Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803

Biochemistry

Volumn 43, Issue 35, 2004, Pages 11321-11330

  Nishiyama, Yoshitaka ^a,c   Allakhverdiev, Suleyman I ^b,c   Yamamoto, Hiroshi ^c   Hayashi, Hidenori ^a   Murata, Norio ^c,d  

^a EHIME UNIVERSITY   (Japan)

^b INSTITUTE OF BASIC BIOLOGICAL PROBLEMS   (Russian Federation)

^c NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^d GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PHOTOSYSTEMS; SUBCELLULAR LOCALIZATION;

PHOTOSYNTHESIS; PROTEINS; RNA;

BIOCHEMISTRY;

CHLORAMPHENICOL; EOSIN; ETHYLEOSIN; PHOTOSENSITIZING AGENT; ROSE BENGAL; SINGLET OXYGEN; UNCLASSIFIED DRUG;

ARTICLE; CELL LABELING; CONTROLLED STUDY; GENE; IN VIVO STUDY; INHIBITION KINETICS; MOLECULAR BIOLOGY; NONHUMAN; NORTHERN BLOTTING; OXIDATIVE STRESS; PHOTOSENSITIZATION; PHOTOSYNTHESIS; PHOTOSYSTEM II; PRIORITY JOURNAL; PSBA GENE; RNA ANALYSIS; RNA TRANSLATION; SYNECHOCYSTIS; SYNECHOCYSTIS SP. PCC 6803; TARGET CELL; TRANSLATION REGULATION;

CYANOBACTERIA; DNA REPAIR; ELECTRON SPIN RESONANCE SPECTROSCOPY; EOSINE YELLOWISH-(YS); GENE EXPRESSION REGULATION, BACTERIAL; LIGHT; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PHOTOCHEMISTRY; PHOTOSENSITIZING AGENTS; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, MESSENGER; ROSE BENGAL; SINGLET OXYGEN;

NEGIBACTERIA; SYNECHOCYSTIS; SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

EID: 4444313478     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi036178q     Document Type: Article

References (44)

