Molecular mechanisms of stress resistance of photosynthetic apparatus

Biologicheskie Membrany

Volumn 24, Issue 3, 2007, Pages 195-217

  Kreslavski, V D ^a   Carpentier, R ^b   Klimov, V V ^a   Murata, N ^c   Allakhverdiev, S I ^a  

^a INSTITUTE OF BASIC BIOLOGICAL PROBLEMS   (Russian Federation)

^b UNIVERSITÉ DU QUÉBEC À TROIS RIVIÈRES   (Canada)

^c NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 34547153275     PISSN: 02334755     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (212)

1. Thomashow M.F. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms // Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999. V. 50. P. 571-599.
2. Allakhverdiev S.I., Sakamoto A., Nishiyama Y., Inaba M., Murata N. Ionic and osmotic effects of NaCl-in-duced inactivation of photosystems I and II in Synechococcus sp. // Plant Physiol. 2000a. V. 123. P. 1047-1056.
3. Allakhverdiev S.I., Sakamoto A., Nishiyama Y., Murata N. Inactivation of photosystems I and II in response to osmotic stress in Synechococcus: contribution of water channels // Plant Physiol. 2000b. V. 122. P. 1201-1208.
4. Wada H., Gombos Z., Murata N. Enhancement of chilling tolerance of a cyanobacterium by genetic manipulation of fatty acid desaturation // Nature. 1990. V. 347. P. 200-203.
5. Gombos Z., Wada H., 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. Sei. USA. 1994a. V. 91. No 19. P. 8787-8791.
6. Gombos Z., Wada H., Hideg E., Murata N. The unsaturation of membrane lipids stabilizes photosynthesis against heat stress // Plant Physiol. 1994b. V. 104. P. 563-567.
7. Russian source
8. Allakhverdiev S.I., Nishiyama Y., Suzuki I., Tasaka Y., Murata N. Genetic engineering of the unsaturation of fatty acids in membrane lipids alters the tolerance of Synechocvstis to salt stress // Proc. Natl. Acad. Sci. USA. 1999. V. 96. P. 5862-5867.
9. Allakhverdiev S.I., Kinoshita M., Inaba M., Suzuki I., Murata N. Unsaturation fatty acids in membrane lipids protect the photosynthetic machinery against salt-induced damage in Synechococcus sp. // Plant Physiol. 2001. V. 125. P. 1842-1853.
10. Allakhverdiev S.I., Tsvetkova N., Mohanty P., Szalontai., Moon B.Y., Debreczeny M., Murata N. Irreversible photoinhibition of photosystem II is caused by exposure of Synechocystis cells to strong light for a prolonged period // Biochem. et biophys. acta. 2005a. V. 1708. P. 342-351.
11. Sharkey T.D. Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene // Plant Cell Env. 2005. V. 28. P. 269-277.
12. Foyer C.H., Descourvieres P., Kunert K.J. Protection against oxygen radicals: an important defense mechanism studied in transgenic plants // Plant Cell Environ. 1994a. V. 17. P. 507-523.
13. Foyer C.H., Lelandais M., Kunert K.J. Photooxidative stress in plants // Physiol. Plant. 1994b. V. 92. P. 696-717.
14. Foyer C.H., Lopez-Delgado H., Dat J.F., Scott I.M. Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling // Physiol. Plant. 1997. V. 100. P. 241-254.
15. Meloni D.A., Oliva M.A., Martinez C.A., Cambraia J. Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress // Environ. Exp. Bot. 2003. V. 49. P. 69-76.
16. Alscher R.G., Donahue J.L., Cramer C.L. Reactive oxygen species and antioxidants: relationships in green cells // Physiol. Plant. 1997. V. 100. P. 224-233.
17. Nishiyama Y., Yamamoto H., Allakhverdiev S.I., Inaba M., Yokota A., Murata N. Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery // EMBO J. 2001. V. 20. P. 5587-5594.
18. Nishiyama Y., Allakhverdiev S.I., Yamamoto H., Hayashi H., Murata N. Singlet oxygen inhibits the repair of photosystem II by suppressing the transport elongation of the D1 protein in Synechocystis sp. PCC 6803 // Biochemistry (USA). 2004. V. 43. P. 11321-11330.
19. Murata N., Takahashi S., Nishiyama Y., Allakhverdiev S.I. Photoinhibition of photosystem II under environmental stress // Biochem. et biophys acta. 2007. (in press).
20. Russian source
21. Asada K. Radical production and scavenging in the chloroplasts // Photosynthesis and the environment / Ed. Baker N.R. Dordrecht, Netherlands: Kluwer Acad. Publ., 1996. P. 123-150.
22. Demmig-Adams B., Adams W.W. Antioxidants in photosynthesis and human nutrition // Science. 2002. V. 298.P. 2149-2153.
23. El-Shitinawy F., Ebrahim M.K.H., Sewelam N., ElShourbagy M .N. Activity of photosystem 2, lipid peroxidation, and the enzymatic antioxidant protective system in heat shocked barley seedlings // Photosynthetica. 2004. V. 42. No 10. P. 15-21.
24. Russian source
25. Russian source
26. Berry J., Bjórkman O. Photosynthetic response and adaptation to temperature in higher plants // Annu. Rev. Plant Physiol. 1980. V. 31. P. 491-543.
27. 2 // J. Plant. Physiol. 2001. V. 158. P. 1125-1130.
