapted leaves

Fv/Fm :

maximum PSII photochemical efficiency in dark adapted leaves

LHCII:

the major Chl a/b pigment-protein complex associated with PSII

NPQ:

non-photochemical quenching

OEC:

oxygen evolving complex

Pheo:

pheophytin

PSI:

photosystem I

PSII:

photosystem II

PSIIβ:

photosystem β centres

PSIIoα:

photosystem a centres

PsbS:

PSII subunit and gene product of thePsbS gene

PQ:

plastoquinone

QA :

primary electron-accepting quinone in PSII reaction centres

Qb :

secondary electron-accepting quinone in PSII reaction centres

qE:

ΔpH dependent high energy quenching; quenching coefficient for basal fluorescence

qP:

photochemical quenching coefficient

TL:

thermoluminescence

T M :

temperature of maximum thermoluminescence emission

V:

violaxanthin

Z:

zeaxanthin

Literature Cited

  • Adams WW, Demmig-Adams B, Rosenstiel TN, Ebbert V (2001) Dependence of photosynthesis and energy dissipation activity upon growth form and light environment during the winter. Photosynth Res67: 51–62

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Klirmov W, Carpentier R (1997) Evidence for the involvement of cyclic electron transport in the protection of photosystem II against photoinhibition: Influence of a new phenolic compound. Biochemistry36: 4149–4154

    Article  PubMed  CAS  Google Scholar 

  • Allen JF (1995) Thylakoid protein phosphorilation, state 1- state 2 transitions, and phosystem stoichiometry adjustment: Redox control at multiple levels of gene expression. Physiol Plant93: 196–205

    Article  CAS  Google Scholar 

  • Anderson JM (1986) Photoregulation of the composition, function and structure of thylakoid membranes. Annu Rev Plant Physiol37: 93–136

    Article  CAS  Google Scholar 

  • Anderson JM (1992) Cytochrome b6/f complex: Dynamic molecular organization, function and acclimation. Photosynth Res34: 341–357

    Article  CAS  Google Scholar 

  • Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta1143: 113–134

    Article  PubMed  CAS  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol50: 601–639

    Article  PubMed  CAS  Google Scholar 

  • Aspinall-O’Dea M, Wentworth M, Pascal A, Robert B, Ruban A, Horton P (2002)In vitro reconstitution of the activated zeaxanthin state associated with energy dissipation in plants. Proc Natl Acad Sci USA99: 16331–16335

    Article  PubMed  CAS  Google Scholar 

  • Barber J, De Las Rivas J (1993) A functional model for the role of cytochrome-b 559 in the protection against donor and acceptor side photoinhibition. Proc Natl Acad Sci USA90: 10942–10946

    Article  PubMed  CAS  Google Scholar 

  • Bassi R, Croce R, Cugini D, Sandona D (1999) Mutational analysis of a higher plant antenna protein provides identification of chromophores bound in multiple sites. Proc Natl Acad Sci USA96: 10056–10061

    Article  PubMed  CAS  Google Scholar 

  • Booij-James IS, Swegle WM, Edelman M, Mattoo AK (2002) Phosphorylation of the D1 photosystem II reaction center protein Is controlled by an endogenous circadian rhythm. Plant Physiol130: 2069–2075

    Article  PubMed  CAS  Google Scholar 

  • Briantais J-M, Dueruet J-M, Hodges M, Krause GH (1992) The effects of low temperature acclimation and photoinhibitory treatments on Photosystem 2 studied by thermoluminescence and fluorescence decay kinetics. Photosynth Res 31: 1–10

    Article  CAS  Google Scholar 

  • Briantais J-M, Vernotte C, Picaud M, Krause GH (1979) A quantitative study of the slow decline of chlorophyll fluorescence in isolated chloroplasts. Biochim Biophys Acta548: 128–138

    Article  PubMed  CAS  Google Scholar 

  • Bruce D, Samson G, Carpenter C (1997) The origins of nonphoto-chemical quenching of chlorophyll fluorescence in photosynthesis. Direct quenching by P680+ in photosystem II enriched membranes at low pH. Biochemistry36: 749–755

    Article  PubMed  CAS  Google Scholar 

  • Bukhov NG, Heber U, Wiese C, Shuvalov VA (2001) Energy dissipation in photosynthesis: Does the quenching of chlorophyll fluorescence originate from antenna complexes of photosystem II or from the reaction center? Planta212: 749–758