1. Halliwell, B., and Gutteridge, J. M. C. (1990) Role of free radicals and catalytic metal ions in human disease: an overview, Methods Enzymol. 186, 1-88.
2. Knox, J. P., and Dodge, A. D. (1985) Singlet oxygen and plants, Phytochemistry 24, 889-896.
3. Asada, K. (1996) Radical Production and Scavenging in the Chloroplasts, in Photosynthesis and the Environment (Baker, N. R., Ed.) pp 123-150, Kluwer Academic Publishers, Dordrecht, The Netherlands.
4. Asada, K. (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons, Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 601-639.
5. Prásil, O., Adir, N., and Ohad, I. (1992) Dynamics of Photosystem II: Mechanism of Photoinhibition and Recovery Processes, in Topics in Photosynthesis, The Photosystems: Structure, Function and Molecular Biology (Barber, J., Ed.) Vol. 11, pp 295-348, Elsevier Science Publishers, Amsterdam, The Netherlands.
6. Aro, E.-M., Virgin, I., and Andersson, B. (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover, Biochim. Biophys. Acta 1143, 113-134.
7. Andersson, B., and Aro, E.-M. (2001) Photodamage and D1 Protein Turnover in Photosystem II, in Regulation of Photosynthesis (Aro, E.-M., and Andersson, B., Eds.) pp 377-393, Kluwer Academic Publishers, Dordrecht, The Netherlands.
8. Vass, I., Styring, S., Hundal, T., Koivuniemi, A., Aro, E.-M., and Andersson, B. (1992) The reversible and irreversible intennediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation, Proc. Natl. Acad. Sci. U.S.A. 89, 1408-1412.
9. Keren, N., Berg, A., van Kan, P. J. M., 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. U.S.A. 94, 1579-1584.
10. Telfer, A., Bishop, S. M., Phillips, D., and Barber, J. (1994) 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, 13244-13253.
11. Hideg, E., Spetea, C., and 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.
12. Hideg, E., Kálai, T., Hideg, K., and Vass, I. (1998) Photoinhibition of photosynthesis in vivo results in singlet oxygen production: detection via nitroxide-induced fluorescence quenching in broad bean leaves, Biochemistry 37, 11405-11411.
13. Okada, K., Ikeuchi, M., Yamamoto, N., Ono, T., and Miyao, M. (1996) 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, 73-79.
14. 2 evolution with lauroylcholine chloride, Biochim. Biophys. Acta 1100, 303-311.
15. Chen, G.-X., Kazimir, J., and Cheniae, G. M. (1992) Photoinhibition of hydroxylamine-extracted photosystem II membranes: studies of the mechanism, Biochemistry 31, 11072-11083.
16. Miyao, M., Ikeuchi, M., Yamamoto, N., and 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.
17. Ohad, I., Kyle, D. J., and Arntzen, C. J. (1984) Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptide in chloroplast membranes, J. Cell Biol. 99, 481-485.
18. Mattoo, A. K., Marder, J. B., and Edelman, M. (1989) Dynamics of the photosystem II reaction center, Cell 56, 241-246.
19. Anbudurai, P. R., Mor, T. S., Ohad, I., Shestakov, S. V., and Pakrasi, H. B. (1994) 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, 8082-8086.
20. Inagaki, N., Yamamoto, Y., and Satoh, K. (2001) A sequential two-step proteolytic process in the carboxy-terminal truncation of precursor D1 protein in Synechocystis sp. PCC 6803, FEBS Lett. 509, 197-201.
21. Nishiyama, Y., Yamamoto, H., Allakhverdiev, S. I., Inaba, M., Yokota, A., and Murata, N. (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery, EMBO J. 20, 5587-5594.
22. Gombos, Z., Wada, H., and Murata, N. (1994) 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, 8787-8791.
23. Arnon, D. I., McSwain, B. D, Tsujimoto, H. Y., and Wada, K. (1974) Photochemical activity and components of membrane preparations from blue-green algae. I. Coexistence of two photosystems in relation to chlorophyll a and removal of phycocyanin, Biochim. Biophys. Acta 357, 231-245.
24. Lion, Y., Delmelle, M., and van de Vorst, A. (1976) New method of detecting singlet oxygen production, Nature 263, 442-443.
25. Lion, Y., Gandin, E., and van de Vorst, A. (1980) On the production of nitroxide radicals by singlet oxygen reaction: An EPR study, Photochem. Photobiol. 31, 305-309.
26. Blumwald, E., Mehlhorn, R. J., and Packer, L. (1983) Studies of osmoregulation in salt adaptation of cyanobacteria with ESP spin-probe techniques, Proc. Natl. Acad. Sci. U.S.A. 80, 2599-2602.
27. Nishiyama, Y., Los, D. A., and Murata, N. (1999) PsbU, a protein associated with photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus species PCC 7002, Plant Physiol. 120, 301-308.
28. Los, D. A., Ray, M., and Murata, N. (1997) Differences in the control of the temperature-dependent expression of four genes for desaturases in Synechocystis sp. PCC 6803, Mol. Microbiol. 25, 1167-1175.
29. Jansson, C., Debus, R. J., Osiewacz, H. D., Gurevitz, M., and McIntosh, L. (1987) Construction of an obligate photoheterotrophic mutant of the cyanobacterium Synechocystis 6803. Inactivation of the psbA gene family, Plant Physiol. 85, 1021-1025.
30. Tyystjärvi, T., Tyystjärvi, E., Ohad, I., and Aro, E.-M. (1998) Exposure of Synechocystis 6803 cells to series of single turnover flashes increases the psbA transcript level by activating transcription and down-regulating psbA mRNA degradation, FEBS Lett. 436, 483-487.
31. Tyystjärvi, T., Herranen, M., and Aro, E.-M. (2001) Regulation of translation elongation in cyanobacteria: membrane targeting of the ribosome nascent-chain complexes controls the synthesis of D1 protein, Mol. Microbiol. 40, 476-484.
32. Park, Y.-I., Chow, W. S., and Anderson, J. M. (1995) Light inactivation of photosystem II in leaves of peas grown in moderate light depends on photon exposure, Planta 196, 401-411.
33. Tyystjärvi, E., and Aro, E.-M. (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity, Proc. Natl. Acad. Sci. U.S.A. 93, 2213-2218.
34. Tyystjärvi, E., Kairavuo, M., Pätsikkä, E., Keränen, M., Khriachtchev, L., Tuominen, I., Guiamet, J. J., and Tyystjärvi, T. (2001) The Quantum Yield of Photoinhibition Is the Same in Flash Light and under Continuous Illumination: Implication for the Mechanism, in Proceedings of the 12th International Congress of Photosynthesis (Critchley, C., Ed.) S8-P032, CSIRO Publishing, Melbourne, Australia.
35. Wydrzynski, T., Hillier, W., and Messinger, J. (1996) On the functional significance of substrate accessibility in the photosynthetic water oxidation mechanism, Physiol. Plant 96, 342-350.
36. Anderson, J. M. (2001) Does functional photosystem II complex have an oxygen channel? FEBS Lett. 488, 1-4.
37. Allakhverdiev, S. I., Nishiyama, Y., Suzuki, I., Tasaka, Y., and Murata, N. (1999) 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, 5862-5867.
38. Allakhverdiev, S. I., Nishiyama, Y., Miyairi, S., Yamamoto, H., Inagaki, N., Kanesaki, Y., and 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.
39. Komenda, J., and Barber, J. (1995) Comparison of psbO and psbH deletion mutants of Synechocystis PCC 6803 indicates that degradation of D1 protein is regulated by the QB site and dependent on protein synthesis, Biochemistry 34, 9625-9631.
40. Zolla, L., and Rinalducci, S. (2002) Involvement of active oxygen species in degradation of light-harvesting proteins under light stresses, Biochemistry 41, 14391-14402.
41. Chung, S. K., and Jung, J. (1995) Inactivation of the acceptor side and degradation of the D1 protein of photosystem II by singlet oxygen photogenerated from the outside, Photochem. Photobiol. 61, 383-389.
42. Tamarit, J., Cabiscol, E., and Ros, J. (1998) Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress, J. Biol. Chem. 273, 3027-3032.
43. Dukan, S., and Nyström, T. (1999) Oxidative stress defense and deterioration of growth-arrested Escherichia coli cells, J. Biol. Chem. 274, 26027-26032.
44. Ayala, A., Parrado, J., Bougria, M., and Machado, A. (1996) Effect of oxidative stress, produced by cumene hydroperoxide, on the various steps of protein synthesis, J. Biol. Chem. 271, 23105-23110.