The chloroplast small heat-shock protein: Evidence for a general role in protecting Photosystem II against oxidative stress and photoinhibition

Journal of Plant Physiology

Volumn 155, Issue 4-5, 1999, Pages 488-496

  Downs, Craig A ^a   Ryan, Samantha L ^a   Heckathorn, Scott A ^a  

^a School of Business   (United States)

Author keywords

Abscisic acid; Chenopodium album (L.); Chloroplast; Cold stress; Drought; Lycopersicum asculentum (Mill.); Oxidative stress; Photoinhibition; Photosynthesis; Photosystem II; Small heat shock protein; Ultraviolet A radiation

Indexed keywords

CHENOPODIUM ALBUM; LYCOPERSICON; LYCOPERSICON ESCULENTUM;

EID: 0032743939     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0176-1617(99)80043-1     Document Type: Article

References (57)

1. ADAMSKA, I., I. OHAD, and K. KLOPPSTECK: Synthesis of the early light-inducible proteins is controlled by blue light and related to light stress. Proc. Natl. Acad. Sci. USA 89, 2610-2613 (1992).
2. ALAMILLO, J., C. ALMOGUERA, D. BARTELS, and J. JORDANO: Constitutive expression of small heat shock proteins in vegetative tissues of the resurrection plant Craterostigma plantagineum. Plant Mol. Biol. 29, 1093-1099 (1995).
3. ASADA, K. and M. TAKAHASHI: Production and scavenging of active oxygen in photosynthesis. In: KYLE, D. J., C. B. OSMOND, and C. J. ARNTSEN (eds.): Photoinhibition. Elsevier, Amsterdam, 227-287 (1987).
4. BANZET, N., C. RICHAUD, Y. DEVEAUX, M. KAZMAIER, J. GAGNON, and C. TRIANTAPHYLIDES: Accumulation of small heat shock proteins, including mitochondrial Hsp22, induced by oxidative stress and adaptive response in tomato cells. Plant J. 13, 519-527 (1998).
5. BERKEL VAN, J., F. SALAMINI, and C. GEBHARDT: Transcripts accumulating during cold storage of potato (Solanum tuberosum L.) tubers are sequence related to stress-responsive genes. Plant Physiol. 104, 445-452 (1994).
6. BOWLER, C., M. VAN MONTAGU, and D. INZÉ: Superoxide dismutase and stress tolerance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 83-116 (1992).
7. BRAY, E.: Drought-and ABA-induced changes in polypeptide and mRNA accumulation in tomato leaves. Plant Physiol. 88, 1210-1214 (1988).
8. -Wild-type levels of abscisic acid are not required for heat shock protein accumulation in tomato. Plant Physiol. 97, 817-820 (1991).
9. CADENAS, E.: Biochemistry of oxygen toxicity. Annu. Rev. Biochem. 58, 79-110 (1989).
10. CHEN, G. X., J. KAZIMIR, and G. M. CHENIAE: Photoinhibition of hydroxylamine-extracted photosystem II membranes: studies of mechanism. Biochem. 31, 11072-11083 (1992).
11. CHONG, K., L. CHEN-CHING, S. LILLE, C. CHANG, and C. SU: Stable overexpression of the constitutive form of heat shock protein 70 confers oxidative tolerance. J. Mol. Cell. Cardiol. 30, 599-608 (1998).
12. COCA, M. A., C. ALMOGUERA, T. L. THOMAS, and J. JORDANO: Differential regulation of small heat-shock genes in plants: analysis of a water-stress-inducible and developmentally activated sunflower promoter. Plant Mol. Biol. 31, 863-876 (1996).
13. DAIE, J., W. F. CAMPBELL, and S. D. SEELEY: Temperature-stress-induced production of abscisic acid and dihydrophaseic acid on warm-and cool-season crops. J. Amer. Soc. Hort. Sci. 106, 11-13 (1981).
14. DAVIES, K. J. A.: Protein damage and degradation by oxygen radicals, I-IV. J. Biol. Chem. 262, 9895-9920 (1987).
15. DAVIES, K. J. A. and A. L. GOLDBERG: Oxygen radicals stimulate intracellular proteolysis and lipid peroxidation by independent mechanisms in erythrocytes. J. Biol. Chem. 262, 8220-8226 (1987).
16. DOWNS, C. A. and S. A. HECKATHORN: The mitochondrial small heat-shock protein protects NADH: ubiquinone oxidoreductase of the electron transport chain during heat stress in plants. FEBS Lett. 430, 246-250 (1998).
17. DOWNS, C. A., S. A. HECKATHORN, J. K. BRYAN, and J. S. COLEMAN: The methionine-rich low-molecular-weight chloroplast heat-shock protein: evolutionary conservation and accumulation in relation to thermotolerance. Amer. J. Bot. 85, 175-183 (1998).