28. Mallick N., Mohn F.H. Reactive oxygen species: Response of algal cells // J. Plant Physiol. 2000. V. 157. P. 183-193.
29. Nishiyama Y, Allakhverdiev S.I., Murata N. A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II // Biochem. et biophys. acta. 2006. V. 1757. P. 742-749.
30. Aro E.-M., Virgin I., Andersson B. Photoinhibition of photosystem II: inactivation, protein damage and turnover // Biochem. et biophys. acta. 1993. V. 1143. P. 113-134.
31. Andersson B., Aro E.-M. Photodamage and D1 protein turnover in photosystem II // Regulation of photosynthesis / Eds Aro E-M., Andersson B. Dordrecht, Netherlands: Kluwer Acad. Publ., 2001. P. 377-393.
32. - mutants of Synechocystis sp. PCC 6803 // Plant Cell Physiol. 2001. V. 42. No 8. P. 803-812.
33. Asada K. Production and action of active oxygen in photosynthetic tissue // Causes of photooxidative stress and amelioration of defense systems in plants / Eds Foyer C.H., Mullineaux P.M. Boca Raton, FL: CRC Press, 1994. P. 77-104.
34. Allen R. Dissection of oxidative stress tolerance using transgenic plants // Plant Physiol. 1995. V. 107. P. 1049-1054.
35. Storz G., Imlay J.A. Oxidative stress // Curr. Opin. Microbiol. 1999. V. 2. P. 188-194.
36. Alscher R.G., Erturk N., Heath L.S. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants // J. Exp. Bot. 2002. V. 53. No 372. P. 1331-1341.
37. Larson RA. The antioxidants in higher plants // Biochemistry. 1988. V. 27. P. 969-978.
38. Russian source
39. Quist G., Cambell D., Clarke A., Gustafsson P. The cyanobacterium Synechococcus modulates photomodulates photosystem II function in response to excitation stress through D1 exchange // Photosynth. Res. 1995. V. 46. P. 151-158.
40. Tichy M., Vermaas W. In vivo role of catalase-peroxidase in Synechocvstis sp. strain PCC 6803 // J. Bacteriol. 1999. V. 181. P. 1875-1882.
41. Los' D.A., Murata N. Responses to cold shock in cyanobacteria // J. Mol. Microbiol. Biotechnol. 1999. V. 1. P. 221-230.
42. Kok B. On inhibition of photosynthesis by intense light // Biochem. et biophys. acta. 1956. V. 21. P. 305-322.
43. Powles S.B. Photoinhibition of photosynthesis induced by visible light // Annu. Rev. Plant Physiol. 1984. V. 35. P. 15-14.
44. Barber J., Andersson B. Too much of a good thing: light can be bad for photosynthesis // Trends Biochem. Sci. 1992. V. 17. P. 61-66.
45. A species promote chlorophyll triplet formation // Proc. Natl Acad. Sci. USA. 1992. V. 89. P. 1408-1412.
46. Andersson B., Barber J. Mechanisms of photodamage and protein degradation during photoinhibition of photosystem II // Photosynthesis and the environment / Ed. Baker N.R. Dordrecht. Netherlands: Kluwer Acad. Publ., 1996. P. 101-121.
47. Zhang L., Paakkarinen V., van Wijk K.J., Aro E.-M. Biogenesis of the chloroplast-encoded D1 protein: regulation of mechanisms of D1 protein translation elongation, insertion and assembly // Plant Cell. 2000. V. 12. P. 1769-1781.
48. Mattoo A.K., Murder J.B.. Edelman M. Dynamics of photosystem two reaction center // Cell. 1989. V. 56. P. 241-246.
49. Nishiyama Y., Allakhverdiev S.I., Murata N. Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria // Photosynth. Res. 2005. V. 84. P. 1-7.
50. Allakhverdiev S.I., Nishiyama Y., Miyairi S., Yamamoto H., Inagaki N., Kanesaki Yu, Murata N. Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis // Plant Physiol. 2002. V. 130. P. 1443-1453.
51. Allakhverdiev S.I., Mohanty P., Murata N. Dissection of photodamage at low temperature and repair in darkness suggests the existence of an intermediate form of photodamaged photosystem II // Biochemistry. 2003a. V. 42. P. 14277-14283.
52. Allakhverdiev S.I., 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 // Biochem. et biophys. acta. 2004. V. 1657. P. 23-32.
53. Allakhverdiev S.J., Nishiyama Y., Takahashi S., Miyairi S., Suzuki J., Murata N. Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem II in Synechocystis H Plant Physiol. 2005b. V. 137. P. 263-273.
54. Allakhverdiev S.I., Klimov V.V., Hagemann M. Cellular energization protects the photosynthetic machinery against salt-induced inactivation in Synechococcus // Biochem. et biophys. acta. 2005c. V. 1708. P. 201-208.
55. Hakala M., Tuominen I., Keränen M., Tyystjärvi T., Tyystjärvi E. Evidence for the role of oxygen-evolving manganese complex in photoinhibition of photosystem II // Biochem. et biophys. acta. 2005. V. 1706. P. 68-80.
56. Ohnishi N., Allakhverdiev S.I., Takahashi S., Higachi S., Watanabe M., Nishiyama Y., 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 (USA). 2005. V. 44. P. 9494-8499.
57. Asada K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons// Annu. Rev. Plant Physiol. Plant MoI. Biol. 1999. V. 50. P. 601-639.
