A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1757, Issue 7, 2006, Pages 742-749

  Nishiyama, Yoshitaka ^a   Allakhverdiev, Suleyman I ^b,c   Murata, Norio ^b  

^a EHIME UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^c INSTITUTE OF BASIC BIOLOGICAL PROBLEMS   (Russian Federation)

Author keywords

Photoinhibition; Photosystem II; Protein synthesis; Reactive oxygen species; Repair

Indexed keywords

CARBON DIOXIDE; MESSENGER RNA; REACTIVE OXYGEN METABOLITE;

ANALYTIC METHOD; CARBON DIOXIDE FIXATION; CHLAMYDOMONAS; ELECTRON TRANSPORT; ESCHERICHIA COLI; LIGHT DAMAGE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHOTOINHIBITION; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RADIATION INJURY; REVIEW; SYNECHOCYSTIS; ULTRAVIOLET RADIATION;

HEAT; MODELS, BIOLOGICAL; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN BIOSYNTHESIS; REACTIVE OXYGEN SPECIES; SYNECHOCYSTIS;

EID: 33746761616     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2006.05.013     Document Type: Review

References (89)

1. Powles S.B. Photoinhibition of photosynthesis induced by visible light. Annu. Rev. Plant Physiol. 35 (1984) 15-44
2. Prásil O., Adir N., and Ohad I. Dynamics of photosystem II: mechanism of photoinhibition and recovery processes. In: Barber J. (Ed). Topics in Photosynthesis. The Photosystems: Structure, Function and Molecular Biology Vol. 11 (1992), Elsevier Science Publishers, Amsterdam, The Netherlands 295-348
3. Aro E.-M., Virgin I., and Andersson B. Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143 (1993) 113-134
4. Andersson B., and Aro E.-M. Photodamage and D1 protein turnover in photosystem II. In: Aro E.-M., and Andersson B. (Eds). Regulation of Photosynthesis (2001), Kluwer Academic Publishers, Dordrecht, The Netherlands 377-393
5. Gombos Z., Wada H., and Murata N. The recovery of photosynthesis from low-temperature photoinhibition is accelerated by the unsaturation of membrane lipids: a mechanism of chilling tolerance. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 8787-8791
6. Tyystjärvi E., and Aro E.-M. The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 2213-2218
7. Anderson J.M., and Chow W.S. Structural and functional dynamics of plant photosystem II. Philos. Trans. R. Soc. Lond., B 357 (2002) 1421-1430
8. Park Y.-I., Chow W.S., and Anderson J.M. Light inactivation of functional photosystem II in leaves of peas grown in moderate light depends on photon exposure. Planta 196 (1995) 401-411
9. Nishiyama Y., Allakhverdiev S.I., Yamamoto H., Hayashi H., and Murata N. Singlet oxygen inhibits the repair of photosystem II by suppressing translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43 (2004) 11321-11330
10. Allakhverdiev S.I., and Murata N. Environmental 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 (2004) 23-32
11. Asada K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 (1999) 601-639
12. Knox J.P., and Dodge A.D. Singlet oxygen and plants. Phytochemistry 24 (1985) 889-896
13. Zolla L., and Rinalducci S. Involvement of active oxygen species in degradation of light-harvesting proteins under light stresses. Biochemistry 41 (2002) 14391-14402
14. Havaux M., Eymery F., Porfirova S., Rey P., and Dörmann P. Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17 (2005) 3451-4369
15. A species promote chlorophyll triplet formation. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 1408-1412
16. Keren N., Berg A., van Kan P.J.M., Levanon H., and Ohad I. Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: The role of back electron flow. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 1579-1584
17. Hideg E., Spetea C., and Vass I. Singlet oxygen and free radical production during acceptor- and donor-side-induced photoinhibition. Studies with spin trapping EPR spectroscopy. Biochim. Biophys. Acta 1186 (1994) 143-152
18. Hideg E., Kálai T., Hideg K., and Vass I. Photoinhibition of photosynthesis in vivo results in singlet oxygen production: detection via nitroxide-induced fluorescence quenching in broad bean leaves. Biochemistry 37 (1998) 11405-11411
19. Telfer A., Bishop S.M., Phillips D., and Barber J. The isolated photosynthetic reaction center of PS II as a sensitiser for the formation of singlet oxygen; detection and quantum yield determination using a chemical trapping technique. J. Biol. Chem. 269 (1994) 13244-13253