    Article  PubMed  CAS  Google Scholar 

  • Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Annu Rev Plant Physiol29: 345–378

    Article  CAS  Google Scholar 

  • Camara-Artigas A, Brune D, Allen JP (2002) Interactions between lipids and bacterial reaction centers determined by protein crystallography. Proc Nat Acad Sci USA99: 11055–11060

    Article  PubMed  CAS  Google Scholar 

  • Delphin E, Duval JC, Etienne AL, Kirilovsky D (1996) State transitions or ΔpH-dependent quenching of photosystem II fluorescence in red algae. Biochemistry35: 9435–9445

    Article  PubMed  CAS  Google Scholar 

  • Delrieu MJ (1998) Regulation of thermal dissipation of absorbed excitation energy and violaxanthin deepoxidation in the thylakoids ofLactuca sativa. Photoprotective mechanism of a population of photosystem II centers. Biochim Biophys Acta1363: 157–173

    Article  PubMed  CAS  Google Scholar 

  • Demeter S, Janda T, Kovacs L, Mende D, Wiessner W (1995) Effects ofin vivo CO2 depletion on electron transport and photoinhibition in the green algae,Chlamydobotrys stellata andChlamydomonas reinhardtii. Biochim Biophys Acta1229: 166–174

    Article  Google Scholar 

  • Demmig B, Winter K, Krüger A, Czygan F-C (1987) Photoinhibition and zeaxanthin formation in intact leaves: a possible role of the xanthophyll cycle in the dissipation of excess light. Plant Physiol84: 218–224

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta1020: 1–24

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol43: 599–626

    Article  CAS  Google Scholar 

  • Devault D, Govindjee (1990) Photosynthetic glow peaks and their relationship with the free-energy changes. Photosynth Res24: 175–181

    CAS  Google Scholar 

  • Dobrikova A, Taneva SG, Busheva M, Apostolova E, Petkanchin I (1997) Surface electric properties of thylakoid membranes fromArabidopsis thaliana mutants. Biophys Chem67: 239–244

    Article  PubMed  Google Scholar 

  • Doege M, Ohmann E, Tschiersch H (2000) Chlorophyll fluorescence quenching in the algaEuglena gracilis. Photosynth Res63: 159–170

    Article  PubMed  CAS  Google Scholar 

  • Dominici P, Caffarri S, Armenante F, Ceoldo S, Crimi M, Bassi R (2002) Biochemical properties of the psbS subunit of photosystem II either purified from chloroplast or recombinant. J Biol Chem277: 22750–22758

    Article  PubMed  CAS  Google Scholar 

  • Falkowski PG, Fujita Y, Ley A, Mauzerall D (1986) Evidence for cyclic electron flow around photosystem II inChlorella pyrenoidosa. Plant Physiol81: 310–312

    Article  PubMed  CAS  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science303: 1831–1838

    Article  PubMed  CAS  Google Scholar 

  • Field TS, Nedbal L, Ort DR (1998) Nonphotochemical reduction of the plastoquinone pool in sunflower leaves originates from chlororespiration. Plant Physiol116: 1209–1218

    Article  Google Scholar 

  • Finazzi G, Johnson GN, Dallosto L, Joliot P, Wollman F-A, Bassi R (2004) A zeaxanthin-independent nonphotochemical quenching mechanism localized in the photosystem II core complex. Proc Natl Acad Sci USA101: 12375–12380

    Article  PubMed  CAS  Google Scholar 

  • Fufenzan C, Rutherford AW, Krieger-Liszkay A (2002) Singlet oxygen production in herbicide-treated photosystem II. FEBS Lett532: 407–410

    Article  Google Scholar 

  • Funk C, Adamska I, Green BR, Andersson B, Renger G (1995a) The nuclear-encoded chlorophyll-binding photosystem II-S protein is stable in the absence of pigments. J Biol Chem270: 30141–30147

    Article  PubMed  CAS  Google Scholar 

  • Funk C, Schröder WP, Napiwotzki A, Tjus SE, Renger G, Andersson B (1995b) The PSII-S protein of higher plants: a new type of pigment-binding protein. Biochemistry34: 11133–11141

    Article  PubMed  CAS  Google Scholar 

  • Gilmore AM (1997) Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiol Plant99: 197–209

    Article  CAS  Google Scholar 

  • Gilmore AM, Ball MC (2000) Protection and storage of chlorophyll in overwintering evergreens. Proc Natl Acad Sci USA97: 11098–11101