18. DOWNS, C. A., S. A. HECKATHORN, and J. S. COLEMAN: The chloroplast 22-kD heat-shock protein: a lumenal protein that associates with the oxygen evolving complex and protects photosystem II during heat stress. J. Plant Physiol. In press (1999a).
19. DOWNS, C. A., L. R. JONES, and S. A. HECKATHORN: Evidence for a novel set of small heat-shock proteins that associates with the mitochondria of murine PC12 cells and protects NADH : ubiquinone oxidoreductase from heat and oxidative stress. Arch. Biochem. Biophys. 365, 344-350 (1999b).
20. ECKEY-KALTENBACH, H., E. KIEFER, E. GROSSKOPF, D. ERNST, and H. SANDERMANN Jr.: Differential transcript induction of parsley pathogenesis-related proteins and of a small heat shock protein by ozone and heat shock. Plant Mol. Biol. 33, 343-350 (1997).
21. FERULLO, J. M., L. NESPOULOUS, and C. TRIANTAPHYLIDES: Gamma-ray-induced changes in the synthesis of tomato pericarp protein. Plant Cell Environ. 17, 901-911 (1994).
22. FINE, P. L. and W. D. FRASCH: The oxygen-evolving complex requires chloride to prevent hydrogen peroxide formation. Biochem. 31, 12204-12210 (1992).
23. GHOSH, S., S. GEPSTEIN, J. J. HEIKKILA, and E. B. DUMBROFF: Use of a scanning densitometer or an ELISA plate reader for measurement of nanogram amounts of protein in crude extracts from biological tissue. Anal. Biochem. 169, 227-233 (1988).
24. HALLIWELL, B.: Oxidative damage, lipid peroxidation and antioxidant protection in chloroplasts. Chem. Phys. Lipids 44, 327-340 (1987).
25. HAVAUX, M.: Stress tolerance of photosystem II in vivo: antagonistic effects of water, heat, and photoinhibition stresses. Plant Physiol. 100, 424-432 (1992).
26. HAVAUX, M. and F. TARDY: Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments. Planta 198, 324-333 (1996).
27. HAVAUX, M., F. TARDY, J. RAVENEL, D. CHANU, and P. PAROT: Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochromic shift in intact potato leaves: influence of the xanthophyll content. Plant Cell. Environ. 19, 1359-1368 (1996).
28. HECKATHORN, S. A., C. A. DOWNS, T. D. SHARKEY, and J. S. COLEMAN: The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiol. 116, 439-444 (1998).
29. HEIKKILA, J. J., J. E. T. PAPP, G. A. SCHULTZ, and J. D. BEWLEY: Induction of heat shock protein messenger RNA in maize mesocotyls by water stress, abscisic acid, and wounding. Plant Physiol. 76, 270-274 (1984).
30. JOSHI, C. P., N. Y. KLUEVA, K. J. MORROW, and H. T. NGUYEN: Expression of a unique plastid-localized heat-shock protein is genetically linked to acquired thermotolerance in wheat. Theor. Appl. Genet. 95, 834-841 (1997).
31. KLECZKOWSKI, L. A.: Inhibitors of photosynthetic enzymes/carriers and metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 339-367 (1993).
32. LAFUENTE, M. T., A. BELVER, M. G. GUYE, and M. E. SALTVEIT Jr.: Effect of temperature conditioning on chilling injury of cucumber cotyledons. Plant Physiol. 95, 443-449 (1991).
33. LESHEM, Y. and P. KUIPER: Is there a GAS (general adaptation syndrome) response to various types of environmental stress? Biol. Plant. 38, 1-19 (1996).
34. Lu, D. B., R. G. SEARS, and G. M. PAULSEN: Increasing stress resistance by in vitro selection for abscisic acid insensitivity in wheat. Crop Sci. 29, 939-943 (1989).
35. LURIE, S. and J. D. KLEIN: Acquisition of low temperature tolerance in tomatoes by exposure to high temperature stress. J. Amer. Soc. Hort. Sci. 116, 1007-1012 (1991).
36. LURIE, S., J. D. KLEIN, and E. FALLIK: Cross protection of one stress by another. In: CHERRY, J. (ed.): Biochemical and Cellular Mechanisms of Stress Tolerance in Plants. Springer-Verlag, Berlin, 201-212 (1994).
37. MEHLEN, P., J. BRIOLAY, L. SMITH, C. DIAZ-LATOUD, N. FABRE, D. PAULI, and A. P. ARRIGO: Analysis of the resistance to heat and hydrogen peroxide stress in Cos cells transiently expressing wild type or deletion mutants of the Drosophila 27 kDa-heat shock protein. Eur. J. Biochem. 215, 277-284 (1993).