20. Fufezan C., Rutherford A.W., and Krieger-Liszkay A. Singlet oxygen production in herbicide-treated photosystem II. FEBS Lett. 532 (2002) 407-410
21. Okada K., Ikeuchi M., Yamamoto N., Ono T., and Miyao M. Selective and specific cleavage of the D1 and D2 proteins of photosystem II by exposure to singlet oxygen: factors responsible for the susceptibility to cleavage of the proteins. Biochim. Biophys. Acta 1274 (1996) 73-79
22. Sopory S.K., Greenberg B.M., Mehta R.A., Edelman M., and Mattoo A.K. Free radical scavengers inhibit light-dependent degradation of the 32 kDa photosystem II reaction center protein. Z. Naturforsch. 45c (1990) 412-417
23. Ananyev G., Wydrzynski T., Renger G., and Klimov V. Transient peroxide formation by the manganese-containing, redox-active donor side of photosystem II upon inhibition of O2 evolution with lauroylcholine chloride. Biochim. Biophys. Acta 1100 (1992) 303-311
24. Chen G.-X., Kazimir J., and Cheniae G.M. Photoinhibition of hydroxylamine-extracted photosystem II membranes: studies of the mechanism. Biochemistry 31 (1992) 11072-11083
25. Miyao M., Ikeuchi M., Yamamoto N., and Ono T. 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 (1995) 10019-10026
26. Callahan F.E., Becker D.W., and Cheniae G.M. Studies on the photoinactivation of the water-oxidizing enzyme. II. Characterization of weak-light photoinhibition of PSII and its light-induced recovery. Plant Physiol. 82 (1986) 261-269
27. Theg S.M., Filar L.J., and Dilley R.A. Photoinactivation of chloroplasts already inhibited on the oxidizing side of photosystem II. Biochim. Biophys. Acta 849 (1986) 104-111
28. Klimov V.V., Shafiev M.A., and Allakhverdiev S.I. Photoinactivation of the reactivation capacity of photosystem II in pea subchloroplast particles after a complete removal of manganese. Photosynth. Res. 23 (1990) 59-65
29. Wada H., Gombos Z., and Murata N. Contribution of membrane lipids to the ability of the photosynthetic machinery to tolerate temperature stress. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 4273-4277
30. Moon B.Y., Higashi S., Gombos Z., and Murata N. Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 6219-6223
31. Nishiyama Y., Yamamoto H., Allakhverdiev S.I., Inaba M., Yokota A., and Murata N. Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J. 20 (2001) 5587-5594
32. Nishiyama Y., Allakhverdiev S.I., and Murata N. Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria. Photosynth. Res. 84 (2005) 1-7
33. Ohnishi N., Allakhverdiev S.I., Takahashi S., Higashi S., Watanabe M., Nishiyama Y., and Murata N. 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 (2005) 8494-8499
34. Hakala M., Tuominen I., Keränen M., Tyystjärvi T., and Tyystjärvi E. Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochim. Biophys. Acta 1706 (2005) 68-80
35. Kyle D.J., Ohad I., and Arntzen C.J. Membrane protein damage and repair: selective loss of quinone-protein function in chloroplast membranes. Proc. Natl. Acad. Sci. U. S. A. 181 (1984) 4070-4074
36. Ohad I., Kyle D.J., and Arntzen C.J. Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptide in chloroplast membranes. J. Cell Biol. 99 (1984) 481-485
37. Mattoo A.K., Marder J.B., and Edelman M. Dynamics of the photosystem II reaction center. Cell 56 (1989) 241-246
38. Aro E.-M., Suorsa M., Rokka A., Allahverdiyeva Y., Paakkarinen V., Saleem A., Battchikova N., and Rintamäki E. Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J. Exp. Bot. 56 (2005) 347-356
39. Anbudurai P.R., Mor T.S., Ohad I., Shestakov S.V., and Pakrasi H.B. The ctpA gene encodes the C-terminal processing protease for the D1 protein of the photosystem II reaction center complex. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 8082-8086
40. Ayala A., Parrado J., Bougria M., and Machado A. Effect of oxidative stress, produced by cumene hydroperoxide, on the various steps of protein synthesis. J. Biol. Chem. 271 (1996) 23105-23110
41. Tamarit J., Cabiscol E., and Ros J. Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J. Biol. Chem. 273 (1998) 3027-3032
42. Cabiscol E., Piulats E., Echave P., Herrero E., and Ros J. Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. J. Biol. Chem. 275 (2000) 27393-27398