    Article  PubMed  CAS  Google Scholar 

  • Gombos Z, Varkonyi Z, Hagio M, Iwaki M, Kovacs L, Masamoto K, Itoh S, Wada H (2002) Phosphatidylglycerol requirement for the function of electron acceptor plastoquinone QB in the photosystem II reaction center. Biochemistry41: 3796–3802

    Article  PubMed  CAS  Google Scholar 

  • Govindjee (1993) Bicarbonate-reversible inhibition of plastoquinone reductase in photosystem-II. Z Naturforsch48C: 251–258

    Google Scholar 

  • Grasses T, Pesaresi P, Schiavon F, Varotto C, Salamini F, Jahns P; Leister D (2002) The role of pH-dependent dissipation of excitation energy in protecting photosystem II against light-induced damage inArabidopsis thaliana. Plant Physiol Biochem40: 41–49

    Article  CAS  Google Scholar 

  • Greer DH, Berry JA, Björkman O (1986) Photoinhibition and photosynthesis in intact bean leaves: role of light and temperature, and requirement for chloroplast-protein synthesis during recovery. Planta168: 253–260

    CAS  Google Scholar 

  • Haldrup A, Jensen PE, Lunde C, Scheller HV (2001) Balance of power: a view of the mechanism of photosynthetic state transitions. Trends Plant Sci6: 301–305

    Article  PubMed  CAS  Google Scholar 

  • Harwood JL (1998) Involvement of chloroplast lipids in the reaction of plants submitted to stress.In P-A Siegenthaler, ed, Advances in photosynthesis and respiration. Lipids in photosynthesis: structure, function and genetics, Vol. VI. Kluwer Academic Publishers, Dordrecht, pp 287–302

    Google Scholar 

  • Hienerwadel R, Berthomieu C (1995) Bicarbonate binding to the non-heme iron of photosystem II investigated by Fourier transform infrared difference spectroscopy and13C-labeled bicarbonate. Biochemistry34: 16288–16297

    Article  PubMed  CAS  Google Scholar 

  • Hillmann B, Brettel K, van Mieghem F, Kamlowski A, Rutherford AW, Schlodder E (1995) Charge recombination reactions in photosystem-II. 2. Transient absorbency difference spectra and their temperature-dependence. Biochemistry34: 4814–4827

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol47: 655–684

    Article  PubMed  CAS  Google Scholar 

  • Huner NPA, Ivanov AG, Sane PV, Pocock T, Krol M, Balseris A, Rosso D, Savitch LV, Hurry VM, Öquist G (2006) Photoprotection of photosystem II: reaction centre quenching versus antenna quenching.In B Demming-Adams, WW Adamslll, AK Mattoo, eds, Advances in Photosynthesis and Respiration: Photoprotection, Photoinhibition, Gene Regulation and Environment, Vol. 21 Springer, Dordrecht, pp 155–173

    Chapter  Google Scholar 

  • Huner NPA, Öquist G, Hurry VM, Krol M, Falk S, Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res37: 19–39

    Article  CAS  Google Scholar 

  • Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci3: 224–230

    Article  Google Scholar 

  • Hurry VM, Huner NPA (1992) Effect of cold hardening on sensitivity of winter and spring wheat leaves to short-term photoinhibition and recovery of photosynthesis. Plant Physiol100: 1283–1290

    Article  PubMed  CAS  Google Scholar 

  • Hurry VM, Strand A, Tobiaeson M, Gardeström P, Öquist G (1995) Cold hardening of spring and winter wheat and rape results in differential effects on growth, carbon metabolism, and carbohydrate content. Plant Physiol109: 697–706

    PubMed  CAS  Google Scholar 

  • Ivanov AG, Sane P, Hurry V, Krol M, Sveshnikov D, Huner NPA, Öquist G (2003) Low-temperature modulation of the redox properties of the acceptor side of photosystem II: photoprotection through reaction centre quenching of excess energy. Physiol Plant119: 376–383

    Article  CAS  Google Scholar 

  • Ivanov AG, Sane PV, Zeinalov Y, Malmberg G, Gardeström P, Huner NPA, Öquist G (2001) Photosynthetic electron transport adjustments in overwintering Scots pine (Pinus sylvestris L). Planta213: 575–585

    Article  PubMed  CAS  Google Scholar 

  • Ivanov AG, Sane PV, Zeinalov Y, Simidjiev I, Huner NPA, Öquist G (2002) Seasonal responses of photosynthetic electron transport in Scots pine (Pinus sylvestris L.) studied by thermoluminescence. Planta215: 457–465