58. Miyao M., Ikeuchi M., Yamamoto N., 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. 1995. V. 34. P. 10019-10026.
59. Hideg E., Spetea C., Vass I. Singlet oxygen and free radical production during acceptor- and donor-side-induced photoinhibition. Studies with spin trapping EPR spectroscopy // Biochem. et biophys. acta. 1994. V. 1186. P. 143-152.
60. Okada K., Ikeuchi M., Yamamoto N., Ono T., Miyao M. Selective and specific cleavage of the Dl and D2 proteins of photosystem II by exposure to singlet oxygen: factors responsible for the susceptibility to cleavage of the proteins // Biochem. et biophys. acta. 1996. V. 1274. P. 73-79.
61. Yamamoto H., Miyake C., Dietz K.-J., Tomizawa K., Murata N., Yokota A. Thioredoxin peroxidase in the cyanobacterium Synechocvstis sp. PCC 6803 // FEBS Lett. 1999. V. 447. P. 269-273.
62. Allakhverdiev S.I., Setlikova E., Klimov V.V., Setlik I. In photoinhibited photosystem II particles pheophytin photoreduction remains unimpaired//FEBS Lett. 1987. V. 226.P. 186-190.
63. Klimov V.V., Schafiev M.A., Allakhverdiev S.I. Photoin-activation of the reactivation capacity of photosystem II in pea subchloroplast particles after a complete removal of manganese//Photosynth. Res. 1990. V. 23. P. 59-65.
64. Setlik I., Allakhverdiev S.I., Nedbal L., Setlikova E., Klimov V. V. Three types of photosystem II photoinactivation: 1. Damaging processes on acceptor side // Photosynth. Res. 1990. V. 23. P. 39-8.
65. Theg SM., Filar L.J., Dilley R.A. Phoinactivation of chloroplasts already inhibited on oxidizing side of photosystem II // Biochem. et biophys. acta. 1986. V. 849. P. 104-111.
66. Melis A. Photosystem II damage and repair cycle in chloroplasts: what modulates the rate of phtodamage in vivo Il Trends Plant Sci. 1999. V. 4. No 4. P. 130-135.
67. Keren N., Berg A., van Kan P.J.M., Levanon H., Ohad I. Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: the role of back electron flow // Proc. Natl. Acad. Sci. USA. 1997. V. 94. P. 1579-1584.
68. Tyystjärvi T., Tuominen I., Herranen M., Aro E.-M., Tyystjärvi E. Action spectrum of psbA gene transcription is similar to that of photoinhibition in Synechocystis sp. PCC 6803 // FEBS Lett. 2002. V. 516. P. 167-171.
69. Russian source
70. Krause G.H. Photoinhibition at photosynthesis. An evaluation of damaging and protective mechanisms // Physiol. Plant. 1988. V. 74. P. 566-574.
71. Havaux M., Tardy F., Ravenel J., Chanu D., Parot P. Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochromic shift in intact potato leaves: influence of the xanthophylls content // Plant Cell Environ. 1996. V. 19. P. 1359-1368.
72. Logan B.A., Demmig-Adams B., Adams W.W., Grace S.C. Antioxidants and xanthophyll cycle-dependent energy dissipation in Cucurbita pepo L. and Vinca major L. acclimated to four growth PPFDs in the field // J. Exp. Bot. 1998. V. 49. P. 1869-1879.
73. Havaux M., Dall' O.L., Cuine S., Giuliano G., Bassi R. The effect of zeaxantin on structure and function of photosynthetic apparatus in Arabidopsis thaliana // J. Biol. Chem. 2004. V. 279. P. 13878-13888.
74. Schreiber U., Kriger A. Two fundamentally different types of variable chlorophyll fluorescence in vivo // FEBS Lett. 1996. V. 397. P. 131-135.
75. Allen J.F. Protein phosphorylation in regulation of photosynthesis // Biochem. et biophys. acta. 1992. V. 1098. P. 275-335.
76. Cajanek V., Stroch M., Lachetova I., Kalina J., Spunda V. Characterization of the photosystem II inactivation of heat-stressed barley leaves as monitored by the various parameters of chlorophyll a fluorescence and delayed fluorescence // J. Phochem. Photobiol. B. Biology. 1998. V. 47. P. 39-45.
77. Satoh K., Nakatani H.Y., Steinback K.E., Watson J., Arntzen C.J. Polypeptide composition of a photosystem II core complex: presence of a herbicide-binding protein // Biochem. et biophys. acta. 1983. V. 724. P. 142-150.
78. Tefler A., Barber J. Role of carotenoid bound to the photosystem II reaction center // Photosynthesis: from light to the biosphere / Ed. Mathis P. Netherlands: Kluwer Acad. Pubi., 1995. V. IV. P. 15-20.
79. Tefler A. Too much light? How ß-carotene protects the photosystem II reaction center// Photochem. Photobiol. Sei. 2005. V. 4. P. 950-956.
80. Allakhverdiev S.I., Klimov V.V., Carpentier R. Evidence for the involvement of cyclic electron transport in the protection of photosystem II against photoinactivation: influence of a new phenolic compound // Biochemistry (USA). 1997. V. 36. P. 4149-4154.
81. Bukhov N.G., Carpentier R. Heterogeneity of photosystem II reaction centers as influenced by heat treatment of barley leaves // Physiol. Plant. 2000. V. 110. P. 279-285.
