Skip to main content
Log in

Application of low temperatures during photoinhibition allows characterization of individual steps in photodamage and the repair of photosystem II

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

Abstract

Recent investigations of photoinhibition have revealed that photodamage to photosystem II (PSII) involves two temporally separated steps: the first is the inactivation of the oxygen-evolving complex by light that has been absorbed by the manganese cluster and the second is the impairment of the photochemical reaction center by light that has been absorbed by chlorophyll. Our studies of photoinhibition in Synechocystis sp. PCC 6803 at various temperatures demonstrated that the first step in photodamage is not completed at low temperatures, such as 10°C. Further investigations suggested that an intermediate state, which is stabilized at low temperatures, might exist at the first stage of photodamage. The repair of PSII involves many steps, including degradation and removal of the D1 protein, synthesis de novo of the precursor to the D1 protein, assembly of the PSII complex, and processing of the precursor to the D1 protein. Detailed analysis of photodamage and repair at various temperatures has demonstrated that, among these steps, only the synthesis of the precursor to D1 appears to proceed at low temperatures. Investigations of photoinhibition at low temperatures have also indicated that prolonged exposure of cyanobacterial cells or plant leaves to strong light diminishes their ability to repair PSII. Such non-repairable photoinhibition is caused by inhibition of the processing of the precursor to the D1 protein after prolonged illumination with strong light at low temperatures.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

DCIP:

Dichlorophenol indophenol

DPC:

Diphenyl carbazide

OEC:

Oxygen-evolving complex

preD1:

Precursor to the D1 protein

RC:

Reaction center

ROS:

Reactive oxygen species

References

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

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1657:23–32

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Mohanty P, Murata N (2003) Dissection of photodamage at low temperature and repair in darkness suggests the existence of an intermediate form of photodamaged photosystem II. Biochemistry 42:14277–14283

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Nishiyama Y, Takahashi S, Miyairi S, Suzuki I, Murata N (2005a) Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem II in Synechocystis. Plant Physiol 137:263–273

    Article  PubMed  CAS  Google Scholar 

  • Allakhverdiev SI, Tsvetkova N, Mohanty P, Szalontai, Moon BY, Debreczeny M, Murata N (2005b) Irreversible photoinhibition of photosystem II is caused by exposure of Synechocystis cells to strong light for a prolonged period. Biochim Biophys Acta 1708:342–351

    Article  PubMed  CAS  Google Scholar 

  • Andersson B, Aro E-M (2001) Photodamage and D1 protein turnover in photosystem II. In: Aro E-M, Andersson B (eds) Regulation of photosynthesis. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 377–393

    Google Scholar 

  • Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    Article  PubMed  CAS  Google Scholar 

  • Baffert C, Collomb MN, Deronzier A, Pecaut J, Limburg J, Crabtree RH, Brudvig G (2002) Two 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

    Article  PubMed  CAS  Google Scholar 

  • Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66

    Article  PubMed  CAS  Google Scholar 

  • Barker M, de Vries R, Nield J, Komenda J, Nixon PJ (2006) The Deg proteases protect Synechocystis sp. PCC 6803 during heat and light stresses but are not essential for removal of damaged D1 protein during the photosystem two repair cycle. J Biol Chem 281:30347–30355

    Article  PubMed  CAS  Google Scholar 

  • Carrell TG, Bourles E, Lin M, Dismukes GC (2003) Transition from hydrogen atom to hydride abstraction by Mn4O4(O2PPh2)6 versus [Mn4O4(O2PPh2)6]+: O–H bond dissociation energies and the formation of Mn4O3(OH)(O2PPh2)6. Inorg Chem 42:2849–2858

    Article  PubMed  CAS  Google Scholar 

  • Chow WS, Lee HY, He J, Hindrickson L, Hong YN, Matsubara S (2005) Photoinhibition in leaves. Photosynth Res 84:35–41

    Article  PubMed  CAS  Google Scholar 

  • Constant S, Eisenberg-Domovitch Y, Ohad I, Kirilovsky D (2000) Recovery of photosystem II activity in photoinhibited Synechocystis cells: light-dependent translation activity is required besides light-independent synthesis of the D1 protein. Biochemistry 79:2032–2041