    Article  PubMed  CAS  Google Scholar 

  • Ivanov AG, Krol M, Apostolova EL, Morgan-Kiss RM, Naydenova N, Huner NPA, Sane PV (2005) Oligomerization state of LHCII modulates the redox properties of the acceptor side of photosystem II inCostata-2/133 mutant of pea. Physiol Mol Biol Plants11: 199–207

    CAS  Google Scholar 

  • Ivanov AG, Sane PV, Krol M, Gray GR, Balseris A, Savitch LV, Öquist G, Hüner NPA (2006). Acclimation to temperature and irradiance modulates PSII charge recombination. FEBS Lett580: 2797–2802

    Article  PubMed  CAS  Google Scholar 

  • Janda T, Szalai G, Paldi E (2000) Thermoluminescence investigation of low temperature stress in maize. Photosynthetica38: 635–639

    Article  Google Scholar 

  • Johnson GN, 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 Acta1229: 202–207

    Article  Google Scholar 

  • Jursinic P; Govindgee (1982) Effects of hydroxylamine and silico-molybdate on the decay in delayed light emission in the 6-100 microsecond range after a single 10 ns flash in pea thylakoids. Photosynth Res3: 161–177

    Article  CAS  Google Scholar 

  • Kim J-H, Kim S-J, Cho SH, Chow WS, Lee C-H (2005) Photosystem I acceptor side limitation is a prerequisite for the reversible decrease in the maximum extent of P700 oxidation after short-term chilling in the light in four plant species with different chilling sensitivities. Physiol Plant123: 100–107

    Article  CAS  Google Scholar 

  • Komenda J, Masojidek J (1998) The effect of photosystem II inhibitors DCMU and BNT on the high-light induced D1 turnover in two cyanobacterial strainsSynechocystis PCC 6803 andSynechococcus PCC 7942. Photosynth Res57: 193–202

    Article  CAS  Google Scholar 

  • Kozaki A, Takeba G (1996) Photorespiration protects C3 plants from photoinhibition. Nature384: 557–560

    Article  CAS  Google Scholar 

  • Krause GH (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol Plant74: 566–574

    Article  CAS  Google Scholar 

  • Krause GH, Jahns P (2003) Pulse amplitude modulated chlorophyll fluorometry and its application in plant science.In BR Green, WW Parson, eds, Advances in photosynthesis and respiration. Light harvesting antennae in photosynthesis, Vol. XIII. Kluwer Academic Publishers, Dordrecht, pp 373–399

    Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: The basics. Annu Rev Plant Physiol Plant Mol Biol42: 313–349

    Article  CAS  Google Scholar 

  • Krieger A, Moya I, Weis E (1992) Energy-dependent quenching of chlorophyll a fluorescence — effect of pH on stationary fluorescence and picosecond-relaxation kinetics in thylakoid membranes and photosystem-II preparations. Biochim Biophys Acta1102: 167–176

    Article  CAS  Google Scholar 

  • Krieger A, Rutherford AW (1997) Comparison of chloride-depleted and calcium-depleted PSII: The midpoint potential of QA and susceptibility to photodamage. Biochim Biophys Acta1319: 91–98

    Article  CAS  Google Scholar 

  • Krieger A, Rutherford AW, Johnson GN (1995) On the determination of redox midpoint potential of the primary quinone electron-acceptor, Qa, in Photosystem-II. Biochim Biophys Acta1229: 193–201

    Article  Google Scholar 

  • Krieger A, Weis E (1993) The role of calcium in the pH-dependent control of photosystem II. Photosynth Res37: 117–130

    Article  CAS  Google Scholar 

  • Krieger A, Weis E, Demeter S (1993) Low-pH induced Ca2+ 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 Acta1144: 411–418

    Article  CAS  Google Scholar 

  • 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. Biochemistry37: 17339–17344

    Article  PubMed  CAS  Google Scholar 

  • Kruse O, Hankamer B, Konczak C, Gerle C, Morris E, Radunz A, Schmid GH, Barber J (2000) Phosphatidylglycerol is involved in the dimerization of photosystem II. J Biol Chem275: 6509–6514

    Article  PubMed  CAS  Google Scholar 

  • Kruse O, Schmid GH (1995) The role of phosphatidylglycerol as a functional effector and membrane anchor of the D1 core peptide from photosystem II particles of the cyanobacteriumOscillatoria chalybea. Z Naturforsch50C: 380–390