82. Roberts D.R., Kristie D.N., Thompson J.E., Dumbroff E.B., Gepstein S. ¡n vitro evidence for the involvement of activated oxygen in light activated aggregation of thylakoid proteins // Physiol. Plant. 1991. V. 82. P. 389-396.
83. Takeba G., Kozaki A. Photorespiration is an essential mechanism for the protection of C3 plants from photooxidation // Stress responses of photosynthetic organisms: molecular mechanisms and molecular regulation / Eds Satoh K., Murata N. Amsterdam, Tokyo: Elsevier, 1998. P. 15-36.
84. Canaani D., Schuster G., Ohad I. Photoinhibition in Chlamydomonas reingardtii: Effect of state transition, intersystem energy distribution and photosystem I cyclic electron flow // Photosynth. Res. 1989. V. 20. P. 129-146.
85. Herbert S.K., Martin R.E., Fork D.C Light adaptation of cyclic electron transport through photosystem I in the cyanobacterium Synechococcus sp. PCC 7942 // Photosynth. Res. 1995. V. 46. P. 277-285.
86. Gilmore A.M., Hazlett T.L., Govindjee. Xanthophyll cycle-dependent quenching of photosystem II chlorophyll a fluorescence: formation of a quenching complex with a short fluorescence lifetime // Proc. Natl. Acad Sci. USA. 1995. V. 92. P. 2273-2277.
87. Burritt D.J., Mackenzie S. Antioxidant metabolism during acclimation of Begonia x erythrophylla to high light levels // Ann. Bot. 2003. V. 91. P. 783-794.
88. Bukhov N.G., Heber U., Wiese C, Shuvalov V.A. Energy dissipation in photosynthesis: does the quenching of chlorophyll fluorescence originate from antenna complexes of photosystem II or from the reaction center? // Planta. 2001. V. 212. P. 729-758.
89. Russian source
90. Nuijs A.M., Shuvalov V.A., van Gorkom H.J., Plijter, J.J., Duysens L.N.M. Picosecond absorbance difference spectroscopy on the primary reactions and the antenna-excited states in photosystem I particles // Biochem. et biophys. acta. 1986. V. 850. P. 310-318.
91. Choudhury N.K., Behera RK. Photoinhibition of photosynthesis: Role of carotenoids in photoprotection of chloroplast constituents//Photosynthetica. 2001. V. 39. No 4. p. 481-488.
92. Havaux M., Tardy F. Temperature-dependent adjustment of the termal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments // Planta. 1996. V. 198. P. 324-333.
93. Tasaka Y., Gombos Z., Nishiyama Y., Mohanty P., Ohba T., Ohki K., Murata N. Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis // EMBO J. 1996. V. 15. P. 6416-6425.
94. Murata N., Nishiyama Y. Molecular mechanisms of the low-temperature tolerance of the photosynthetic machinery // Stress responses of photosynthetic organisms. / Eds Satoh K., Murata N. Amsterdam, Tokyo: Elsevier, 1998. P. 93-112.
95. Leakey A.D.B., Press M.C. Scholes J.D. High-temperature inhibition of photosynthesis is greater under sunflecks than uniform irradiance in a tropical rain forest tree seedling // Plant Cell Environ. 2003. V. 26. P. 1681-1690.
96. Charles SA, Halliwell B. Light activation of fructose biphosphatase in isolated spinach chloroplasts and deactivation by hydrogen peroxide // Planta. 1981. V. 151. P. 242-246.
97. Takeda T., Yokota Á.. Shigeoka S. Resistance of photosynthesis to hydrogen peroxide in algae // Plant Cell Physiol. 1995. V. 36. P. 1089-1095.
98. Santarius K.A. Sites of heat sensitivity in chloroplasts and differential inactivation of cyclic and noncyclic photophosphorilation by heating // J. Therm. Biol. 1975. V. 1. P. 101-107.
99. Enami I., Kitamura M., Tomo T., Isokawa Y., Ohta H., Katoh S. Is the primary cause of thermal inactivation of oxygen evolution in spinach PS II membranes release of the extrinsic 33 kDa protein or of Mn? // Biochem. et biophys. acta. 1994. V. 1186. P. 52-58.
100. Stefanov D., Yordanov J., Tsonev T. Effect of thermal stress combined with different light conditions on some photosynthetic characteristics of barley (Hordeum vulgare L.) plants // Photosynthetica. 1996. V. 32. No 2. P. 171-180.
101. Thompson L.K., Blaylock R., Sturtevant J.M., Brudvig G.W. Molecular basis of the heat denaturation of photosystem II // Biochemistry. 1989. V. 28. P. 6686-6695.
102. Yamane Y., Kashino Y., Koike H., Satoh K. Effects of high temperatures on the photosynthetic systems in spinach: oxygen-evolving activities, fluorescence characteristics and the denaturation process // Photosynth. Res. 1998. V. 57. P. 51-59.
103. Russian source
104. Havaux M., Greppin H., Strasser R.J. Functioning of Photosystems I and II in pea leaves exposed to heat stress in the presence or absence of light // Planta. 1991. V. 186. P. 88-98.
105. Bukhov N.G., Mohanty P. Elevated temperature stress effects on photosystems: characterization and evaluation of the nature of heat induced impairments // Concepts in photobiology: photosynthesis and photomorphogenesis / Eds Singhal G.S, Renger G., Sopory S.K., Irrgang K-D., Govindjee. New Delhi: Narosa Publ. House, 1999. P. 617-648.
