Photosynthetica, 2011 (vol. 49), issue 3

Photosynthetica 2011, 49(3):353 | DOI: 10.1007/s11099-011-0044-9

Biphasic regulation of superoxide radical levels in Mn-depleted and photoactivated photosystem II

Y. G. Song1,2, B. Liu3, Y. P. Liu2, L. B. Du1, F. A. Villamena2, Y. Liu1,*
1 State Key laboratory for Structural Chemistry of Unstable and Stable Species, Center for Molecular Science, Institute of Chemistry, The Chinese Academy of Sciences, Beijing, China
2 Center for Biomedical EPR Spectroscopy and Imaging, The Davis Heart and Lung Research Institute, the Division of Cardiovascular Medicine, Department of Internal Medicine, and Department of Pharmacology, College of Medicine, The Ohio State University, Columbus, USA
3 Cardiovascular Research Center, Shantou University Medical College, Shantou, China

In the past decades, it has become clear that superoxide radical (O2 .-) can be generated from photosystem II (PSII) during photosynthesis. Depending on the extent of its accumulation, O2 .- plays an important role in plant physiology and pathology. The photoinhibition/repair cycle is a typical process in PSII which is mainly responsible for the survival of plants under the photoinihibition condition. It is therefore of significant importance to determine O2 .- production in this cycle, and then explore how O2 .- is controlled by PSII within a normal physiological level. With this in mind, we herein investigate the variation of the O2 .- levels in PSII under Mn-depleted and photoactivated conditions mimicking the photoinhibition/repair cycle in vitro. The effect of intrinsic SOD-like component on the O2 .- levels was also studied. Results show that PSII has the ability to regulate the O2 .- levels in these two processes by simultaneously modulating the O2 .- generation activity and intrinsic SOD-like activity. This finding could shed new lights on the photoprotective property of PSII against O2 .- and other reactive oxygen species.

Keywords: biphasic regulation; cytochrome b559; Mn-depletion; photoactivation; photosystem II; superoxide radical

Received: November 15, 2010; Accepted: May 11, 2011; Published: September 1, 2011Show citation

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Song, Y.G., Liu, B., Liu, Y.P., Du, L.B., Villamena, F.A., & Liu, Y. (2011). Biphasic regulation of superoxide radical levels in Mn-depleted and photoactivated photosystem II. Photosynthetica49(3), 353. doi: 10.1007/s11099-011-0044-9.
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References