    Google Scholar 

  • Kruse O, Zheleva D, Barber J (1997) Stabilization of photosystem two dimers by phosphorylation: Implication for the regulation of the turnover of D1 protein. FEBS Lett408: 276–280

    Article  PubMed  CAS  Google Scholar 

  • Kühlbrandt W, Wang DN, Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature367: 614–621

    Article  PubMed  Google Scholar 

  • Lee HY, Hong YN, Chow WS (2001) Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbours inCapsicum annuum L. leaves. Planta212: 332–342

    Article  CAS  Google Scholar 

  • Li X-P; Björkman O, Shin C, Grossman A, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature403: 391–395

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Napiwotzki A, Eckert H-J, Eichler HJ, Renger G (1993) Studies on the recombination kinetics of the radical pair P680+Pheo- in isolated PSII core complexes from spinach. Biochim Biophys Acta1142: 129–138

    Article  CAS  Google Scholar 

  • Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol45: 633–642

    Article  CAS  Google Scholar 

  • Los DA, Murata N (2002) Sensing and responses to low temperature in cyanobacteria.In KB Storey, JM Storey, eds, Sensing, signalling and cell adaptation, Elsevier Science BV, Amsterdam, pp 139–153

    Chapter  Google Scholar 

  • Lunde C, Jensen PE, Haldrup A, Knoetzel J, Scheller HV (2000) The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature408: 613–615

    Article  PubMed  CAS  Google Scholar 

  • Mäenpää P, Miranda T, Tyystjarvi E, Tyystjarvi T, Govindjee, Ducruet JM, Etienne AL, Kirilovsky D (1995) A mutation in the D-Ioop of D1 modifies the stability of the S2QA - and S2Qb - states in photosystem-II. Plant Physiol107: 187–197

    PubMed  Google Scholar 

  • Matsubara S, Chow WS (2004) Populations of photo in activated photosystem II reaction centers characterized by chlorophyll a fluorescence lifetimein vivo. Proc Natl Acad Sci USA101: 18234–18239

    Article  PubMed  CAS  Google Scholar 

  • Mattoo AK, Elich TD, Ghirardi ML, Callahan FE, Edelman M (1993) Post-translational modification of chloroplast proteins and the regulation of protein turnover.In NH Battey, HG Dickinson, AM Hetherington, eds, Post-translational modification in plants, Vol. 53. Cambridge University Press, Cambridge, pp 65–78

    Google Scholar 

  • Melis A (1999) Photosystem II damage and repair cycle in chloroplasts: what modulates the rate of photodamagein vivo? Trends Plant Sci4: 130–135

    Article  PubMed  Google Scholar 

  • Messinger J, Seaton G, Wydrzynski T, Wacker U, Renger G (1997) S-3 state of the water oxidase in photosystem II. Biochemistry36: 6862–6873

    Article  PubMed  CAS  Google Scholar 

  • Milligan G, Parenti M, Magee AI (1995) The dynamic role of palmitoylation in signal transduction. Trends Biochem Sci20: 256–256

    Article  CAS  Google Scholar 

  • Minagawa J, Narusaka Y, Inoue Y, Satoh K (1999) Electron transfer between QA and QB in photosystem II is thermodynamically perturbed in phototolerant mutants ofSynechocystis sp. PCC 6803. Biochemistry38: 770–775

    Article  PubMed  CAS  Google Scholar 

  • Miyake C, Yokota A (2001) Cyclic flow of electrons within PSII in thylakoid membranes. Plant Cell Physiol42: 508–515

    Article  PubMed  CAS  Google Scholar 

  • Miyake C, Yonekura K, Kobayashi Y, Yokota A (2002) Cyclic electron flow within PSII functions in intact chloroplasts from spinach leaves. Plant Cell Physiol43: 951–957

    Article  PubMed  CAS  Google Scholar 

  • Nield J, Funk C, Barber J (2000) Supermolecular structure of photosystem II and location of the PsbS protein. Phil Trans Royal Soc London Ser B-Biol Sci355: 1337–1343

    Article  CAS  Google Scholar 

  • Nishida I, Murata N (1996) Chilling sensitivity in plants and cyano-bacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol47: 541–568

    Article  PubMed  CAS  Google Scholar 

  • Nixon PJ, Komenda J, Barber J, Deak Z, Vass I, Diner BA (1995) Deletion of the Pest-like region of photosystem 2 modifies the QB-binding pocket but does not prevent rapid turnover of D1. J Biol Chem270: 14919–14927

