Photoinhibition of photosystem II under environmental stress

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1767, Issue 6, 2007, Pages 414-421

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

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c EHIME UNIVERSITY   (Japan)

^d INSTITUTE OF BASIC BIOLOGICAL PROBLEMS   (Russian Federation)

Author keywords

Environmental stress; Photodamage; Photoinhibition; Photosystem II; Protein synthesis; Repair

Indexed keywords

CARBON DIOXIDE; REACTIVE OXYGEN METABOLITE; SODIUM CHLORIDE;

CARBON DIOXIDE FIXATION; ENVIRONMENTAL STRESS; LIGHT STRESS; NONHUMAN; OXIDATIVE STRESS; PHOTOINHIBITION; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; SALT STRESS; SYNECHOCYSTIS; TEMPERATURE STRESS;

ADAPTATION, PHYSIOLOGICAL; ENVIRONMENT; LIGHT; MODELS, BIOLOGICAL; PHOTOSYSTEM II PROTEIN COMPLEX;

EID: 34249787332     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2006.11.019     Document Type: Review

References (102)

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 process. In: Barber J. (Ed). 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 Anderson B. (Eds). Regulation of Photosynthesis (2001), Kluwer Academic, 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 Biol. Sci. 357 (2002) 1421-1430
8. 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
9. Moon B.Y., Higashi S.I., 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
10. Vass I., Styring S., Hundal T., Koivuniemi A., Aro E.M., and Andersson B. Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 1408-1412
11. Keren N., Berg A., VanKan 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
12. Allakhverdiev S.I., and Murata N. Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim. Biophys. Acta 1657 (2004) 23-32
13. 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
14. Nishiyama Y., Allakhverdiev S.I., Yamamoto H., Hayashi H., and Murata N. Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43 (2004) 11321-11330
15. 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
16. Lee H.Y., Hong Y.N., and Chow W.S. Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves. Planta 212 (2001) 332-342
17. Jones L.W., and Kok B. Photoinhibition of chloroplast reactions: I. Kinetics and action spectra. Plant Physiol. 41 (1966) 1037-1043
18. 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
19. 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
20. Särvikas 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
21. 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
22. 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
23. 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
24. Nishiyama Y., Allakhverdiev S.I., and Murata N. A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim. Biophys. Acta 1757 (2006) 742-749
25. Berry J., and Björkman O. Photosynthetic response and adaptation to temperature in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 31 (1980) 491-543
26. Demmig-Adams B., and Adams W.W. Photoprotection and other responses of plants to high-light stress. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43 (1992) 599-626
27. Jones L.W., and Kok B. Photoinhibition of chloroplast reactions: II. Multiple effects. Plant Physiol. 41 (1966) 1044-1049
28. Boyer J.S., and Bowen B.L. Inhibition of oxygen evolution in chloroplasts isolated from leaves with low water potentials. Plant Physiol. 45 (1970) 612-615
29. Keck R.W., and Boyer J.S. Chloroplast response to low leaf water potentials: III. Differing inhibition of electron transport and photophosphorylation. Plant Physiol. 53 (1974) 474-479
30. Björkman O., and Powles S.B. Inhibition of photosynthetic reactions under water stress: interaction with light level. Planta 161 (1984) 490-504
31. Melis A. Photosystem II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo?. Trends Plant Sci. 4 (1999) 130-135
32. Keren N., and Ohad I. State transition and photoinhibition. In: Rochaix J.D., Goldschmidt-Clermont M., and Merchant S. (Eds). The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas (1998), Kluwer Academic Publishers, Dordrecht, The Netherlands 569-596
33. Adir N., Zer H., Shochat S., and Ohad I. Photoinhibition: a historical perspective. Photosynth. Res. 76 (2003) 343-370
34. 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
35. Takahashi S., Nakamura T., Sakamizu M., Van Woesik R., and Yamasaki H. Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol. 45 (2004) 251-255
36. Jegerschjöld C., Virgin I., and Styring S. Light-dependent degradation of the D1 protein in photosystem II is accelerated after inhibition of the water-splitting reaction. Biochemistry 29 (1990) 6179-6186
37. Kirilovsky D., Rutherford A.W., and Etienne A.L. Influence of DCMU and ferricyanide on photodamage in photosystem II. Biochemistry 33 (1994) 3087-3095
38. Krause G.H., and Behrend U. ΔPH-dependent chlorophyll fluorescence quenching indicating a mechanism of protection against photoinhibition of chloroplasts. FEBS Lett. 200 (1986) 298-302