    Article  CAS  Google Scholar 

  • Erickson JM (1998) Assembly of photosystem II. In: Rochaix J-D, Goldschmidt-Clermont M, Merchant S (eds) The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 255–285

    Google Scholar 

  • Giacometti GM, Barbato R, Chiaramonte S, Friso G, Rigoni F (1996) Effects of ultraviolet-B radiation on photosystem II of the cyanobacterium Synechocystis sp. PCC 6803. Eur J Biochem 242:799–806

    Article  PubMed  CAS  Google Scholar 

  • Hakala M, Tuominen I, Keränen M, Tyystjärvi T, Tyystjärvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochim Biophys Acta 1706:68–80

    Article  PubMed  CAS  Google Scholar 

  • Hideg E, Murata N (1997) The irreversible photoinhibition of the photosystem II complex in leaves of Vicia faba under strong light. Plant Sci 130:151–158

    Article  CAS  Google Scholar 

  • Hideg E, Spetea C, Vass I (1994) Singlet oxygen and free radical production during acceptor- and donor-side-induced photoinhibition. Studies with spin trapping EPR spectroscopy. Biochim Biophys Acta 1186:143–152

    Article  CAS  Google Scholar 

  • Huesgen PF, Schuhmann H, Adamska I (2006) Photodamaged D1 protein is degraded in Arabidopsis mutants lacking the Deg2 protease. FEBS Lett 580:6929–6932

    Article  PubMed  CAS  Google Scholar 

  • Hundal T, Aro E-M, Carlberg I, Andersson B (1990) Restoration of light-induced photosystem II inhibition without de novo protein synthesis. FEBS Lett 267:203–206

    Article  PubMed  CAS  Google Scholar 

  • Inagaki N, Yamamoto Y, Satoh K (2001) A sequential two-step proteolytic process in the carboxy-terminal truncation of precursor D1 protein in Synechocystis 6803. FEBS Lett 509:197–201

    Article  PubMed  CAS  Google Scholar 

  • Jegerschöld C, Virgin I, Styring S (1990) Light-dependent degradation of the D1 protein in photosystem II is accelerated after inhibition of the water-splitting reaction. Biochemistry 29:6179–6186

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Kanervo E, Aro E-M, Murata N (1995) Low unsaturation level of thylakoid membrane lipids limits turnover of the Dl protein of photosystem II at high irradiance. FEBS Lett 364:239–242

    Article  PubMed  CAS  Google Scholar 

  • Kanervo E, Tasaka Y, Murata N, Aro A-M (1997) Membrane lipid unsaturation modulates processing of the photosystem II reaction-center protein D1 at low temperature. Plant Physiol 114:841–849

    Article  PubMed  CAS  Google Scholar 

  • Keren N, Ohad I (1998) State transition and photoinhibition. In: Rochaix J-D, Goldschmidt-Clermont M, Merchant S (eds) The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 570–596

    Google Scholar 

  • Kirilovsky DL, Vernotte C, Etienne AL (1990) Protection from photoinhibition by low temperature in Synechocystis 6714 and in Chlamydomonas reinhardtii: detection of an intermediary state. Biochemistry 29:8100–8106

    Article  PubMed  CAS  Google Scholar 

  • Kuvikova S, Tichy M, Komenda J (2005) A role of the C terminal extension of photosystem II D1 protein is sensitive of the cyanobacterium Synechocystis PCC 6803 to photoinhibition. Photochem Photobiol Sci 4:1044–1048

    Article  PubMed  CAS  Google Scholar 

  • Kyle DJ, Ohad I, Arntzen CJ (1984) Membrane protein damage and repair: selective loss of a quinone-protein function in chloroplast membranes. Proc Natl Acad Sci USA 81:4070–4074

    Article  PubMed  CAS  Google Scholar 

  • Lee HY, Hong YN, Chow WS (2001) Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbors in Capsicum annuum L. leaves. Planta 212:332–342

    Article  PubMed  CAS  Google Scholar 

  • Mattoo AK, Hoffman-Falk H, Marder JB, Edelman M (1984) Regulation 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

    Article  PubMed  CAS  Google Scholar 

  • Mattoo AK, Marder JB, Edelman M (1989) Dynamics of the photosystem II reaction center. Cell 56:241–246