    Article  PubMed  CAS  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: Genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol50: 333–359

    Article  PubMed  CAS  Google Scholar 

  • Ohad I, Hirschberg J (1992) Mutations in the D1 subunit of photosystem II distinguish between quinone and herbicide binding sites. Plant Cell4: 273–282

    Article  PubMed  CAS  Google Scholar 

  • Olaizola M, Laroche J, Kolber Z, Falkowski PG (1994) Nonphoto-chemical fluorescence quenching and the diadinoxanthin cycle in a marine diatom. Photosynth Res41: 357–370

    Article  CAS  Google Scholar 

  • Olaizola M, Yamamoto HY (1994) Short-term response of the diadinoxanthin cycle and fluorescence yield to high irradiance inChaetoceros muelleri (Bacillariophyceae). J Phycol30: 606–612

    Article  CAS  Google Scholar 

  • Öquist G, Chow WS, Anderson JM (1992) Photoinhibition of photosynthesis represents a mechanism for long-term regulation of photosystem II. Planta186: 450–460

    Article  Google Scholar 

  • Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Annu Rev Plant Biol54: 329–355

    Article  PubMed  CAS  Google Scholar 

  • Ort DR (2001) When there is too much light. Plant Physiol125: 29–32

    Article  PubMed  CAS  Google Scholar 

  • Ort DR, Baker NR (2002) A photo protective role for O2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol5: 193–198

    Article  PubMed  CAS  Google Scholar 

  • Osmond, B (1981) Photorespiration and photoinhibition: some implications for the energetics of photosynthesis. Biochim Biophys Acta639: 77–98

    CAS  Google Scholar 

  • Pali T, Garab G, Horvath LI, Kota Z (2003) Functional significance of the lipid-protein interface in photosynthetic membranes. Cell Mol Life Sci60: 1591–1606

    Article  PubMed  CAS  Google Scholar 

  • Peterson RB, Havir EA (2001) Photosynthetic properties of anArabidopsis thaliana mutant possessing a defective PsbS gene. Planta214: 142–152

    Article  PubMed  CAS  Google Scholar 

  • Peterson RB, Havir EA (2003) Contrasting modes of regulation of PSII light utilization with changing irradiance in normal and PsbS mutant leaves ofArabidopsis thaliana. Photosynth Res75: 57–70

    Article  PubMed  CAS  Google Scholar 

  • Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol35: 15–44

    Article  CAS  Google Scholar 

  • Prasil O, Kolber Z, Berry JA, Falkowski PG (1996) Cyclic electron flow around photosystem IIin vivo. Photosynth Res48: 395–410

    Article  CAS  Google Scholar 

  • Quigg A, Beardall J, Wydrzynski T (2003) Photoacclimation involves modulation of the photosynthetic oxygen-evolving reactions inDunaliella tertiolecta andPhaeodactylum tricornutum. Funct Plant Biol30: 301–308

    Article  Google Scholar 

  • Quiles MJ (2006) Stimulation of chlororespiration by heat and high light intensity in oat plants. Plant Cell Environ29: 1463–1470

    Article  PubMed  CAS  Google Scholar 

  • Reifarth F, Christen G, Seeliger AG, Dormann F; Benning C, Renger G (1997) Modification of the water oxidizing complex in leaves of thedgd1 mutant ofArabidopsis thaliana deficient in the galactolipid digalactosyldiacylglycerol. Biochemistry36: 11769–11776

    Article  PubMed  CAS  Google Scholar 

  • Richter M, Goss R, Wagner B, Holzwarth AR (1999) Characterization of the fast and slow reversible components of non-photochemical quenching in isolated pea thylakoids by picosecond time-resolved chlorophyll fluorescence analysis? Biochemistry38: 12718–12726

    Article  PubMed  CAS  Google Scholar 

  • Rintamärki E, Aro E-M (2001) Phosphorylation of photosystem II proteins.In E-M Aro, B Andersson, eds, Advances in photosynthesis and respiration, Vol. XI. Kluwer Academic Publishers, Dordrecht, pp 395–418

    Google Scholar 

  • Rinyu L, Martin EW, Takahashi E, Maroti P, Wraight CA (2004) Modulation of the free energy of the primary acceptor (QA) in reaction centers fromRhodobacter sphaeroides: contributions from protein and protein-lipid (cardiolipin) interactions. Biochim Biophys Acta1655: 93–101

