Skip to main content
SpringerLink
Log in

The interaction of visible and UV-B light during photodamage and repair of Photosystem II

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

In order to understand the mechanism of photodamage induced by solar radiation under natural conditions, we studied the interaction of visible and ultraviolet-B light in the inactivation and repair of the Photosystem II complex by using oxygen evolution and flash-induced chlorophyll fluorescence measurements. In isolated spinach thylakoids and Synechocystis 6803 cells, in which de novo protein synthesis is blocked by lincomycin, photodamage of Photosystem II by visible and UV-B light is characterized by linear semilogarithmic inactivation curves for both separate and combined illumination protocols. The extent of PS II inactivation obtained after combined illumination can be well simulated by assuming independent damaging events induced by visible and UV-B photons. In intact Synechocystis cells capable of protein repair, simultaneous illumination by visible and UV-B light impairs Photosystem II activity to a smaller extent than expected from the independent damaging events. This protective effect is pronounced at low visible light (130 μE m−2 s−1), but becomes negligible at high intensities (1300 μE m−2 s−1). Exposure of intact Synechocystis 6803 cells to direct sunlight leads to a rapid inactivation of PS II, accompanied by the accumulation of donor side inhibited centers. This phenomenon, which shows the impairment of the manganese cluster of water oxidation was not observed when the ultraviolet components of sunlight were filtered out. We conclude that visible and UV-B photons inactivate PS II via non-interacting mechanisms, which affect different target sites. In intact cells, the two spectral regions do interact, and results in synergistically enhanced protein repair capacity when UV-B radiation is accompanied by low intensity visible light, which provides protection against photodamage. However, this ameliorating effect becomes insignificant at high light intensities characteristic of direct sunlight.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson JM (2001) Does functional Photosystem II complex have an oxygen channel? FEBS Lett 488: 1–4

    Article  PubMed  CAS  Google Scholar 

  • Andersson B and Styring S (1991) Photosystem II: molecular organization, function, and acclimation. Curr Top Bioenerg 16: 1–81

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Blaubaugh D and Cheniae GM (1990) Kinetics of photoinhibition in hydroxylamine-extracted II membranes: relevance to photoactivation and sites of electron donation. Biochemistry 29: 5109–5118

    Article  Google Scholar 

  • Coggle JE (1973) Biological effects of radiation. In:Mott N, Noakes GR and Yapp WB (eds) TheWykeham Science Series.Wykeham Publications, London

    Google Scholar 

  • Critchley C, Russel AW and Morrison BC (1999) Photoinhibition of PS II in leaves: stress, acclimation, or regulatory response? In: Pessarakli M (ed) Handbook of Plant and Crop Stress, pp 545–553. Marcel Dekker, New York

    Google Scholar 

  • Dring MJ, Wagner A and Lüning K (2001) Contribution of the UV component of natural sunlight to photoinhibition of photosynthesis in six species of suntidal brown and red seaweeds. Plant Cell Environ 24: 1153–1164

    Article  CAS  Google Scholar 

  • Durrant JR, Giorgi LB, Barber J, Klug DR and Porter G (1990) Characterization of triplet states in isolated photossytem II reaction centres: oxygen quenching as a mechanism for photodamage. Biochim Biophys Acta 1017: 167–175

    Article  CAS  Google Scholar 

  • Eckert H-J, Geiken B, Bernading J, Napiwotzki A, Eichler H-J and Renger G (1991) Two sites of photoinhibition of the electron transfer in oxygen evolving and Tris-trated PS II membrane fragments from spinach. Photosynth Res 27: 97–108

    Article  CAS  Google Scholar 

  • Friso G, Spetea C, Giacometti GM, Vass I and Barbato R (1993) Degradation of Photosystem II reaction center D1-protein induced by UVB irradiation in isolated thylakoids. Identification and characterization of C-and N-terminal breakdown products. Biochim Biophys Acta 1184: 78–84