38. MEHLER, A. H.: Studies on reactions of illuminated chloroplasts. (I) Mechanism of the reduction of oxygen and other Hill reagents. Arch. Biochem. Biophys. 33, 65-77 (1951).
39. MIYAO, M.: Involvement of active oxygen species in degradation of the D1 protein under strong illumination in isolated subcomplexes of Photosystem II. Biochem. 33, 9722-9730 (1994).
40. MIYAO, M., M. IKEUCHI, N. YAMAMOTO, and T. ONO: Specific degradation of the D1 protein of photosystem II by treatment with hydrogren peroxide in darkness: implications for the mechanism of degradation of the D1 protein under illumination. Biochem. 34, 10019-10026 (1995).
41. NEDUNCHEZHIAN, N., K. ANNAMALAINATHAN, and G. KULANDAIVELU: Induction of heat shock-like proteins in Vigna sinensis seedlings growing under ultraviolet-B (280-320 nm) enhanced radiation. Physiol. Plant. 85, 503-506 (1992).
42. OKADA, K., M. IKEUCHI, N. YAMAMOTO, T. ONO, and M. MIYAO: 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 (1996).
43. ORZECH, K. A. and J. J. BURKE: Heat shock and the protection against metal toxicity in wheat leaves. Plant Cell Environ. 11, 711-714 (1988).
44. PARK, S., R. SHWAJI, J. V. KRANS, and D. S. LUTHE: Heat-shock response in heat-tolerant and nontolerant variants of Agrostis palustris Huds. Plant Physiol. 111, 515-524 (1996).
45. PARK, S., K. CHANG, R. SHIVAJI, and D. S. LUTHE: Recovery from heat shock in heat-tolerant and nontolerant variants of creeping bentgrass. Plant Physiol. 115, 229-240 (1997).
46. PECAKER, I., V. CHAMOVITZ, G. MANN, P. SANDMANN, P. BOGER, and J. HIRSCHBERG: Molecular characterization of carotenoid biosynthesis in plants: the phyoene desaturase gene in tomato. In: MURATA, N. (ed.): Research in Photosynthesis III. Kluwer, Dordrecht, 11-18 (1992).
47. POLLA, B. S., S. KANTENGA, D. FRANCOIS, C. SALVIOLI, C. FRANCESCHI, S. MARSAC, and C. COSSARIZZA: Mitochondria are selective targets for the protective effects of heat shock against oxidative injury. Proc. Natl. Acad. Sci. USA 93, 6458-6463 (1996).
48. RISTIC, Z. and D. D. CASS: Chloroplast structure after water and high-temperature stress in two lines of maize that differ in endogenous levels of abscisic acid. Intl. J. Plant Sci. 153, 186-196 (1992).
49. ROBERTSON, A. J., M. ISHIKAWA, L. V. GUSTA, and S. L. MACKENZIE: Abscisic acid-induced heat tolerance in Bromus inermis Leyss cell-suspension cultures. Plant Physiol. 105, 181-190 (1994).
50. SABEHAT, A., S. LURIE, and D. WEISS: Expression of small heat-shock proteins at low temperatures: a possible role in protecting against chilling injuries. Plant Physiol. 117, 651-658 (1998).
51. SCHUSTER, G., D. EVEN, K. KLOPPSTECH, and I. OHAD: Evidence for protection by heat-shock proteins against photoinhibition during heat shock. EMBO J. 7, 1-6 (1988).
52. SHEPTOVITSKY, Y. G. and G. W. BRUDVIG: Isolation and characterization of spinach photosystem II membrane-associated catalase and polyphenol oxidase. Biochem. 35, 16255-16263 (1996).
53. 2-evolving complex does not dismutate hydrogen peroxide. Biochem. 37, 5052-5059 (1998).
54. STAPEL, D., E. KRUSE, and K. KLOPPSTECH: The protective effect of heat shock proteins against photoinhibition under heat shock in barley (Hordeum vulgare). J. Photochem. Photobiol. B: Biol. 21, 211-218 (1993).
55. TEFLER, A., S. M. BISHOP, D. PHILLIPS, and J. BARBER: Isolated photosynthetic reaction center of photosystem II as a sensitizer for the formation of singlet oxygen. Detection and quantum yield determination using a chemical trapping technique. J. Biol. Chem. 269, 13244-13253 (1994).
56. VIERLING, E.: The roles of heat shock proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 579-620 (1991).
57. ZHANG, Y., O. MARCILLAT, C. GIULIVI, L. ERNSTER, and K. J. A. DAVIES: The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J. Biol. Chem. 265, 16330-16336 (1990).