43. Dukan S., and Nyström T. Oxidative stress defense and deterioration of growth-arrested Escherichia coli cells. J. Biol. Chem. 274 (1999) 26027-26032
44. Parrado J., Absi E.H., Machado A., and Ayala A. "In vitro" effect of cumene hydroperoxide on hepatic elongation factor-2 and its protection by melatonin. Biochim. Biophys. Acta 1624 (2003) 139-144
45. Klein R.R., and Mullet J.E. Control of gene expression during higher plant chloroplast biogenesis: protein synthesis and transcript levels of psbA, psaA-psaB, and rbcL in dark-grown and illuminated barley seedlings. J. Biol. Chem. 262 (1987) 4341-4348
46. Zhang L., and Aro E.-M. Synthesis, membrane insertion and assembly of the chloroplast-encoded D1 protein into photosystem II. FEBS Lett. 512 (2002) 13-18
47. Trebitsh T., and Danon A. Translation of chloroplast psbA mRNA is regulated by signals initiated by both photosystems II and I. Proc. Natl. Acad. Sci. U. S. A. 21 (2001) 12289-12294
48. Tyystjärvi T., Herranen M., and Aro E.-M. Regulation of translation elongation in cyanobacteria: membrane targeting of the ribosome nascent-chain complexes controls the synthesis of D1 protein. Mol. Microbiol. 40 (2001) 476-484
49. Tyystjärvi T., Sirpio S., and Aro E.-M. Post-transcriptional regulation of the psbA gene family in the cyanobacterium Synechococcus sp. PCC 7942. FEBS Lett. 576 (2004) 211-215
50. Danon A., and Mayfield S.P. Light-regulated translation of chloroplast messenger RNAs through redox potential. Science 266 (1994) 1717-1719
51. Trebitsh T., Levitan A., Sofer A., and Danon A. Translation of chloroplast psbA mRNA is modulated in the light by counteracting oxidizing and reducing activities. Mol. Cell. Biol. 20 (2000) 1116-1123
52. Kuroda H., Kobayashi K., Kaseyama H., and Satoh K. Possible involvement of a low redox potential component(s) downstream of photosystem I in the translational regulation of the D1 subunit of the photosystem II reaction center in isolated pea chloroplasts. Plant Cell Physiol. 37 (1996) 754-761
53. Zhang L., Paakkarinen V., van Wijk K.J., and Aro E.-M. Biogenesis of the chloroplast-encoded D1 protein: regulation of translation elongation, insertion, and assembly into photosystem II. Plant Cell 12 (2000) 1769-1781
54. Mühlbauer S.K., and Eichacker L.A. Light-dependent formation of the photosynthetic proton gradient regulates translation elongation in chloroplasts. J. Biol. Chem. 273 (1998) 20935-20940
55. Allakhverdiev S.I., Nishiyama Y., Takahashi S., Miyairi S., Suzuki I., and Murata N. Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem II in Synechocystis. Plant Physiol. 137 (2005) 263-273
56. Kuroda H., Inagaki N., and Satoh K. The level of stromal ATP regulates translation of the D1 protein in isolated chloroplasts. Plant Cell Physiol. 33 (1992) 33-39
57. Yamazaki D., Motohashi K., Kasama T., Hara Y., and Hisabori T. Target proteins of the cytosolic thioredoxins in Arabidopsis thaliana. Plant Cell Physiol. 45 (2004) 18-27
58. Lee H.Y., Hong Y.N., and Chow W.S. Photoinactivation of photosystem II complex and photoprotection by non-functional neighbours in Capsicum annuum L. leaves. Planta 212 (2001) 332-342
59. Wydrzynski T., Hillier W., and Messinger J. On the functional significance of substrate accessibility in the photosynthetic water oxidation mechanism. Physiol. Plant. 96 (1996) 342-350
60. Anderson J.M. Does functional photosystem II complex have an oxygen channel?. FEBS Lett. 488 (2001) 1-4
61. Tyystjärvi E., Hakala M., and Sarvikas P. Mathematical modelling of the light response curve of photoinhibition of photosystem II. Photosynth. Res. 84 (2005) 21-27
62. Jones L.W., and Kok B. Photoinhibition of chloroplast reactions. I. Kinetics and action spectra. Plant Physiol. 41 (1966) 1037-1043
63. Jung J., and Kim H.S. The chromophores as endogenous sensitizers involved in the photogeneration of singlet oxygen in spinach thylakoids. Photochem. Photobiol. 52 (1990) 1003-1009
64. Sarvikas P., Hakala M., Pätsikkä E., Tyystjärvi T., and Tyystjärvi E. Action spectrum of photoinhibition in leaves of wild type and npq1-2 and npq4-1 mutants of Arabidopsis thaliana. Plant Cell Physiol. 47 (2006) 391-400
65. Baffert C., Collomb M.-N., Deronzier A., Pécaut J., Limburg J., Crabtree R.H., and Brudvig G.W. 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 (2002) 1404-1411
66. 6. Inorg. Chem. 42 (2003) 2849-2858