    Google Scholar 

  • Greenberg BM, Gaba V, Canaani O, Malkin S, Mattoo AK and Edelman M (1989) Separate photosensitizers mediate degradation of the 32-kDa Photosystem II reaction centre protein in visible and UV spectral regions. Proc Natl Acad Sci USA 86: 6617–6620

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jansen MAK, Greenberg BM, Edelman M, Mattoo AK and Gaba V (1996) Accelerated degradation of the D2 protein of Photosystem II under ultraviolet radiation. Photochem Photobiol 63: 814–817

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Jordan BR, Chow WS, Strid A and Anderson JM (1991) Reduction in cab and psbA RNA transcripts in response to supplementary ultraviolet-B radiation. FEBS Lett 284: 5–8

    Article  PubMed  CAS  Google Scholar 

  • Keren N, Berg A, van Kan PJM, Levanon H and Ohad I (1997) Mechanism 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

    CAS  Google Scholar 

  • Krause GH (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol Planta 74: 566– 574

    Article  CAS  Google Scholar 

  • Larkum AWD, Karge M, Reifarth F, Eckert H-J, Post A and Renger G (2001) Effect of monochromatic UV-B radiation on electron transfer reactions of Photosystem II. Photosynth Res 68: 49–60

    Article  PubMed  CAS  Google Scholar 

  • Máté Z, Sass L, Szekeres M, Vass I and Nagy F (1998) UV-B induced differential transcription of psbA genes encoding the D1protein of Photosystem II in the cyanobacterium Synechocystis 6803. J Biol Chem 273: 17439–17444

    Article  PubMed  Google Scholar 

  • Mäenpää P, Miranda T, Tyystjärvi E, Tyystjärvi T, Govindjee, Ducruet J-M, Etienne A-L and Kirilovsky D (1995) A mutation in the D-E loop of D1 modifies the stability of the S2QA-and S2QB-states in Photosystem II. Plant Physiol 107: 187–197

    PubMed  Google Scholar 

  • Melis A, Nemson JA and Harrison MA (1992) Damage to functional components and partial degradation of Photosystem II reaction center proteins upon chloroplast exposure to ultraviolet-B radiation. Biochim Biophys Acta 1100: 312–320

    CAS  Google Scholar 

  • Nagy L, Bálint E, Barber J, Ringler A, Cook KM and Maróti P (1995) Photoinhibition and law of reciprocity in photosynthetic reactions of Synechocystis sp. PCC 6803. J Plant Physiol 145: 410–415

    CAS  Google Scholar 

  • Nanba O and Satoh K (1987) Isolation of a Photosystem II reaction center consisting of D1 and D2 polypeptides and cytochrome b- 559. Proc Natl Acad Sci USA 84: 109–112

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Park Y-I, Chow WS and Anderson JM (1995) Light inactivation of functional Photosystem II in leaves of peas grown in moderate light depends on photon exposure. Planta 196: 401–411

    Article  CAS  Google Scholar 

  • Post A, Lukins PB, Walker PJ and Larkum AWD (1996) The effects of ultraviolet irradiation on P680+ reduction in PS II core complexes measured for individual S-states and during repetitive cycling of the oxygen-evolving complex. Photosynth Res 49: 21–27

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sass L, Spetea C, Máté Z, Nagy F and Vass I (1997) Repair of UVB induced damage of Photosystem II via de novo synthesis of the D1 and D2 reaction centre subunits in Synechocystis sp. PCC 6803. Photosynth Res 54: 55–62

    Article  CAS  Google Scholar 

  • Sinclair J, Park YI, Chow WS and Anderson JM (1996) Target theory and the photoinactivation of Photosystem II. Photosynth Res 50: 33–40

    Article  CAS  Google Scholar 

  • Sippola K and Aro E-M (2000) Expression of psbA genes is regulated at multiple levels in the cyanobacterium synechococcus sp. PCC 7942. Photochem Photobiol 71: 706–714