106. Mamedov M.D., Hayashi H., Murata N. Effects of glycinebetaine and unsaturation of membrane lipids on heat stability of photosynthetic electron transport and phosphorilation reactions in Synechocystis PCC 6803 // Biochem. et biophys. acta. 1993. V. 1142. P. 1-5.
107. Nash D., Miyao M., Murata N. Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese// Biochem. et biophys. acta. 1985. V. 807. P. 127-133.
108. Pas tenes C., Horton R. Effect of high temperature on photosynthesis in beans // Plant Physiol. 1996. V. 112. P. 1245-1251.
109. Bukhov N., Egorova E., Carpentier R. Electron flow to photosystem I from stromal reductants in vivo: the size of the pool of stromal reductants controls the rate of electron donation to both rapidly and slowly reducing photosystem I units//Planta. 2002. V. 215. P. 812-820.
110. Havaux M. Short-term responses of phoptosystem I to heat stress - induction of a PS II-independent electron transport through PS I fed by stromal components // Photosynth. Res. 1996. V. 47. P. 88-97.
111. o increases by high temperatures in higher plants // Photosynth. Res. 2000. V. 63. P. 23-34.
112. Tunaka Y., Nishiyama Y., Murata N. Acclimation of the photosynthetic machinery to high temperature in Chlamydomonas reinhardtii requires synthesis de novo of proteins encoded by the nuclear and chloroplast genomes // Plant Physiol. 2000. V. 124. P. 441-150.
113. Russian source
114. Gounaris K., Brain A.R.R., Williams W.P. Structural reorganization of chloroplast thylakoid membranes in response to heat-stress // Biochem. et biophys. acta. 1984. V. 766. P. 198-208.
115. Semenova G.A. Structural reorganization of thylakoid systems in response to heat treatment // Photosynthetica. 2004. V. 42. No 4. P. 521-527.
116. Yordanov I.T. Response of photosynthetic apparatus to temperature stress and molecular mechanisms of its adaptation // Photosynthetica. 1993. V. 26. P. 517-531.
117. Feller U., Grafts-Brander S.J., Salvucci ME. Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase / oxygenase (Rubisco) activase-mediated activation of Rubisco // Plant Physiol. 1998. V. 116. P. 539-546.
118. Weis E. Reversible heat inactivation of Calvin cycle: a possible mechanism of the temperature regulation of photosynthesis// Planta. 1981. V. 151. P. 33-39.
119. Law R.D., 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. 1999. V. 120. P. 173-182.
120. Eckardt N.A., Portis A.R.Jr. Heat denaturation profiles of ribulose-1,5-bisphosphate carboxilase / oxigenase (Rubisco) and Rubisco activase and the inability of " Rubisco activase to restore activity of heat-denaturated Rubisco // Plant Physiol. 1997. V. 113. P. 539-546.
121. Salvucci M.E., Crafts-Brandner S.J. Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis // Physiol. Plant. 2004. V. 120. P. 179-186.
122. Haldimann P., Feller U. Growth at moderately elevated temperature alters the physiological response of the photosynthetic apparatus to heat stress in pea (Pisum sativum L.) leaves // Plant Cell Environ. 2005. V. 28. P. 302-317.
123. 2 assimilation after heat stress is correlated with recovery of oxygen-evolving complex proteins in Zea mays L. // Phosynthetica. 1997. V. 34. No 1. P. 13-20.
124. Wang H.S., Goffeda M., Leustek. T. Characteristics of an Hsp70 homolog localized in higher plant chloroplasts that is similar to DnaK, the Hps70 prokaryotes // Plant Physiol. 1993. V. 102. P. 843-850.
125. Gilmore A., Govindjee. How higher plants respond to excess light: Energy dissipation in photosystem II // Concepts in photobiology: photosynthesis and photomorphogenesis / Eds Singhal G.S., Renger G., Irrgang K.-D., Sopory S., Govindjee. Narosa Publ.: Kluwer Acad. Publ., 1999. P. 513-548.
126. Heckathorn S.A., Bryan J.K., Coleman J.S. The methionine-rich low-molecular-weight chloroplast heatshock protein: evolutionary conservation and accumulation in relation to thermotolerance // Am. J. Bot. 1998a. V. 85. P. 175-183.
127. Heckathorn S.A., Downs S.A., Sharkey T.D., Soleman J.S. The small, methionine-rich chloroplast heatshock protein protects photosystem II electron transport during heat stress // Plant Physiol. 1998b. V. 116. No 1. p. 439-444.
128. Sairam R.K., Svastava G.C., Saxena D.C. Increased antioxidant activity under elevated temperatures; A mechanism of heat stress tolerance in wheat genotypes // Biol. Plant. 2000. V. 43. No 2. P. 245-251.
129. Demmig-Adams B. Carotenoids and photoprotection in plants: a role for the xanthophyll, zeaxanthin // Biochem. et biophys. acta. 1990. V. 1020. P. 1-24.
130. Rokka A., Aro EM., Herrmann R.G., Anderrson B., Vener A.V. Dephosphorilation of photosystem II reaction center proteins in plant photosynthetic membranes as an immediate response to abrupt elevation of temperature // Plant Physiol. 2000. V. 123. P. 1525-1535.
131. Hansson M., Vener A.V. Identification of three previously unknown in vivo protein phosphorilation sites in thylakoid membranes of Arabidopsis thatiana // Mol. Cell. Proteom. 2003. V. 2. P. 550-559.
