Dual role for tomato heat shock protein 21: Protecting photosystem II from oxidative stress and promoting color changes during fruit maturation

Plant Cell

Volumn 17, Issue 6, 2005, Pages 1829-1838

  Neta Sharir, Inbal ^a   Isaacson, Tal ^a   Lurie, Susan ^b   Weiss, David ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b VOLCANI CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPHYLL; COLOR; FRUITS; GROWTH KINETICS; PLANTS (BOTANY);

CAROTENOIDS; MATURE GREEN FRUITS; THERMOTOLERANCE; TRANSGENIC FRUITS;

PROTEINS;

CHLOROPHYLLS; COLOR; FRUITS; GROWTH; PLANTS; PLASTIDS; PROTEINS;

LYCOPERSICON ESCULENTUM;

ARABIDOPSIS PROTEIN; CAROTENOID; HEAT SHOCK PROTEIN; HSP21 PROTEIN, ARABIDOPSIS; VEGETABLE PROTEIN;

ARTICLE; CHLOROPLAST; FRUIT; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; OXIDATIVE STRESS; PHOTOSYSTEM II; PHYSIOLOGY; PLASTID; TEMPERATURE; TOMATO; TRANSGENIC PLANT;

ARABIDOPSIS PROTEINS; CAROTENOIDS; CHLOROPLASTS; FRUIT; HEAT-SHOCK PROTEINS; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PLASTIDS; TEMPERATURE;

EID: 32944457560     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.105.031914     Document Type: Article

References (45)