    Article  PubMed  CAS  Google Scholar 

  • Strid A, Chow WS and Anderson JM (1994) UV-B damage and protection at the molecular level in plants. Photosynth Res 39: 475–489

    Article  CAS  Google Scholar 

  • Teramura AH, Biggs RH and Kossuth S (1980) Effects of ultraviolet-B irradiances on soybean. II. Interaction between ultraviolet-B and photosynthetically active radiation on net photosynthesis, dark respiration, and transpiration. Plant Physiol 65: 483–488

    PubMed  CAS  Google Scholar 

  • Trebst A and Depka B (1990) Degradation of the D-1 protein subunit of Photosystem II in isolated thylakoids by UV light. Z Naturforsch 45c: 765–771

    CAS  Google Scholar 

  • Trtilek M, Kramer DM and Koblizek M (1997) Dual-modulation LED kinetic fluorometer. J Lumin 72-74: 597–599

    Article  Google Scholar 

  • Turcsányi E and Vass I (2000) Inhibition of Photosynthetic electron transport by UV-A radiation targets the Photosystem II complex. Photochem Photobiol 72: 513–520

    Article  PubMed  Google Scholar 

  • Tyystjarvi E, Kairavuo M, Patsikka E, Keranen M, Khriachtchev L, Tuominen I, Guiamet JJ and Tyystjarvi T (2001) The quantum yield of photoinhibition is the same in flash light and under continuous illumination – implications for the mechanismPS2001Proceedings. 12th International Congress on Photosynthesis CSIRO Publishing, Collingwood, Australia

    Google Scholar 

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

    CAS  Google Scholar 

  • Vass I, Sass L, Spetea C, Bakou A, Ghanotakis D and 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

    Article  PubMed  CAS  Google Scholar 

  • Vass I (1996) Adverse effects of UV-B light on the structure and function of the photosynthetic apparatus. In: Pessarakli M (ed) Handbook of Photosynthesis, pp 931–950. Marcel Dekker, New York

    Google Scholar 

  • Vass I, Kirilovsky D and Etienne A-L (1999) UV-B radiationinduced donor-and acceptor-side modifications of Photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 38: 12786–12794

    Article  PubMed  CAS  Google Scholar 

  • Vass I, Kirilovsky D, Perewoska I, Máté Z, Nagy F and Etienne AL (2000) UV-B radiation induced exchange of the D1 reaction centre subunits produced from the psbA2 and psbA3 genes in the cyanobacterium Synechocystis sp. PCC 6803. Eur J Biochem 267: 2640–2648

    Article  PubMed  CAS  Google Scholar 

  • Vass I, Máté Z, Turcsányi E, Sass L, Nagy F and Sicora C (2001) Damage and repair of Photosystem II under exposure to UV radiation PS2001 Proceedings. 12th International Congress on Photosynthesis. CSIRO Publishing, Collingwood, Australia

    Google Scholar 

  • Vass I, Turcsányi E, Touloupakis E, Ghanotakis D and Petroluleas V (2002) The Mechanism of UV-A Radiation-Induced Inhibition of Photosystem II Electron Transport Studied by EPR and Chlorophyll Fluorescence. Biochemistry 41: 10200–10208

    Article  CAS  Google Scholar 

  • Yerkes CT, Kramer DM, Fenton JM and Crofts AR (1990) UV-photoinhibition: studies in vitro and in intact plants. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol II, pp II.6.381–II.6.384. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Plant Biology, Biological Research Center, 6726, Szeged, Temesvári krt. 62, Hungary

    Cosmin Sicora, Zoltán Máté & Imre Vass

Authors
  1. Cosmin Sicora
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zoltán Máté
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Imre Vass
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sicora, C., Máté, Z. & Vass, I. The interaction of visible and UV-B light during photodamage and repair of Photosystem II. Photosynthesis Research 75, 127–137 (2003). https://doi.org/10.1023/A:1022852631339

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022852631339

Search

Navigation