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Inhibition of the repair of Photosystem II by oxidative stress in cyanobacteria

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Abstract

The activity of Photosystem II (PS II) is severely restricted by a variety of environmental factors and, under environmental stress, is determined by the balance between the rate of damage to PS II and the rate of the repair of damaged PS II. The effects of oxidative stress on damage and repair can be examined separately, and it appears that, while light can damage PS II directly, oxidative stress acts primarily by inhibiting the repair of PS II. Studies in cyanobacteria have demonstrated that oxidative stress suppresses the de novo synthesis of proteins, in particular, the D1 protein, which is required for the repair of PS II.

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Abbreviations

Chl:

chlorophyll

DCMU:

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

P680:

primary electron donor in PS II

PS II:

Photosystem II

QA:

the primary electron acceptor of PS II

QB:

the secondary electron acceptor of PS II

ROS:

reactive oxygen species

References

  • SI Allakhverdiev N Murata (2004) ArticleTitleEnvironmental stress inhibits the synthesis de novo of D1 protein in the photodamage-repair cycle of Photosystem II in Synechocystis sp. PCC 6803 Biochim Biophys Acta 1657 23–32 Occurrence Handle15238209

    PubMed  Google Scholar 

  • SI Allakhverdiev Y Nishiyama S Miyairi H Yamamoto N Inagaki Y Kanesaki N Murata (2002) ArticleTitleSalt stress inhibits the repair of photodamaged Photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis Plant Physiol 130 1443–1453 Occurrence Handle12428009

    PubMed  Google Scholar 

  • PR Anbudurai TS Mor I Ohad SV Shestakov HB Pakrasi (1994) ArticleTitleThe ctpA gene encodes the C-terminal processing protease for the D1 protein of the Photosystem II reaction center Proc Natl Acad Sci USA 91 8082–8086 Occurrence Handle8058761

    PubMed  Google Scholar 

  • JM Anderson (2001) ArticleTitleDoes functional Photosystem II complex have an oxygen channel FEBS Lett 488 1–4 Occurrence Handle11163784

    PubMed  Google Scholar 

  • B. Andersson E-M. Aro (2001) Photodamage and D1 protein turnover in Photosystem II E-M. Aro B. Andersson (Eds) Regulation of Photosynthesis Kluwer Academic Publishers Dordrecht, The Netherlands 377–393

    Google Scholar 

  • E-M Aro I Virgin B Andersson (1993) ArticleTitlePhotoinhibition of Photosystem II. Inactivation, protein damage and turnover Biochim Biophys Acta 1143 113–134 Occurrence Handle8318516

    PubMed  Google Scholar 

  • B Arntz A Trebst (1986) ArticleTitleOn the role of the QB protein of Photosystem II in photoinhibition FEBS Lett 194 43–49 Occurrence Handle10.1016/0014-5793(86)80048-5

    Article  Google Scholar 

  • K Asada (1999) ArticleTitleThe water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons Annu Rev Plant Physiol Plant Mol Biol 50 601–639 Occurrence Handle15012221

    PubMed  Google Scholar 

  • A Ayala J Parrado M Bougria A Machado (1996) ArticleTitleEffect of oxidative stress, produced by cumene hydroperoxide, on the various steps of protein synthesis J Biol Chem 271 23105–23110 Occurrence Handle8798501

    PubMed  Google Scholar 

  • C Baffert MN Collomb A Deronzier J Pecaut J Limburg RH Crabtree GW Brudvig (2002) ArticleTitleTwo new terpyridine dimanganese complexes: a manganese (III,III) complex with a single unsupported oxo bridge and a manganese (III,IV) complex with a dioxo bridge. Synthesis, structure, and redox properties Inorg Chem 41 1404–1411 Occurrence Handle11896708

    PubMed  Google Scholar 

  • J Berry O Björkman (1980) ArticleTitlePhotosynthetic response and adaptation to temperature in higher plants Ann Rev Plant Physiol 31 491–543 Occurrence Handle10.1146/annurev.pp.31.060180.002423

    Article  Google Scholar 

  • FE Callahan DW Becker GM Cheniae (1986) ArticleTitleStudies on the photoinactivation of the water-oxidizing enzyme. II. Characterization of weak-light photoinhibition of PS II and its light-induced recovery Plant Physiol 82 261–269

    Google Scholar 

  • G-X Chen J Kazimir GM Cheniae (1992) ArticleTitlePhotoinhibition of hydroxylamine-extracted Photosystem II membranes: studies of the mechanism Biochemistry 31 11072–11083 Occurrence Handle1332749