132. Vener A.V., Harms A., Sussman M.R., Vierstra R.D. Mass spectrometric resolution of reversible protein phosphorylation in photosynthetic membranes of Arabidopsis thaliana // J. Biol. Chem. 2001. V. 276. P. 6959-6966.
133. Demmig-Adams B., Adams W.W. Photoprotection and other responses of plants to high light stress // Annu. Rev. Plant Physiol. Plant Mol. Biol. 1992. V. 43. P. 599-626.
134. Heber U., Walker D. Concerning a dual function of coupled cyclic electron transport in leaves // Plant Physiol. 1992. V. 100. P. 1621-1626.
135. Heber U. Irrungen, Wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants // Photosynth. Res. 2002. V. 73. P. 223-231.
136. Vierling E. The role of heat shock proteins in plants // Ann. Rev. Plant Physiol. Plant Mol. Biol. 1991. V. 42. P. 579-620.
137. Russian source
138. Heckathorn S.A., Ryan S.L., Baylis J.A., Wang D., Hamilton Hl E.W., Cundiff L., Luthe D.S. In vivo evidence from an Agrostis stolonifera selection genotype that chloroplast small heat-shock proteins can protect photosystem II during heat stress // Funct. Plant Biol. 2002. V. 29. P. 933-944.
139. Vigh L., Maresca B., Harwood J.L. Does the membrane's physical state control the expression of heat shock and other genes? // Trends Biochem. Sci. 1998. V. 23. P. 369-374.
140. Grover A., Agarwal M., Katiyar-Agarwal S., Sahi C., Agarwal S. Production of high temperature tolerant transgenic plants through manipulation of membrane lipids // Curr. Sci. 2000. V. 79. P. 557-559.
141. Murakami Y., Tsuyama M., Kobayashi Y., Kodama H., Iba K. Trienoic fatty acids and plant tolerance of high temperature // Science 2000. V. 287. P. 476-479.
142. Suzuki /., Los D.A., Kanesaki Y., Mikami K., Murata N. The pathway for perception and transduction of low-temperature signals in Synechocystis // EMBO J. 2000. V. 19. Xs 6. P. 1327-1334.
143. Russian source
144. Nishiyama Y., Los' D.A., Murata N. PsbU, a protein associated with photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus species PCC 7002 // Plant Physiol. 1999. V. 120. P. 301-308.
145. Metis A. Dynamics of photosynthetic membrane composition and function // Biochem. et biophys. acta. 1991. V. 1056. P. 87-106.
146. Tsonev T., Velikova V., Lambreva M., Stefanov D. Recovery of photosynthetic apparatus in bean plants after high and low temperature induced photoinhibition // BuIg. J. Plant. Physiol. 1999. V. 25. P. 45-53.
147. YangX., Wen X., GongH.,Lu Q., Yang Z., Tang Y., Liang Z., Lu C. Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants // Planta. Sep 5. 2006. (in press).
148. Kreslavski V., Khristin M., Tatarinzev N., Shabnova N., Semenova G., Kosobryukhov A. Photosynthetic response in wheat seedlings during recovery after heat shock // J. Plant Physiol. 2007. (in press).
149. Russian source
150. Russian source
151. Lyons JM. Chilling injury in plants // Annu. Rev. Plant Physiol. 1973. V. 24. P. 445-466.
152. Russian source
153. Shen J.-R., Terashita I., Kato S. The cause for dark, chilling induced inactivation of photosynthetic oxygenevolving system in cucumber leaves // Plant Physiol. 1990. V. 93. P. 1354-1357.
154. Kratsch H.A., Wise R.R. The ultrastructure of chilling stress // Plant Cell Environ. 2000. V. 23. P. 337-350.
155. Nishida I., Murata N. Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids // Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996. V. 47. P. 541-568.
156. Moon B.Y., Higashi S-I., Gombos Z., Murata N. Unsaturation of the ntembrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants // Proc. Natl. Acad. Sci. USA. 1995. V. 92. P. 6219-6223.
157. Terano J., Piskua M., Yao Q. Protective effect of epicatechin, epicatecin gallate and quercetin on lipid peroxidation in phospholipid bilayers // Arch. Biochem. Biophys. 1994. V. 308. P. 278-284.
158. Krause G.H. Photoinhibition induced by low temperatures // Photoinhibition of photosynthesis. From molecular mechanisms to the field / Eds Baker N.R., Bowyer J.R. Oxford: Bios Scientific Publ., 1994a. P. 331-348.
159. Krause G.H. The role of oxygen photoinhibition of photosynthesis // Causes of photooxidative stress and amelioration of defence system in plants / Eds Foyer CH., Millenaux P.M. Boca Raton: CRC Press, 1994b. P. 43-76.
160. Tsonev T., Velikova V., Georgieva K., Hyde P.E., Jones H.G. Low temperature enhances photosynthetic down-regulation in French bean (Phaseolus vulgaris L.) plants // Ann. Bot. 2003. V. 91. P. 343-352.
161. Feierabend J., Schaan C., Hertwig B. Photoinactivation of catalase occurs under both high- and low-temperature stress conditions and accompanies photoinhibition of PSII // Plant Physiol. 1992. V. 100. P. 1554-1561.
162. Gong H., Nilson S. Effect of temperature on photoinhibition of photosynthesis, recovery and turnover of the 32 kD chloroplast protein in Lemma gibba // J. Plant Physiol. 1989. V. 135. P. 9-14.