    Article  PubMed  CAS  Google Scholar 

  • Rosso D, Ivanov AG, Fu A, Geisler-Lee J, Hendrickson1 L, Geisler M, Stewart G, Krol M, Hurry V, Rodermel SR, Maxwell DP, Hüner NPA (2006) IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatusof Arabidopsis thaliana during steady state photosynthesis. Plant Physiol142: 574–585

    Article  PubMed  CAS  Google Scholar 

  • Ruban AV, Pascal AA, Robert B, Horton P (2002) Activation of zeaxanthin is an obligatory event in the regulation of photosynthetic light harvesting. J Biol Chem277: 7785–7789

    Article  PubMed  CAS  Google Scholar 

  • Sakurai I, Hagio M, Gombos Z, Tyystjarvi T, Paakkarinen V, Aro EM, Wada H (2003) Requirement of phosphatidylglycerol for maintenance of photosynthetic machinery. Plant Physiol133: 1376–1384

    Article  PubMed  CAS  Google Scholar 

  • 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-acclimatedArabidopsis. Plant Physiol132: 2144–2151

    Article  PubMed  CAS  Google Scholar 

  • Sane PV, Ivanov AG, Sveshnikov D, Huner NPA, Öquist G (2002) A transient exchange of the photosystem II reaction center protein D1:1 with D1:2 during low temperature stress ofSynechococcus sp PCC 7942 in the light lowers the redox potential of QB. J Biol Chem277: 32739–32745

    Article  PubMed  CAS  Google Scholar 

  • Schatz GH, Brock H, Holzwarth AR (1988) Kinetic and energetic model for the primary processes in photosystem II. Biophys J54: 397–405

    Article  CAS  PubMed  Google Scholar 

  • Schmid GH, Bader KP, Schulder R (1994) A study on the life time of the S-3-state in the filamentous cyanobacteriumOscillatoria chalybea. Z Naturforsch49C: 108–114

    Google Scholar 

  • Schreiber U, Krieger A (1996) Two fundamentally different types of variable chlorophyll fluorescencein vivo. FEBS Lett397: 131–135

    Article  PubMed  CAS  Google Scholar 

  • Schreiber U, Neubauer C (1990) O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth Res25: 279–293

    Article  CAS  Google Scholar 

  • Schweitzer RH, Brudvig GW (1997) Fluorescence quenching by chlorophyll cations in photosystem II. Biochemistry36: 11351–11359

    Article  PubMed  CAS  Google Scholar 

  • Sebban P, Parot P, Baciou L, Mathis P, Vermeglio A (1991) Effects of low temperature and lipid rigidity on the charge recombination process inRps. Viridis andRb. sphaeroides reaction centres. Biochim Biophys Acta1057: 109–114

    Article  CAS  Google Scholar 

  • Shatz GH, Brock H, Holzwarth AR (1988) Kinetic and energetic model for the primary processes in photosystem II. Biophys J54: 397–405

    Article  Google Scholar 

  • Somersalo S, Krause GH (1990) Reversible photoinhibition of unhardened and cold-acclimated spinach leaves at chilling temperatures. Planta180: 181–187

    Article  CAS  Google Scholar 

  • Stewart DH, Cua A, Chisholm DA, Diner BA, Bocian DF, Brudvig GW (1998) Identification of histidine 118 in the D1 polypeptide of photosystem II as the axial ligand to chlorophyll Z. Biochemistry37: 10040–10046

    Article  PubMed  CAS  Google Scholar 

  • Stitt M, Hurry V (2002) A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation inArabidopsis. Curr Opin Plant Biol5: 199–206

    Article  PubMed  CAS  Google Scholar 

  • Strand Å, Foyer CH, Gustafsson P, Gardeström P, Hurry V (2003) Altering flux through the sucrose biosynthesis pathway in transgenicArabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance. Plant Cell Environ26: 523–535

    Article  CAS  Google Scholar 

  • Strand Å, Hurry V, Gustafsson P, Gardeström P (1997) Development ofArabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant J12: 605–614

    Article  PubMed  CAS  Google Scholar 

  • Streb P, Josse E-M, Gallouet E, Baptist F, Kuntz M, Cornic G (2005) Evidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain plant speciesRanunculus glacialis. Plant Cell Environ28: 1123–1135

    Article  CAS  Google Scholar 

  • Takahashi Y, Hansson O, Mathis P, Satoh K (1987) Primary radical pair in the photosystem II reaction center. Biochim Biophys Acta893: 49–59