39. Barr P., Young A.J., and Britton G. Photodestruction of pigments in higher plants by herbicide action: I. The effect of DCMU (diuron) on isolated chloroplasts. J. Exp. Bot. 41 (1990) 123-134
40. Krause G.H. The role of oxygen in photoinhibition of photosynthesis. In: Foyer C.H., and Mullineaux P.M. (Eds). Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants (1994), CRC Press, Boca Raton, FL 43-77
41. Komenda J., and Masojidek J. The effect of photosystem II inhibitors DCMU and BNT on the high-light induced D1 turnover in two cyanobacterial strains, Synechocystis PCC 6803 and Synechococcus PCC 7942. Photosynth. Res. 57 (1998) 193-202
42. Kyle D.J., Ohad I., and Arntzen C.J. Membrane protein damage and repair: selective loss of a quinone protein function in chloroplast membranes. Proc. Natl. Acad. Sci. U. S. A. 81 (1984) 4070-4074
43. Zer H., and Ohad I. Photoinactivation of photosystem II induces changes in the photochemical reaction center II abolishing the regulatory role of the QB site in the D1 protein degradation. Eur. J. Biochem. 231 (1995) 448-453
44. 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
45. Mattoo A.K., Hoffman-Falk H., Marder J.B., and Edelman M. Regulation of protein metabolism: coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes. Proc. Natl. Acad. Sci. U. S. A. 81 (1984) 1380-1384
46. 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. 98 (2001) 12289-12294
47. 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
48. Kuroda H., Kobashi 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
49. 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
50. Gold L. Posttranscriptional regulatory mechanisms in Escherichia coli. Annu. Rev. Biochem. 57 (1988) 199-233
51. Sicher R.C. Glycolaldehyde inhibition of photosynthetic carbon assimilation by isolated chloroplasts and protoplasts. In: Sybesma C. (Ed). Advances in Photosynthetic Research vol. 3 (1984), W. Junk, Hague 413-416
52. 2 fixation in the cyanobacterium Synechococcus UTEX 625 without inhibiting the accumulation of inorganic carbon or the associated quenching of chlorophyll a fluorescence. Plant Physiol. 91 (1989) 1044-1049
53. 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
54. 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
55. 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
56. 2 assimilation. Plant Physiol. 58 (1976) 336-340
57. Radmer R., and Ollinger O. Light-driven uptake of oxygen, carbon dioxide, and bicarbonate by the green alga Scenedesmus. Plant Physiol. 65 (1980) 723-729
58. 2 in intact spinach chloroplasts: evidence for scavenging of hydrogen peroxide by peroxidase. Plant Cell Physiol. 25 (1984) 1169-1179
59. Allahverdiyeva Y., Mamedov F., Mäenpää P., Vass I., and Aro E.M. Modulation of photosynthetic electron transport in the absence of terminal electron acceptors: characterization of the rbcL deletion mutant of tobacco. Biochim. Biophys. Acta 1709 (2005) 69-83
60. Wiese C., Shi L.B., and Heber U. Oxygen reduction in the Mehler reaction is insufficient to protect photosystems I and II of leaves against photoinactivation. Physiol. Plant. 102 (1998) 437-446
61. Nash D., Miyao M., and Murata N. Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese. Biochim. Biophys. Acta 807 (1985) 127-133
62. Warner M.E., Fitt W.K., and Schmidt G.W. Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 8007-8012
63. Tchernov D., Gorbunov M.Y., de Vargas C., Yadav S.N., Milligan A.J., Haggblom M., and Falkowski P.G. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 13531-13535
64. X. Yang, X. Wen, H. Gong, Q. Lu, Z. Yang, Y. Tang, Z. Liang, C. Lu, Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants, Planta (in press).
65. Weis E. The temperature-sensitivity of dark inactivation and light activation of the ribulose-1,5-bisphosphate carboxylase in spinach chloroplasts. FEBS Lett. 129 (1981) 197-200
66. Weis E. Reversible heat inactivation of the Calvin cycle: a possible mechanism of the temperature regulation of photosynthesis. Planta 151 (1981) 33-39
67. Weis E. Influence of light on the heat sensitivity of the photosynthetic apparatus in isolated spinach chloroplasts. Plant Physiol. 70 (1982) 1530-1534
68. Feller U., Crafts-Brandner S.J., and Salvucci M.E. Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase-mediated activation of Rubisco. Plant Physiol. 116 (1998) 539-546
69. Law R.D., and Crafts-Brandner S.J. Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol. 120 (1999) 173-181
70. Eckardt N.A., and Portis A.R. Heat-denaturation profiles of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase and the inability of Rubisco activase to restore activity of heat-denatured Rubisco. Plant Physiol. 113 (1997) 243-248
71. 2. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 13430-13435
72. Boyer J.S. Plant productivity and environment. Science 218 (1982) 443-448