    PubMed  Google Scholar 

  • SK Chung J Jung (1995) ArticleTitleInactivation of the acceptor side and degradation of the D1 protein of Photosystem II by singlet oxygen photogenerated from the outside Photochem Photobiol 61 383–389

    Google Scholar 

  • RE Cleland (1988) ArticleTitleMolecular events of photoinhibitory inactivation in the reaction centre of Photosystem II Aus J Plant Physiol 15 135–150

    Google Scholar 

  • S Demeter PJ Neale A Melis (1987) ArticleTitlePhotoinhibition: impairment of the primary charge separation between P680 and pheophytin in PS II of chloroplasts FEBS Lett 214 370–374 Occurrence Handle10.1016/0014-5793(87)80090-X

    Article  Google Scholar 

  • B Demmig-Adams WW Adams SuffixIII (1992) ArticleTitlePhotoprotection and other responses of plants to high-light stress Ann Rev Plant Physiol Plant Mol Biol 43 599–626 Occurrence Handle10.1146/annurev.pp.43.060192.003123

    Article  Google Scholar 

  • S Dukan T Nyström (1999) ArticleTitleOxidative stress defense and deterioration of growth-arrested Escherichia coli cells J Biol Chem 274 26027–26032 Occurrence Handle10473549

    PubMed  Google Scholar 

  • T Hirose M Sugiura (1996) ArticleTitleCis-acting elements and trans-acting factors for accurate translation of chloroplast psbA mRNAs: development of an in vitro translation system from tobacco chloroplasts EMBO J 15 1687–1695 Occurrence Handle8612593

    PubMed  Google Scholar 

  • LW Jones B Kok (1966) ArticleTitlePhotoinhibition of chloroplast reactions. I. Kinetics and action spectra Plant Physiol 41 1037–1043

    Google Scholar 

  • J Jung HS Kim (1990) ArticleTitleThe chromophores as endogenous sensitizers involved in the photogeneration of singlet oxygen in spinach thylakoids Photochem Photobiol 52 1003–1009

    Google Scholar 

  • N Keren A Berg PJM Kan Particlevan H Levanon I Ohad (1997) ArticleTitleMechanism of Photosystem II photoinactivation and D1 protein degradation at low light: the role of back electron flow Proc Natl Acad Sci USA 94 1579–1584 Occurrence Handle11038602

    PubMed  Google Scholar 

  • VV Klimov SI Allakhverdiev S Demeter AA Krasnovsky (1979) ArticleTitlePhotoreduction of pheophytin in the Photosystem II of chloroplasts depending on the oxidation-reduction potential of the medium Dokl Acad Nauk USSR 249 227–230

    Google Scholar 

  • VV Klimov MA Shafiev SI Allakhverdiev (1990) Photoinactivation of the reactivation capacity of Photosystem II in pea subchloroplast particles after a complete removal of manganese Photosynth Res 23 59–65

    Google Scholar 

  • JP Knox AD Dodge (1985) ArticleTitleSinglet oxygen and plants Phytochemistry 24 889–896 Occurrence Handle10.1016/S0031-9422(00)83147-7

    Article  Google Scholar 

  • HY Lee YN Hong WS Chow (2001) ArticleTitlePhotoinactivation of Photosystem II complex and photoprotection by non-functional neighbours in Capsicum annuum L. leaves Planta 212 332–342 Occurrence Handle11289597

    PubMed  Google Scholar 

  • AK Mattoo H Hoffman-Falk JB Marder M Edelman (1984) ArticleTitleRegulation of protein metabolism: coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes Proc Natl Acad Sci USA 81 1380–1384

    Google Scholar 

  • A Melis (1999) ArticleTitlePhotosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci 4 130–135 Occurrence Handle10322546

    PubMed  Google Scholar 

  • BY Moon S Higashi Z Gombos N Murata (1995) ArticleTitleUnsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants Proc Natl Acad Sci USA 92 6219–6223 Occurrence Handle7603975

    PubMed  Google Scholar 

  • Y Nishiyama H Yamamoto SI Allakhverdiev M Inaba A Yokota N Murata (2001) ArticleTitleOxidative stress inhibits the repair of photodamage to the photosynthetic machinery EMBO J 20 5587–5594 Occurrence Handle11598002

    PubMed  Google Scholar 

  • Y Nishiyama SI Allakhverdiev H Yamamoto H Hayashi N Murata (2004) ArticleTitleSinglet oxygen inhibits the repair of Photosystem II by suppressing translation elongation of the D1 protein in Synechocystis sp. PCC 6803 Biochemistry 43 11321–11330 Occurrence Handle15366942