67. Zsiros O., Allakhverdiev S.I., Higashi S., Watanabe M., Nishiyama Y., and Murata N. Very strong UV-A light temporally separates the photoinhibition of photosystem II into light-induced inactivation and repair. Biochim. Biophys. Acta 1757 (2006) 123-129
68. Klimov V.V., Allakhverdiev S.I., Demeter S., and Krasnovsky A.A. Photoreduction of pheophytin in the photosystem II of chloroplasts depending on the oxidation-reduction potential of the medium. Dokl. Akad. Nauk Ukr. SSR 249 (1979) 227-230
69. Long S.P., Humphries S., and Falkowski P.G. Photoinhibition of photosynthesis in nature. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45 (1994) 633-662
70. Takahashi S., and Murata N. Interruption of the Calvin cycle inhibits the repair of photosystem II from photodamage. Biochim. Biophys. Acta 1708 (2005) 352-361
71. 2 fixation in the Calvin cycle, is critical for the synthesis of the D1 protein of photosystem II. Biochim. Biophys. Acta 1757 (2006) 198-205
72. Boyer J.S. Plant productivity and environment. Science 218 (1982) 443-448
73. Hagemann M., and Erdmann N. Environmental stresses. In: Rai A.K. (Ed). Cyanobacterial Nitrogen Metabolism and Environmental Biotechnology (1997), Springer-Verlag, Heidelberg, Germany 156-221
74. Sharma P.K., and Hall D.O. Interaction of salt stress and photoinhibition on photosynthesis in barley and sorghum. J. Plant Physiol. 138 (1991) 614-619
75. Hertwig B., Streb P., and Feierabend J. Light dependence of catalase synthesis and degradation in leaves and the influence of interfering stress conditions. Plant Physiol. 100 (1992) 1547-1553
76. Neale P.J., and Melis A. Salinity-stress enhances photoinhibition of photosystem II in Chlamydomonas reinhardtii. J. Plant Physiol. 134 (1989) 619-622
77. Lu C.-M., and Zhang J.-H. Effects of salt stress on PSII function and photoinhibition in the cyanobacterium Spirulina platensis. J. Plant Physiol. 155 (1999) 740-745
78. Allakhverdiev S.I., Nishiyama Y., Suzuki I., Tasaka Y., and Murata N. Genetic engineering of the unsaturation of fatty acids in membrane lipids alters the tolerance of Synechocystis to salt stress. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 5862-5867
79. Allakhverdiev S.I., Nishiyama Y., Miyairi S., Yamamoto H., Inagaki N., Kanesaki Y., and Murata N. Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiol. 130 (2002) 1443-1453
80. Wingler A., Lea P.J., Quick W.P., and Leegood R.C. Photorespiration: metabolic pathways and their role in stress protection. Philos. Trans. R. Soc. Lond., B 355 (2000) 1517-1529
81. Nomura M., Hibino T., Takabe T., Sugiyama T., Yokota A., Miyake H., and Takabe T. Transgenically produced glycinebetaine protects ribulose 1,5-bisphosphate carboxylase/oxygenase from inactivation in Synechococcus sp. PCC 7942 under salt stress. Plant Cell Physiol. 39 (1998) 425-432
82. Demmig-Adams B., and Adams III W.W. Antioxidants in photosynthesis and human nutrition. Science 298 (2002) 2149-2153
83. Niyogi K.K., Li X.-P., Rosenberg V., and Jung H.-S. Is PsbS the site of non-photochemical quenching in photosynthesis?. J. Exp. Bot. 56 (2005) 375-382
84. Bugos R.C., and Yamamoto H.Y. Molecular cloning of violaxanthin de-epoxidase from romaine lettuce and expression in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 6320-6325
85. Li X.-P., Björkman O., Shih C., Grossman A.R., Rosenquist M., Jansson S., and Niyogi K.K. A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403 (2000) 391-395
86. Li X.-P., Müller-Moulé P., Gilmore A.M., and Niyogi K.K. PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 15222-15227
87. Tyystjärvi E., King N., Hakala M., and Aro E.-M. Artificial quenchers of chlorophyll fluorescence do not protect against photoinhibition. J. Photochem. Photobiol. 48 (1999) 142-147
88. Santabarbara S., Barbato R., Zucchelli G., Garlaschi F.M., and Jennings R.C. The quenching of photosystem II fluorescence does not protect the D1 protein against light induced degradation in thylakoids. FEBS Lett. 505 (2001) 159-162
89. Nishiyama Y., Allakhverdiev S.I., and Murata N. Regulation by environmental conditions of the repair of photosystem II in cyanobacteria. In: Demmig-Adams B., Adams III W.W., and Mattoo A.K. (Eds). Photoprotection, Photoinhibition, Gene Regulation and Environment (2005), Springer, The Netherlands 193-203