163. Havaux M., Kloppstech K. The protective functions of carotenoid and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants // Planta. 2001. V. 213. P. 953-966.
164. Vigh L., Los' D.A., Horvatch I., Murata N. The primary signal in the biological perception of temperature: Pd-catalyzed hydrogenation of membrane lipids stimulated the expression of the desA gene in Synechocvstis sp. PCC 6803 // Proc. Natl. Acad. Sci. USA. 1993. V. 90. P. 9090-9094.
165. Murata N., Los' D.A. Membrane fluidity and temperature perception // Plant Physiol. 1997. V. 115. P. 875-879.
166. Boyer J.S. Water deficits and photosynthesis // Water deficit and plant growth / Ed. Kozlowsky T.T. N. Y.-San Fransisco-London: Acad. Press, 1976. V. IV. P. 153-190.
167. Kirst GD. Salinity tolerance of eukaryotic marine algae// Annu. Rev. Plant Physiol. Plant Mol. Biol. 1989. V. 40. P. 21-53.
168. Moisender P.H., McClinton E.. Paerl H.W. Salinity effects on growth, photosynthetic parameters, and nitrogenase activity in estuarine planctonic cyanobacteria // Microbial Ecol. 2002. V. 43. P. 432-442.
169. Hagemann M., Erdmann N. Environmental stresses // Cyanobacterial nitrogen metabolism and environmental biotechnology / Ed. Rai A.K. Heidelberg, Germany: Springer-Verlag, 1997. P. 156-221.
170. Hayashi H., Murata N. Genetically engineered enhancement of salinity tolerance in higher plants // Stress responses of photosynthetic organisms / Eds Satoh K., Murata N. Amsterdam, Tokyo: Elsevier, 1998. P. 133-148.
171. Sudhir P., Murthy S.D.S. Effects of salt stress on basic processes of photosynthesis // Photosynthetica. 2004. V. 42. No 4. P. 481-486.
172. Shapiguzov A., Lyukevich A.A.. Allakhverdiev S.I., Sergeyenko T. V., Suzuki I., Murata N., Los D.A. Osmot_ic shrinkage of cells of Synechocystis sp. PCC 6803 by water efflux via aquaporins regulates the osmostress-inducible gene expression // Microbiology. 2005. V. 151. p. 447-455.
173. Joset F., Jeanjean R., Hagemann M. Dynamics of response of cyanobacteria to salt stress: deciplrering of molecular events // Physiol. Plant. 1996. V. 96. P. 738-744.
174. Hernandez J.A., Jimenez A., Mullineaux P., Sevilla F. Tolerance of pea plants (Pisum sativum) to long term salt stress is associated with induction of antioxidant defences // Plant Cell Environ. 2000. V. 23. P. 853-862.
175. Hernandez J.A., Olmos E., Corpas F.J., Sevilla F., del Rio L.A. Salt-induced oxidative stress in chloroplasts of pea plants//Plant Sci. 1995. V. 105. P. 151-167.
176. Lu C., Torzilo G., Vonshak A. Kinetic response of photosystem II photochemistry in cyanobacterium Spirulinaplatensis to high salinity is charactcrized two distinct phases // Aust. J. Plant Physiol. 1999. V. 26. P. 283-292.
177. Lu C., Vonshak A. Effects of salinity on photosystem II function in cyanobacterial Spirulina platensis cells // Physiol. Plant. 2002. V. 114. P. 405-413.
178. Schubert H., Hagemann M. Salt effects on 77K fluorescence and photosynthesis in the cyanobacterium Synechocystis sp. PCC 6803 // FEMS Microbiol. Lett. 1990. V. 71. P. 169-172.
179. Schubert H., Fulda S., Hagemann M. Effects of adaptation to different salt concentrations on photosynthesis and pigmentation of the cyanobacterium Synechocystis sp. PCC. 6803 // J. Plant Physiol. 1993. V. 142. P. 291-295.
180. Jeanjean R., Matthijs H.C.P., Onana B., Havaux M., Joset F. Exposure of the cyanobacterium Synechosystis sp. PCC 6803 to salt stress induces concerted changes in respiration and photosynthesis // Plant Cell Physiol. 1993. V. 34. P. 1073-1079.
181. Gilmour D.J., Hipkins M.F., Webber A.N., Backer N.R., Boney A.D. The effect of ionic stress on photosynthesis in Dunaliella tertiolecta. Chlorophyll fluorescence kinetics and characteristics // Planta. 1985. V. 163. P. 250-256.
182. Takabe T., Incharoensakdi A., Arakawa K., Yokota S. CO2 fixation rate and RuBisCO increase in the halotolerant cyanobacterium, Aphanothece halophytica, grown in high salinities // Plant Physiol. 1988. V. 88. P. 1120-1124.
183. Neale P.J., Melis A. Salinity-stress enhances photoinhibition of photosystem II in Chlamydomonas reinhardtii H J. Plant Physiol. 1989. V. 134. P. 619-622.
184. Sharma P.K., Hall D.O. Interaction of salt stress and photoinhibition on photosynthesis in barley and sorghum // J. Plant Physiol. 1991. V. 138. P. 614-619.
185. Lu C., Qiu N., Wang B., Zhang J. Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa // J. Exp. Bot. 2003. V. 54. No. 383. P. 851-860.
