Photosynthesis Research

, Volume 81, Issue 1, pp 41–47

Superoxide, Hydrogen Peroxide and Hydroxyl Radical in D1/D2/cytochrome b-559 Photosystem II Reaction Center Complex

  • Ke Liu
  • Jian Sun
  • Yu-guang Song
  • Bin Liu
  • Ying-kai Xu
  • Shu-xiao Zhang
  • Qiu Tian
  • Yang Liu
Article

Abstract

Spin-trapping electron spin resonance (ESR) was used to monitor the formation of superoxide and hydroxyl radicals in D1/D2/cytochrome b-559 Photosystem II reaction center (PS II RC) Complex. When the PS II RC complex was strongly illuminated, superoxide was detected in the presence of ubiquinone. SOD activity was detected in the PS II RC complex. A primary product of superoxide, hydrogen peroxide, resulted in the production of the most destructive reactive oxygen species, •OH, in illuminated PS II RC complex. The contributions of ubiquinone, SOD and H2O2 to the photobleaching of pigments and protein photodamage in the PS II RC complex were further studied. Ubiquinone protected the PS II RC complex from photodamage and, interestingly, extrinsic SOD promoted this damage. All these results suggest that PS II RC is an active site for the generation of superoxide and its derivatives, and this process protects organisms during strong illumination, probably by inhibiting more harmful ROS, such as singlet oxygen.