73. Neale P.J., and Melis A. Salinity stress enhances photoinhibition of photosynthesis in Chlamydomonas reinhardtii. J. Plant Physiol. 134 (1989) 619-622
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. 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
77. 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
78. Brady C.J., Gibson T.S., Barlow E.W.R., Speirs J., and Jones R.G.W. Salt tolerance in plants: I. Ions, compatible organic solutes and the stability of plant ribosomes. Plant Cell Environ. 7 (1984) 571-578
79. Gibson T.S., Speirs J., and Brady C.J. Salt tolerance in plants: II. In vitro translation of mRNAs from salt-tolerant and salt-sensitive plants on wheat germ ribosomes: responses to ions and compatible organic solutes. Plant Cell Environ. 7 (1984) 579-587
80. + transport in higher plants. Ann. Bot. 91 (2003) 503-527
81. Solomon A., Beer S., Waisel Y., Jones G.P., and Paleg L.G. Effects of NaCl on the carboxylating activity of Rubisco from Tamarix jordanis in the presence and absence of proline-related compatible solutes. Physiol. Plant. 90 (1994) 198-204
82. Öquist G., and Huner N.P.A. Photosynthesis of overwintering evergreen plants. Annu. Rev. Plant Biol. 54 (2003) 329-355
83. Öquist G., and Huner N.P.A. Effects of cold acclimation on the susceptibility of photosynthesis to photoinhibition in Scots pine and in winter and spring cereals: a fluorescence analysis. Funct. Ecol. 5 (1991) 91-100
84. Öquist G., Hurry V.M., and Huner N.P.A. Low-temperature effects on photosynthesis and correlation with freezing tolerance in spring and winter cultivars of wheat and rye. Plant Physiol. 101 (1993) 245-250
85. Kanervo E., Tasaka Y., Murata N., and Aro E.M. Membrane lipid unsaturation modulates processing of the photosystem II reaction-center protein D1 at low temperatures. Plant Physiol. 114 (1997) 841-849
86. Chen T.H.H., and Murata N. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr. Opin. Plant Biol. 5 (2002) 250-257
87. Hayashi H., Alia, Mustardy L., Deshnium P., Ida M., and Murata N. Transformation of Arabidopsis thaliana with the codA gene for choline oxidase; accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. Plant J. 12 (1997) 133-142
88. Hayashi H., Alia, Sakamoto A., Nonaka H., Chen T.H.H., and Murata N. Enhanced germination under high-salt conditions of seeds of transgenic Arabidopsis with a bacterial gene (codA) for choline oxidase. J. Plant Res. 111 (1998) 357-362
89. Alia, Hayashi H., Sakamoto A., and Murata N. Enhancement of the tolerance of Arabidopsis to high temperatures by genetic engineering of the synthesis of glycinebetaine. Plant J. 16 (1998) 155-161
90. Alia, Hayashi H., Chen T.H.H., and Murata N. Transformation with a gene for choline oxidase enhances the cold tolerance of Arabidopsis during germination and early growth. Plant Cell Environ. 21 (1998) 232-239
91. Alia, Kondo Y., Sakamoto A., Nonaka H., Hayashi H., Saradhi P.P., Chen T.H.H., and Murata N. Enhanced tolerance to light stress of transgenic Arabidopsis plants that express the codA gene for a bacterial choline oxidase. Plant Mol. Biol. 40 (1999) 279-288
92. Sakamoto A., and Murata N. The use of bacterial choline oxidase, a glycinebetaine-synthesizing enzyme, to create stress-resistant transgenic plants. Plant Physiol. 125 (2001) 180-188
93. Sakamoto A., and Murata N. The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ. 25 (2002) 163-171
94. Sulpice R., Tsukaya H., Nonaka H., Mustardy L., Chen T.H.H., and Murata N. Enhanced formation of flowers in salt-stressed Arabidopsis after genetic engineering of the synthesis of glycine betaine. Plant J. 36 (2003) 165-176
95. Park E.J., Jeknic Z., Sakamoto A., DeNoma J., Yuwansiri R., Murata N., and Chen T.H.H. Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. Plant J. 40 (2004) 474-487
96. Deshnium P., Los D.A., Hayashi H., Mustardy L., and Murata N. Transformation of Synechococcus with a gene for choline oxidase enhances tolerance to salt stress. Plant Mol. Biol. 29 (1995) 897-907
97. Deshnium P., Gombos Z., Nishiyama Y., and Murata N. The action in vivo of glycine betaine in enhancement of tolerance of Synechococcus sp. strain PCC 7942 to low temperature. J. Bacteriol. 179 (1997) 339-344
98. Ohnishi N., and Murata N. Glycinebetaine counteracts the inhibitory effects of salt stress on the degradation and synthesis of D1 protein during photoinhibition in Synechococcus sp. PCC 7942. Plant Physiol. 141 (2006) 758-765
99. Papageorgiou G.C., and Murata N. The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving photosystem II complex. Photosynth. Res. 44 (1995) 243-252
100. Yang X., Liang Z., and Lu C. Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants. Plant Physiol. 138 (2005) 2299-2309
101. Barrs H.D. Cyclic variations in stomatal aperture, transpiration, and leaf water potential under constant environmental conditions. Annu. Rev. Plant Physiol. 22 (1971) 223-236
102. 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 Biol. Sci. 355 (2000) 1517-1529