  1. Allakhverdiev, S.I., Karacan, M.S., Somer, G., et al.: Reconstitution of the water-oxidizing complex in manganese-depleted photosystem-II complexes by using synthetic binuclear manganese complexes. - Biochemistry 33: 12210-12214, 1994. Go to original source...
  2. Allakhverdiev, S.I., Ozdemir, U., Harnois, J., et al.: Reconstruction of the water-oxidizing complex in manganesedepleted photosystem II preparations using mononuclear manganese complexes. - Photochem. Photobiol. 70: 57-63, 1999. Go to original source...
  3. Ananyev, G., Renger, G., Wacker, U., Klimov, V.: The photoproduction of superoxide radicals and the superoxidedismutase activity of photosystem-II - the possible involvement of cytochrome b559. - Photosynth. Res. 41: 327-338, 1994. Go to original source...
  4. Apel, K., Hirt, H.: Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. - Annu. Rev. Plant Biol. 55: 373-399, 2004. Go to original source...
  5. Arnon, D.I.: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. - Plant Physiol. 24: 1-15, 1949. Go to original source...
  6. Aro, E. M., Virgin, I., Andersson, B.: Photoinhibition of photosystem-2 - inactivation, protein damage and turnover. - Biochim. Biophys. Acta 1143: 113-134, 1993. Go to original source...
  7. Berthold, D.A., Babcock, G.T., Yocum, C.F.: A highly resolved, oxygen-evolving photosystem-II preparation from spinach thylakoid membranes - electron-paramagnetic-res and electron-transport properties. - FEBS Lett. 134: 231-234, 1981. Go to original source...
  8. Bhattacharjee, S.: Reactive oxygen species and oxidative burst: Roles in stress, senescence and signal transduction in plants. - Curr. Sci. 89: 1113-1121, 2005.
  9. Callahan, F.E., Becker, D.W., Cheniae, G.M.: Studies on the photo-inactivation of the water-oxidizing enzyme. II. Characterization of weak light photoinhibition of PSII and its light-induced recovery. - Plant Physiol. 82: 261-269, 1986. Go to original source...
  10. Chen, C.G., Kazimir, J., Cheniae, G.M.: Calcium modulates the photoassembly of photosystem II (Mn)4-clusters by preventing ligation of nonfunctional high-valency states of manganese. - Biochemistry 34: 13511-13526, 1995. Go to original source...
  11. Chen, G.X., Kazimir, J., Cheniae, G.M.: Photoinhibition of hydroxylamine-extracted photosystem II membranes: studies of the mechanism. - Biochemistry 31: 11072-11083, 1992. Go to original source...
  12. Cleland, R.E., Grace, S. C.: Voltammetric detection of superoxide production by photosystem II. - FEBS Lett. 457: 348-352, 1999. Go to original source...
  13. Dasgupta, J., Ananyev, G. M., Dismukes, G. C.: Photoassembly of the water-oxidizing complex in photosystem II. - Coordin. Chem. Rev. 252: 347-360, 2008.
  14. Frejaville, C., Karoui, H., Tuccio, B., et al.: 5-(Diethoxyphosphoryl)-5-methyl-1-pyrroline N-oxide: a new efficient phosphorylated nitrone for the in vitro and in vivo spin trapping of oxygen-centered radicals. - J. Med. Chem. 38: 258-265, 1995. Go to original source...
  15. Gadjieva, R., Mamedov, F., Renger, G., Styring, S.: Interconversion of low- and high-potential forms of cytochrome b 559 in tris-washed photosystem II membranes under aerobic and anaerobic conditions. - Biochemistry 38: 10578-10584, 1999. Go to original source...
  16. Guan, L.M., Scandalios, J.G.: Hydrogen peroxide-mediated catalase gene expression in response to wounding. - Free Radical Bio. Med. 28: 1182-1190, 2000. Go to original source...
  17. Hakala, M., Tuominen, I., Keränen, M., Tyystjärvi, T., Tyystjärvi, E.: Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of Photosystem II. - Biochim. Biophys. Acta 1706: 68-80, 2005. Go to original source...
  18. Iwasaki, I., Tamura, N., Okayama, S.: Effects of light stress on redox potential forms of cyt b559 in photosystem-II membranes depleted of water-oxidizing complex. - Plant Cell Physiol. 36: 583-589, 1995.
  19. Johnson, G. N., Rutherford, A. W., Krieger, A.: 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, 1995. Go to original source...
  20. Karacan, M. S., Somer, G.: Reconstruction of the wateroxidizing complex in manganese-depleted Photosystem II by using Schiff base manganese complexes. - J. Photochem. Photobiol. A 163: 307-310, 2004. Go to original source...
  21. Klimov, V., Ananyev, G., Zastryzhnaya, O., Wydrzynski, T., Renger, G.: Photoproduction of hydrogen peroxide in Photosystem II membrane fragments: A comparison of four signals. - Photosynth. Res. 38: 409-416, 1993. Go to original source...
  22. Knox, J.P., Dodge, A.D.: The photodynamic-action of eosin, a singlet-oxygen generator. - Planta 164: 30-34, 1985. Go to original source...
  23. Krieger, A., Rutherford, A.W., Johnson, G.N.: On the determination of redox midpoint potential of the primary quinone electron-acceptor, QA, in Photosystem II. - Biochim. Biophys. Acta 1229: 193-201, 1995. Go to original source...
  24. Krieger-Liszkay, A.: Singlet oxygen production in photosynthesis. - J. Exp. Bot. 56: 337-346, 2005. Go to original source...
  25. Kruk, J., Strzałka, K.: Dark reoxidation of the plastoquinonepool is mediated by the low-potential form of cytochrome b-559 in spinach thylakoids. - Photosynth. Res. 62: 273-279, 1999. Go to original source...
