Skip to main content
Log in

Singlet oxygen production in photosystem II and related protection mechanism

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

High-light illumination of photosynthetic organisms stimulates the production of singlet oxygen by photosystem II (PSII) and causes photo-oxidative stress. In the PSII reaction centre, singlet oxygen is generated by the interaction of molecular oxygen with the excited triplet state of chlorophyll (Chl). The triplet Chl is formed via charge recombination of the light-induced charge pair. Changes in the midpoint potential of the primary electron donor P680 of the primary acceptor pheophytin or of the quinone acceptor QA, modulate the pathway of charge recombination in PSII and influence the yield of singlet oxygen formation. The involvement of singlet oxygen in the process of photoinhibition is discussed. Singlet oxygen is efficiently quenched by β-carotene, tocopherol or plastoquinone. If not quenched, it can trigger the up-regulation of genes, which are involved in the molecular defence response of photosynthetic organisms against photo-oxidative stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

Chl:

Chlorophyll

DCMU:

3-(3,4-Dichlorophenyl)-1,1-dimethylurea

Fv :

Variable fluorescence

Fm :

Maximal fluorescence

P680 :

Primary electron donor in PSII

QA :

Primary quinone electron acceptor in PSII

QB :

Secondary quinone electron acceptor in PSII

Ph:

Pheophytin—primary electron acceptor

PSII:

Photosystem II

References

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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  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 Acta 1319:91–98. doi:10.1016/S0005-2728(96)00117-X

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  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. Biochemistry 37:17339–17344. doi:10.1021/bi9822628

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    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-acclimated Arabidopsis. Plant Phys 132:2144–2151

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    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 reaction pathways in photosystem II in vivo. Biochemistry 39:14831–14838

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Diana Kirilovsky (CEA Saclay) for providing the data for Fig. 4 and Bill Rutherford, Arezki Sedoud (both CEA Saclay) and Giles Johnson (University of Manchester) for scientific discussions and critical reading of the manuscript. Financial support by the Alexander von Humboldt foundation to C.F. and by the Deutsche Forschungsgemeinschaft via SFB 480 to AT is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anja Krieger-Liszkay.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Krieger-Liszkay, A., Fufezan, C. & Trebst, A. Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98, 551–564 (2008). https://doi.org/10.1007/s11120-008-9349-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-008-9349-3

Keywords

Navigation