    Article  CAS  Google Scholar 

  • Taly A, Baciou L, Sebban P (2002) The DMPC lipid phase transition influences differently the first and the second electron transfer reactions in bacterial reaction centers. FEBS Lett532: 91–96

    Article  PubMed  CAS  Google Scholar 

  • Telfer A, Dhami S, Bishop SM, Phillips D, Barber J (1994) β -carotene quenches singlet oxygen formed by isolated photosystem II reaction centers. Biochemistry33: 14469–14474

    Article  PubMed  CAS  Google Scholar 

  • Telfer A, Rivas JD, Barber J (1991) β -carotene within the isolated photosystem-11 reaction center — photooxidation and irreversible bleaching of this chromophore by oxidized P680. Biochim Biophys Acta1060: 106–114

    Article  CAS  Google Scholar 

  • Thompson LK, Brudvig GW (1988) Cytochromeb 559 may function to protect photosystem II from photoinhibition. Biochemistry27: 6653–6658

    Article  PubMed  CAS  Google Scholar 

  • Tschiersch H, Ohmann E, Doege M (2002) Modification of the thylakoid structure ofEuglena gracilis by norflurazon-treatment: consequences for fluorescence quenching. Environ Exp Bot47: 259–270

    Article  CAS  Google Scholar 

  • van Mieghem F, Brettel K, Hillmann B, Kamlowski A, Rutherford AW, Schlodder E (1995) Charge recombination reactions in photosystem II. 1. Yields, recombination pathways, and kinetics of the primary pair. Biochemistry34: 4798–4813

    Article  PubMed  Google Scholar 

  • Vass I, Styring S, Hundal T, Koivuniemi A, Aro E-M, Andersson B (1992) Reversible and irreversible intermediates during photo-inhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci USA89: 1408–1412

    Article  PubMed  CAS  Google Scholar 

  • Vavilin DV, Vermaas WFJ (2000) Mutations in the CD-loop region of the D2 protein in Synechocystis sp PCC 6803 modify charge recombination pathways in photosystem IIin vivo. Biochemistry39: 14831–14838

    Article  PubMed  CAS  Google Scholar 

  • Wagner B, Goss R, Richter M, Wild A, Holzwarth AR (1996) Picosecond time-resolved study on the nature of high-energy-state quenching in isolated pea thylakoids — Different localization of zeaxanthin dependent and independent quenching mechanisms. J Photochem Photobiol B36: 339–350

    Article  CAS  Google Scholar 

  • Walters RG, Horton P (1993) Theoretical assessment of alternative mechanisms for non-photochemical quenching of PSII fluorescence in barley leaves. Photosynth Res36: 119–139

    Article  CAS  Google Scholar 

  • Wedel, N, Klein R, Ljungderg U, Andersson B, Herrmann RC (1992) The single copy gene PsbS codes foe a phylogenetically intriguing 22 kDa polypeptide of photosystem II. FEBS Lett314: 61–66

    Article  PubMed  CAS  Google Scholar 

  • Weis E, Berry JA (1987) Quantum efficiency of photosystem II in relation to ‘energy’-dependent quenching of chlorophyll fluorescence. Biochim Biophys Acta894: 198–207

    Article  CAS  Google Scholar 

  • Woodbury NW, Parson WW, Gunner MR, Prince RC, Dutton PL (1986) Radical-pair energetics and decay mechanisms in reaction centers containing anthraquinones, naphtoquinones or benzoquinones in place of ubiquinone. Biochim Biophys Acta851: 6–22

    Article  PubMed  CAS  Google Scholar 

  • Xu CC, Jeon YA, Lee C-H (1999) Relative contributions of photochemical and non-photochemical routes to excitation energy dissipation in rice and barley illuminated at a chilling temperature. Physiol Plant107: 447–453

    Article  CAS  Google Scholar 

  • Zulfugarov IS, Ham O-K, Misra SR, Kim J-Y, Nath K, Koo H-Y, Kim H-S, Lee C-H (2007) Dependence of reaction center-type energy-dependent quenching on photosystem II antenna size. Biochim Biophys Acta1767: 773–780

    Article  PubMed  CAS  Google Scholar 

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Ivanov, A.G., Hurry, V., Sane, P.V. et al. Reaction centre quenching of excess light energy and photoprotection of photosystem II. J. Plant Biol. 51, 85–96 (2008). https://doi.org/10.1007/BF03030716

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