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Miyao M, Ikeuchi M, Yamamoto N, Ono T (1995) Specific degradation of the D1 protein of photosystem II by treatment with hydrogen peroxide in darkness: implication for the mechanism of degradation of the D1 protein under illumination. Biochemistry 34:10019–10026

    Article  PubMed  CAS  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta (in press)

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

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2005) Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria. Photosynth Res 84:1–7

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749

    Article  PubMed  CAS  Google Scholar 

  • Nixon P, 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ohad I, Kyle DJ, Hirschberg J (1985) Light-dependent degradation of the QB-protein in isolated pea thylakoids. EMBO J 4:1655–1659

    PubMed  CAS  Google Scholar 

  • Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, Murata N (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44:8494–8499

    Article  PubMed  CAS  Google Scholar 

  • Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Annu Rev Plant Biol 54:329–355

    Article  PubMed  CAS  Google Scholar 

  • Ossenbuhi F, Inaba-Sulpice M, Meurer J, Soll J, Eichacker LA (2006) The Synechocystis PCC 6803 Oxa1 homolog is essential for integration of reaction center protein pD1. Plant Cell 18:2236–2246

    Article  CAS  Google Scholar 

  • Renger G, Volker M, Eckert HJ, Fromme R, Hohm-Veit S, Graber P (1989) On the mechanism of photosystem II deterioration by UV-B irradiation. Photochem Photobiol 49:97–105

    Article  CAS  Google Scholar 

  • Sippola K, Kanervo E, Murata N, Aro E-M (1998) A genetically engineered increase in fatty acid unsaturation in Synechococcus sp. PCC 7942 allows exchange of D1 protein forms and sustenance of photosystem II activity at low temperature. Eur J Biochem 251:641–648

    Article  PubMed  CAS  Google Scholar 

  • Sundby C, Schioett T (1992) Characterization of the reversible state of photoinhibition occurring in vitro under anaerobic conditions. Photosynth Res 33:195–202

    Article  CAS  Google Scholar 

  • Szalontai B, Nishiyama Y, Gombos Z, Murata N (2000) Membrane dynamics as seen by Fourier transform infrared spectroscopy in a cyanobacterium, Synechocystis PCC 6803. The effects of lipid unsaturation and the protein-to-lipid ratio. Biochim Biophys Acta 1509:409–419

    Article  PubMed  CAS  Google Scholar 

  • Tasaka Y, Gombos Z, Nishiyama Y, Mohanty P, Ohba T, Ohki K, Murata N (1996) Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis. EMBO J 15:6416–6425

    PubMed  CAS  Google Scholar 

  • Telfer A, Bishop SM, Phillips D, Barber J (1994) The isolated photosynthetic reaction center of PSII as a sensitiser for the formation of singlet oxygen; detection and quantum yield determination using a chemical trapping technique. J Biol Chem 269:13244–13253

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Vass I, Styring S, Hundal T, Koivuniemi A, Aro E-M, Andersson B (1992) The 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

    Article  PubMed  CAS  Google Scholar 

  • Zsiros O, Allakhverdiev SI, Higashi S, Watanabe M, Nishiyama Y, Murata N (2006) Very strong UV-A light temporally separates the photoinhibition of photosystem II into light-induced inactivation and repair. Biochim Biophys Acta 1757:123–129

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors acknowledge Dr. J. S. S. Prakash, Hyderabad University, and Dr. Shunichi Takahashi, the Australian National University, for their kind help during the preparation of the manuscript. This work was supported, in part, by the Cooperative Research Program on Stress-Tolerant Plants of the National Institute for Basic Biology, Japan, and by grants from the Russian Foundation for Basic Research (no. 05-04-49672) and from the Molecular and Cell Biology Programs of the Russian Academy of Sciences (to S.I.A.). P.M. thanks the Indian National Science Academy, New Delhi, for his assignment as an honorary scientist at RPRC Bhubaneswar.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Norio Murata.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mohanty, P., Allakhverdiev, S.I. & Murata, N. Application of low temperatures during photoinhibition allows characterization of individual steps in photodamage and the repair of photosystem II. Photosynth Res 94, 217–224 (2007). https://doi.org/10.1007/s11120-007-9184-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-007-9184-y

Keywords

Navigation