186. Wen X., Qiu N., Lu Q., Lu C Enhanced thermotolerance of photosystem II in salt-adapted plants of the halophyte Artemisia anethifolia // Planta. 2005. V. 220. No 3. p. 486-497.
187. Casas A.M., Bressan R.A., Nasegawa R.M. Cell growth and water relations of the halophyte, Atriplex mumu_laria L. in response to NaCl stress // Plant Cell Reports. 1991. V. 10. P. 81-84.
188. Kanesaki Y., Suzuki I., Allakhverdiev S.I., Mikami K., Murata N. Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803 // Biochem. Biophys. Res. Commun. 2002. V. 290. P. 339-348.
189. Nixon P.J., Barker M., Boehm M., de Ries R., Komenda J. FtsH-mediated repair of the photosystem II complex in response to light stress // J. Exp. Bot. 2005. V. 56. No 411. P. 357-363.
190. +-ATPase in the common ice plant is developmentally controlled and tissue specific // Plant Physiol. 2001. V. 125. P. 1643-1654.
191. Ford C.W. Accumulation of low molecular solutes in water stress tropical legumes // Phytochemistry. 1984. V. 23. P. 1007-1015.
192. Russian source
193. Allakhverdiev S.I., Feyziev Y.M., Ahmed A., Hayashi H., Aliev JA., Klimov V.V., Murata N., Carpentier R. Stabilization of oxygen evolution and primary electron transport reactions in photosystem II against heat stress with glycinebetaine and sucrose // J. Photochem. Photobiol. 1996. V. 34. P. 149-157.
194. Allakhverdiev S.I., Hayashi H., Nishiyama Y., Ivanov A.G., Aliev Ja.A., Klimov V.V., Murata N., Carpentier R. Glycinebetaine protects the D1/D2/Cytb559 complex of photosystem II against photo-induced and heat-induced inactivation // J. Plant Physiol. 2003. V. 160. P. 41-49.
195. Chinnusamy V., Jagendorf A., ZhuJ.-K. Understanding and improving salt tolerance in plants // Crop Sci. 2005. V. 45. P. 437-148.
196. Russian source
197. Bohnert H.J., Jensen R.G. Strategies for engineering water-stress tolerance in plants // Trends Biotechnol. 1996. V. 14. P. 89-97.
198. Mackay C.E., Senaratna T., McKersie B.D., Fletcher R.A. Ozone induced injury to cellular membranes in Triticum aestivum L. and protection by the Triasole S3307 // Plant Cell Physiol. 1987. V. 128. P. 1271-1278.
199. Rademacher W. New types of plant growth retardants: Additional perspectives for practical application in agriculture and horticulture // Plant growth substances / Eds Pharis R.P., Rood S.B. Berlin, Heidelberg: Springer Verlag, 1990. P. 611-618.
200. Kreslavski V.D., Balakhnina T.J., Khristin M.S., Bukhov N.G. Pretreatment of bean seedlings by choline compounds increases the resistance of photosynthetic apparatus to UV radiation and elevated temperatures // Photosynthetica. 2001. V. 39. No 3. P. 353-358.
201. Kreslavski V., Kobzar E., Ivanova E., Kuznetsov E. Effects of short-term red radiation and choline compounds on cytokinin content, chlorophyll accumulation and photomorphogenesis in wheat seedlings // Plant Growth. Reg. 2005. V. 47. P. 9-15.
202. Russian source
203. Alexieva V.. Ivanov S., Sergiev I., Karanov E. Interaction between stresses // BuIg. J. Plant Physiol. Special Issue. 2003. P. 1-17.
204. Takabe T., Nakamura T., Nomura M., Hayashi Y., Ishitani M., Muramoto Y., Tanaka A., Takabe T. Glycinebetaine and the genetic engineering of salinity tolerance in plants // Stress responses of hotosynthetic organisms / Eds Satoh K., Murata N. Amsterdam, Tokyo: Elsevier, 1998. P. 115-131.
205. Caldas T., Demont-Caulet N., Ghasi A., Richarme G. Thermoprotection by glycinebetaine and choline // Microbiology. 1999. V. 145. No 9. P. 2543-2548.
206. Klimov V.V., Baranov S.V., Allakhverdiev S.I. Bicarbonate protects the donor side of photosystem II against photoinhibition and thermoinactivation // FEBS Lett. 1997. V. 418. P. 243-246.
207. Sabehat A., Weiss D., Lurie S. Heat shock proteins and cross-tolerance in plants//Physiol. Plant. 1998. V. 103. p. 437-441.
208. Schoner S., Krause G.H. Protective systems against active oxygen in spinach: response to cold acclimation in excess light//Planta. 1990. V. 180. P. 383-389.
209. Stapel D., Kruse E., Kloppstech K. The protective effect of heat shock protein against photoinhibition under heat shock in barley (Hordeum vulgare) // J. Photochem. Photobiol. 1993. V. 21. P. 211-218.
210. Strid A.W., Chow S., Anderson J.M. UV-B damage and protection at the molecular level in plants // Photosynth. Res. 1994. V. 39. P. 475-489.
211. Karpinski S., Reynolds H., Karpinska B., Wingsle G., Creissen G., Mullineaux P. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis // Science. 1999. V. 284. P. 654-657.
212. Pastori C.M., Foyer C.H. Common components, networks and pathways of cross-tolerance to stress. The central role of 'redox' and abscisic-acid-mediated controls // Plant Physiol. 2002. V. 129. P. 460-468.