  26. Levine, A., Tenhaken, R., Dixon, R., Lamb, C.: H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. - Cell 79: 583-593, 1994. Go to original source...
  27. Liu, B., Shen, P.P., Shi, W., Song, Y.G., Li, W., Nie, Z., Liu, Y.: Highly efficient photoactivation of Mn-depleted photosystem II by imidazole-liganded manganese complexes. - J. Biol. Inorg. Chem. 11: 626-632, 2006. Go to original source...
  28. Liu, K., Sun, J., Song, Y.G., Liu, B., Xu, Y.K., Zhang, S.X., Tian, Q., Liu, Y.: Superoxide, hydrogen peroxide and hydroxyl radical in D1/D2/cytochrome b-559 Photosystem II reaction center complex. - Photosynth. Res. 81: 41-47, 2004. Go to original source...
  29. Melis, A.: Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? - Trends Plant Sci. 4: 130-135, 1999. Go to original source...
  30. Miller, A.F., Brudvig, G.W.: Manganese and calcium requirements for reconstitution of oxygen-evolution activity in manganese-depleted photosystem II membranes. - Biochemistry 28: 8181-8190, 1989. Go to original source...
  31. Mizusawa, N., Ebina, M., Yamashita, T.: Restoration of the high-potential form of cytochrome b-559 through the photoreactivation of Tris-inactivated oxygen-evolving center. - Photosynth. Res. 45: 71-77, 1995. Go to original source...
  32. Mizusawa, N., Miyao, M., Yamashita, T.: Restoration of the high-potential form of cytochrome b-559 by electron transport reactions through Photosystem II in Tris-treated Photosystem II membranes. - Biochim. Biophys. Acta 1318: 145-158, 1997. Go to original source...
  33. Mizusawa, N., Yamashita, T., Miyao, M.: Restoration of the high-potential form of cytochrome b559 of photosystem II occurs via a two-step mechanism under illumination in the presence of manganese ions. - Biochim. Biophys. Acta 1410: 273-286, 1999. Go to original source...
  34. Müh, F., Renger, T., Zouni, A.: Crystal structure of cyanobacterial photosystem II at 3.0 Å resolution: A closer look at the antenna system and the small membrane-intrinsic subunits. - Plant Physiol. Bioch. 46: 238-264, 2008.
  35. Navari-Izzo, F., Pinzino, C., Quartacci, M.F., Sgherri, C.L.M.: Superoxide and hydroxyl radical generation, and superoxide dismutase in PSII membrane fragments from wheat. - Free Radical Res. 31: S3-S9, 1999. Go to original source...
  36. Nishiyama, Y., Allakhverdiev, S. I., Murata N.: A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. - Biochim. Biophys. Acta 1757: 742-749, 2006. Go to original source...
  37. Nugent, J.H.A.: Photoreducible high spin iron electron paramagnetic resonance signals in dark-adapted Photosystem II: are they oxidised non-haem iron formed from interaction of oxygen with PSII electron acceotors? - Biochem. Biophys. Acta 1504: 228-298, 2001. Go to original source...
  38. Pospíšil, P.: Production of reactive oxygen species by photosystem II. - Biochim. Biophys. Acta 1787: 1151-1160, 2009. Go to original source...
  39. Pospíšil, P., Arató, A., Krieger-Liszkay, A., Rutherford, A.W.: Hydroxyl radical generation by photosystem II. - Biochemistry 43: 6783-6792, 2004.
  40. Pospíšil, P., Šnyrychová, I., Kruk, J., Strzałka, K., Nauš, J.: Evidence that cytochrome b 559 is involved in superoxide production in photosystem II: effect of synthetic short-chain plastoquinones in a cytochrome b 559 tobacco mutant. - Biochem. J. 397: 321-327, 2006.
  41. Rivas, J. D., Klein, J., Barber, J.: pH sensitivity of the redox state of cytochrome b559 may regulate its function as a protectant against donor and acceptor side photoinhibition. - Photosynth. Res. 46: 193-202, 1995. Go to original source...
  42. Song, Y. G., Liu, B., Wang, L.F., Li, M.H., Liu, Y.: Damage to the oxygen-evolving complex by superoxide anion, hydrogen peroxide, and hydroxyl radical in photoinhibition of photosystem II. - Photosyth. Res. 90: 67-78, 2006. Go to original source...
  43. Tiwari, A., Pospíšil, P.: Superoxide oxidase and reductase activity of cytochrome b 559 in photosystem II. - Biochim. Biophys. Acta 1787: 985-994, 2009. Go to original source...
  44. Tjus, S.E., Scheller, H.V., Andersson, B., Møller, B.L.: Active oxygen produced during selective excitation of photosystem I is damaging not only to photosystem I, but also to photosystem II. - Plant Physiol. 125: 2007-2015, 2001.
  45. Tyystjärvi, E.: Photoinhibition of Photosystem II and photodamage of the oxygen evolving manganese cluster. - Coordin. Chem. Rev. 252: 361-376, 2008. Go to original source...
  46. Vass, I., Styring, S., Hundal, T., Koivuniemi, A., Aro, E. M., Andersson, B.: Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. - Proc. Nat. Acad. Sci. USA 89: 1408-1412, 1992. Go to original source...
  47. Vass, I., Cser, K.: Janus-faced charge recombinations in photosystem II photoinhibition. - Trends Plant Sci. 14: 200-205, 2009. Go to original source...
  48. Yruela, I., Montoya, G., Alonso, P.J., Picorel, R.: Identification of the pheophytin-QA-Fe domain of the reducing side of the photosystem II as the Cu (II)-inhibitory binding site. - J. Biol. Chem. 266: 22847-22850, 1991.
  49. Zhang, S., Weng, J., Pan, J.X., Tu, T.C., Yao S., Xu, C.H.: Study on the photo-generation of superoxide radicals in Photosystem II with EPR spin trapping techniques. - Photosynth. Res. 75: 41-48, 2003. Go to original source...