    PubMed  Google Scholar 

  • I Ohad DJ Kyle CJ Arntzen (1984) ArticleTitleMembrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptide in chloroplast membranes J Cell Biol 99 481–485 Occurrence Handle6378924

    PubMed  Google Scholar 

  • SB Powles (1984) ArticleTitlePhotoinhibition of photosynthesis induced by visible light Annu Rev Plant Physiol 35 15–44 Occurrence Handle10.1146/annurev.pp.35.060184.000311

    Article  Google Scholar 

  • I Setlik SI Allakhverdiev L Nedbal E Setlikova VV Klimov (1990) ArticleTitleThree types of Photosystem II photoinactivation: I. Damaging processes on the acceptor side Photosynth Res 23 39–48 Occurrence Handle10.1007/BF00030061

    Article  Google Scholar 

  • J Tamarit E Cabiscol J Ros (1998) ArticleTitleIdentification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress J Biol Chem 273 3027–3032 Occurrence Handle9446617

    PubMed  Google Scholar 

  • SM Theg LJ Filar RA Dilley (1986) ArticleTitlePhotoinactivation of chloroplasts already inhibited on the oxidizing side of Photosystem II Biochim Biophys Acta 849 104–111

    Google Scholar 

  • T Trebitsh A Danon (2001) ArticleTitleTranslation of chloroplast psbA mRNA is regulated by signals initiated by both photosystems II and I Proc Natl Acad Sci USA 21 12289–12294 Occurrence Handle10.1073/pnas.211440698

    Article  Google Scholar 

  • E Tyystjärvi E-M Aro (1996) ArticleTitleThe rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity Proc Natl Acad Sci USA 93 2213–2218 Occurrence Handle11607639

    PubMed  Google Scholar 

  • Tyystjärvi E, Kairavuo M, Pätsikkä E, Keränen M, Khriachtchev L, Tuominen I, Guiamet JJ and Tyystjärvi T (2001) The quantum yield of photoinhibition is the same in flash light and under continuous illumination: implication for the mechanism. In: Critchley C (ed) Proceedings of the 12th International Congress of Photosynthesis, S8-P032. CSIRO Publishing, Melbourne, Australia.

  • T Tyystjärvi I Tuominen M Herranen E-M Aro E Tyystjärvi (2002) ArticleTitleAction spectrum of psbA gene transcription is similar to that of photoinhibition in Synechocystis sp PCC 6803 IssueIDFEBS Lett 516 167–171

    Google Scholar 

  • I Vass S Styring T Hundal A Koivuniemi E-M Aro B Andersson (1992) ArticleTitleThe reversible and irreversible intermediates during photoinhibition of Photosystem II: stable reduced QA species promote chlorophyll triplet formation Proc Natl Acad Sci USA 89 1408–1412 Occurrence Handle11607279

    PubMed  Google Scholar 

  • H Wada Z Gombos N Murata (1994) ArticleTitleContribution of membrane lipids to the ability of the photosynthetic machinery to tolerate temperature stress Proc Natl Acad Sci USA 91 4273–4277 Occurrence Handle11607472

    PubMed  Google Scholar 

  • CB Yohn A Cohen A Danon SP Mayfield (1996) ArticleTitleAltered mRNA binding activity and decreased translation initiation in a nuclear mutant lacking translation of the chloroplast psbA mRNA Mol Cell Biol 16 3560–3566 Occurrence Handle8668172

    PubMed  Google Scholar 

  • L Zhang V Paakkarinen KJ Wijk Particlevan E-M Aro (2000) ArticleTitleBiogenesis of the chloroplast-encoded D1 protein: regulation of translation elongation, insertion, and assembly into Photosystem II Plant Cell 12 1769–1781 Occurrence Handle11006346

    PubMed  Google Scholar 

  • L Zolla S Rinalducci (2002) ArticleTitleInvolvement of active oxygen species in degradation of light-harvesting proteins under light stresses Biochemistry 41 14391–14402 Occurrence Handle12450406

    PubMed  Google Scholar 

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Correspondence to Yoshitaka Nishiyama.

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Nishiyama, Y., Allakhverdiev, S.I. & Murata, N. Inhibition of the repair of Photosystem II by oxidative stress in cyanobacteria. Photosynth Res 84, 1–7 (2005). https://doi.org/10.1007/s11120-004-6434-0

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