hydroxyl radical Photosystem II reaction center superoxide superoxide dismutase 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ananyev GM, Wydrzynski T, Renger G and Klimov VV (1992) Transient peroxide formation by the Mn-containing, redox-active donor side of Photosystem II upon inhibition of O2 evolution with lauroylcholine chloride. Biochim Biophys Acta 1100: 303–311Google Scholar
  2. Ananyev GM, Renger G, Wacker U and Klimov VV (1994) The photoproduction of superoxide radicals and the superoxide dismutase activity of Photosystem II. The possible involvement of cytochrome b559. Photosynth Res 41: 327–338Google Scholar
  3. Andersson B and Barber J (1996) Mechanisms of photodamage and protein degradation during photoinhibition of Photosystem II. In: Baker NR (ed) Photosynthesis and the Environment, pp 101–121. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  4. Asada K (1992) Production and scavenging of active oxygen in chloroplasts. In: Scandalios JG (ed) Molecular Biology of Free Radical Scavenging Systems, 173 pp. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New YorkGoogle Scholar
  5. Asada K and Kiso K (1973) Initiation of aerobic oxidation of sulfite by illuminated spinach chloroplasts. Eur J Biochem 33: 253–257Google Scholar
  6. Asada K and Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Topics in Photosynthesis, Photoinhibition, Vol. 9, 227 pp. Elsevier, AmsterdamGoogle Scholar
  7. Asada K, Kiso K and Yoshikawa K (1974) Univalent reduction of molecular oxygen by spinach chloroplasts on illumination. J Biol Chem 249: 2175–2181Google Scholar
  8. Barenyi B and Krause GH (1985) Inhibition of photosynthetic reactions by light. A study with isolated spinach chloroplasts. Planta 163: 218–226Google Scholar
  9. Chapman DJ, Gounaris K and Barber J (1988) Electron-transport properties of the isolated D1-D2-cytochrome b-559 Photosystem II reaction center. Biochim Biophy Acta 933: 423–431Google Scholar
  10. Cleland RE and Grace SC (1999) Voltammetric detection of superoxide production by Photosystem II. FEBS Lett 457: 348–352Google Scholar
  11. Durrant JR, Giorgi LB, Barber J, Klug DR and Porter G (1990) Characterization of triplet states in isolated Photosystem II reaction centres: oxygen quenching as a mechanism of photodamage. Biochim Biophys Acta 1017: 167–175Google Scholar
  12. Furbank RT, Badger MR and Osmond CB (1983) Photoreduction of oxygen in mesophyll chloroplasts of C4 plants. A model system for studying an in vivo Mehler reaction. Plant Physiol 73: 1038–1041Google Scholar
  13. Halliwell B and Gutteridge (1985) Free Radicals in Biology and Medicine. Clarendon Press, OxfordGoogle Scholar
  14. Hayakawa T, Kanematsu S and Asada K (1984) Occurrence of copper, zinc-superoxide dismutase in the intrathylakoid space of spinach chloroplasts. Plant Cell Physiol 25: 883–889Google Scholar
  15. Hayakawa T, Kanematsu S and Asada K (1985) Purification and characterization of thylakoid-bound manganese superoxide dismutase in spinach chloroplasts. Planta 166: 111–116Google Scholar
  16. Hideg \(\hat E_.\) and Spetea C (1994) Singlet oxygen and free radical production during acceptor-and donor-side-induced photoinhibition. Studies with spin-trapping ESR spectroscopy. Biochim Biophys Acta 1186: 143–152Google Scholar
  17. Hideg \(\hat E_.\), Spetea C and Vass I (1994) Singlet oxygen production in thylakoid membranes during photoinhibition as detected by ESR spectroscopy. Photosynth Res 39: 191–199Google Scholar
  18. Kirilovsky D, Ducruet JM and Etienne A-L (1990) Primary events occurring in photoinhibition in Synechocystis 6714 wild-type and an atrazine-resistant mutant. Biochim Biophys Acta 1020: 87–93Google Scholar
  19. Klimov VV, Ananyev GM, Zastryzhnaya OM, Wydryzynski T and Renger G (1993) Photoproduction of hydrogen peroxide in Photosystem II membrane fragments: a comparison of four signals. Photosynth Res 38: 409–416Google Scholar
  20. Kuwabara T and Murata N (1982) Inactivation of photosynthetic oxygen evolution and concomitant release of three polypeptides in the Photosystem II particles of spinach chloroplasts. Plant Cell Physio 23: 533–539Google Scholar
  21. Liu K, Sun J, Liu Y, Zhang QY and Kuang TY (2001) ESR study on superoxide radicals generated in Photosystem II of higher plant. Prog Biochem Biophys 28: 372–376Google Scholar
  22. Mehler AH (1951) Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys 33: 650–677Google Scholar
  23. Mishra NP and Ghanotakis DF (1994) Exposure of a Photosystem II complex to chemically generated singlet oxygen results in D1 fragments similar to the ones observed during aerobic photoinhibition. Biochim Biophys Acta 1187: 296–300Google Scholar
  24. Miyao M (1994) Involvement of active oxygen species in degradation of the D1 protein under strong illumination in isolated subcomplexes of Photosystem II. Biochemistry 33: 9722–9730Google Scholar
  25. Nakane H, Iwaki M, Satoh K and Itoh S (1991) Artificial quinones replace the function of quinone electron acceptor (QA) in the isolated D1-D2-cytochrome b559 Photosystem II reaction center complex. Plant Cell Physiol 32: 1165–1171Google Scholar
  26. Nanba O and Satoh K (1987) Isolation of a Photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci USA 84: 109–112Google Scholar
  27. Navari-Izzo F, Pinzino C, Quartacci MF and Sgherri CLM (1999) Superoxide and hydroxyl radical generation, and superoxide dismutase in PS II membrane fragments from wheat. Free Radical Res 31(Suppl): 3–9Google Scholar
  28. Setlik I, Allakhverdiev SI, Nedbal L, Setlikova E and Klimov VV (1990) Three types of Photosystem II photoinactivation. 1. Damaging processes on the acceptor side. Photosynth Res 23: 39–48Google Scholar
  29. Shiraishi T, Takahashi MA and Asada K (1992) Production and decay of superoxide anion radicals in illuminated thylakoid membranes. In: Murata N (ed) Research in Photosynthesis, Vol. II Kluwer Academic Publishers, Dordrecht, The Netherlands, 627 ppGoogle Scholar
  30. Takahashi MA and Asada K (1988) Superoxide production in aprotic interior of chloroplast thylakoids. Arch Biochem Biophys 26: 714–722Google Scholar
  31. Telfer A, Dhami S, Bishop SM, Philips D and Barber J (1994) β-Carotene quenches singlet oxygen formed by isolated Photosystem II reaction centers. Biochemistry 33: 14469–14474Google Scholar
  32. Vass I, Styring S, Hundal T, Koivuniemi A, Aro E-M and 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: 1408–1412Google Scholar
  33. Wydrzynski T, Aangstroem J and Vaenngaard T (1989) Hydrogen peroxide formation by Photosystem II. Biochim Biophys Acta 973: 23–28Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Ke Liu
    • 1
  • Jian Sun
    • 1
  • Yu-guang Song
    • 1
  • Bin Liu
    • 1
  • Ying-kai Xu
    • 1
  • Shu-xiao Zhang
    • 1
  • Qiu Tian
    • 1
  • Yang Liu
    • 1
  1. 1.State Key Laboratory for Structural Chemistry of Unstable and Stable Species, Center for Molecular ScienceInstitute of Chemistry, The Chinese Academy of SciencesBeijingChina

Personalised recommendations