1. Allen, D.J., and Ort, D.R. (2001). Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci. 6, 36-42.
2. Almoguera, C., Prieto-Dapena, P., and Jordano, J. (1998). Dual regulation of a heat shock promoter during embryogenesis: Stage-dependent role of heat shock elements. Plant J. 13, 437-446.
3. Andersson, B., and Aro, E.-M. (2001). Photodamage and D1 protein turnover in photosystem II. In Advances in Photosynthesis and Respiration, Regulation of Photosynthesis, Vol. 11, E.-M. Aro and B. Andersson, eds (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 377-393.
4. Asada, K. (1996). Radical production and scavenging in the chloroplasts. In Molecular Biology of Free Radical Scavenging Systems, Vol. 5, N.R. Baker, ed (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 123-150.
5. Broido, S., Loyter, A., and Vainstein, A. (1991). Expression of plant genes in transfected mammalian cells: Accumulation of recombinant preLHCIIb proteins within cytoplasmic inclusion bodies. Exp. Cell Res. 192, 248-255.
6. Chen, Q., and Vierling, E. (1991). Analysis of conserved domains identifies a unique structural feature of a chloroplast heat shock protein. Mol. Gen. Genet. 226, 425-431.
7. Cheung, A.Y., McNellis, T., and Piekos, B. (1993). Maintenance of chloroplast components during chromoplast differentiation in the tomato mutant green flesh. Plant Physiol. 101, 1223-1229.
8. Comai, L., Moran, P., and Maslyar, D. (1990). Novel and useful properties of a chimeric plant promoter combining CaMV 35S and MAS elements. Plant Mol. Biol. 15, 373-381.
9. Gillaspy, G., Ben-David, H., and Gruissem, W. (1993). Fruits: A developmental perspective. Plant Cell 5, 1439-1451.
10. Gustavsson, N., Kokke, B.P.A., Anzelius, B., Boelens, W.C., and Sundby, C. (2001). Substitution of conserved methionines by leucines in chloroplast small heat shock protein results in loss of redox-response but retained chaperone-like activity. Protein Sci. 10, 1785-1793.
11. Gustavsson, N., Kokke, B.P.A., Härndahl, U., Silow, M., Bechtold, U., Poghosyan, Z., Murphy, D., Boelens, W.C., and Sundby, C. (2002). A peptide methionine sulfoxide reductase highly expressed in photosynthetic tissue in Arabidopsis thaliana can protect the chaperone-like activity of a chloroplast-localized small heat shock protein. Plant J. 29, 545-553.
12. Hamilton, E.W., and Heckathorn, S.A. (2001). Mitochondrial adaptation to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betain. Plant Physiol. 126, 1266-1274.
13. Härndahl, U., Hall, R.B., Osteryoung, K.W., Vierling, E., Bornman, J.F., and Sundby, C. (1999). The chloroplast small heat shock protein undergoes oxidation-dependent conformational changes and may protect plants from oxidative stress. Cell Stress Chaperones 4, 129-138.
14. Härndahl, U., Kokke, B.P.A., Gustavsson, N., Linse, S., Berggern, K., Tjerneld, F., Boelens, W.C., and Sundby, C. (2001). The chaperone-like activity of a small heat shock protein is lost after sulfoxidation of conserved methionines in a surface-exposed amphipathic α-helix. Biochim. Biophys. Acta 1545, 227-237.
15. Härndahl, U., and Sundby, C. (2001). Does the chloroplast small heat shock protein protect photosystem II during heat stress in vitro? Physiol. Plant. 111, 273-275.
16. Heckathorn, S.A., Downs, C.A., Sharkey, T.D., and Coleman, J.S. (1998). The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiol. 116, 439-444.
17. Heckathorn, S.A., Ryan, S.L., Baylis, J.A., Wang, D., Hamilton, E.W., Cundiff, L., and Dawn, S.L. (2002). In vitro evidence from an Agrostis stolonifera selection genotype that chloroplast small heat-shock protein can protect photosystem II during heat stress. Funct. Plant Biol. 29, 933-944.
18. Hurkman, W.J., and Tanaka, C.K. (1986). Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol. 81, 802-806.
19. Inoglia, T., and Craig, E. (1982). Four small Drosophila heat shock proteins are related to each other and to mammalian α-crystallin. Proc. Natl. Acad. Sci. USA 79, 2360-2364.
20. Isaacson, T., Ohad, I., Beyer, P., and Hirschberg, J. (2004). Analysis in vitro of the enzyme CRTISO establishes a poly-cis-carotenoid biosynthesis pathway in plants. Plant Physiol. 136, 4246-4255.
21. Jofre, A., Molinas, M., and Pla, M. (2003). A 10-kDa class-Cl sHsp protects E. coli from oxidative and high-temperature stress. Planta 217, 813-819.
22. Krause, G.H., and Weis, E. (1991). Chlorophyll fluorescence and photosynthesis-The basics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 313-349.
23. Kuntz, M., Chen, H.C., Simkin, A.J., Romer, S., Shipton, C.A., Drake, R., Schuch, W., and Bramley, P.M. (1998). Upregulating of two ripening-related genes from a nonclimacteric plant (pepper) in a transgenic climacteric plant (tomato). Plant J. 13, 351-361.
24. Lawrence, S.D., Cline, K., and Moore, G.A. (1997). Chromoplast development in ripening tomato fruit: Identification of cDNAs for chromoplast-targeted proteins and characterization of a cDNA encoding a plastid-localized low-molecular-weight heat shock protein. Plant Mol. Biol. 33, 483-492.
25. Lee, G.J., Roseman, A.M., Saibil, H.R., and Vierling, E. (1997). A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J. 16, 659-671.
26. Lee, G.J., and Vierling, E. (2000). A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol. 122, 189-198.
27. Levine, R.L., Mosoni, L., Berlett, B.S., and Stadtman, E.R. (1996). Methionine residues as endogenous antioxidants in proteins. Proc. Natl. Acad. Sci. USA 93, 15036-15040.
28. Lichtenthaler, H.K. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic membranes. Methods Enzymol. 148, 350-382.
29. Livne, A., and Gepstein, S. (1988). Abundance of the major chloroplast polypeptides during development and ripening of tomato fruits. Plant Physiol. 87, 239-243.
30. Low, D., Brandle, K., Nover, L., and Forreiter, C. (2000). Cytosolic heat-stress proteins Hsp17.7 class I and Hsp17.3 class II of tomato act as molecular chaperones in vivo. Planta 211, 575-582.
31. Lurie, S., and Klein, J.D. (1991). Acquisition of low-temperature tolerance in tomatoes by exposure to high temperature stress. J. Am. Soc. Hortic. Sci. 116, 1007-1012.
32. McCormick, S. (1991). Transformation of tomato with Agrobacterium tumefaciens. In Plant Tissue Culture Manual, H. Linclsey, ed (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 1-9.
33. Medina-Escobar, N., Cardenas, J., Munoz-Blanco, J., and Caballero, J.L. (1998). Cloning and molecular characterization of a strawberry fruit ripening-related cDNA corresponding a mRNA for a low-molecular-weight heat-shock protein. Plant Mol. Biol. 36, 33-42.
34. Osteryoung, K.W., and Vierling, E. (1994). Dynamics of small heat shock protein distribution within the chloroplasts of higher plants. J. Biol. Chem. 269, 28676-28682.
35. Pecker, I., Gabbay, R., Cunningham, F.X., Jr., and Hirschberg, J. (1996). Cloning and characterization of the cDNA for lycopene β-cyclase from tomato reveals decrease in its expression during fruit ripening. Plant Mol. Biol. 30, 807-819.
36. Römer, S., D'Harlingue, A., Camera, B., Schantz, R., and Kuntz, M. (1992). Cysteine synthase from Capicum annuum chloroplasts characterization and cDNA cloning and up-regulated enzyme during fruit development. J. Biol. Chem. 267, 17966-17970.
37. Ronen, G., Cohen, M., Zamir, D., and Hirschberg, J. (1999). Regulation of carotenoid biosynthesis during tomato fruit development: Expression of the gene for lycopene epsilon-cyclase is down-regulated during ripening and is elevated in the mutant Delta. Plant J. 17, 341-351.
38. Sabehat, A., Lurie, S., and Weiss, D. (1998). Expression of small heat-shock proteins at low temperatures: A possible role in protecting against chilling injuries. Plant Physiol. 117, 651-658.
39. Sabehat, A., Weiss, D., and Lurie, S. (1996). The correlation between heat shock protein accumulation and persistence and chilling tolerance in tomato fruit. Plant Physiol. 110, 531-537.
40. Sun, W., Bernard, C., van de Cotte, B., van Montagu, M., and Verbruggen, N. (2001). At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J. 27, 407-415.
41. Sun, W., van Montagu, M., and Verbruggen, N. (2002). Small heat shock proteins and stress tolerance in plants. Biochim. Biophys. Acta 1577, 1-9.
42. Tsvetkova, N.M., Horvath, I., Torok, Z., Wolkers, W.F., Balogi, Z., Shigapova, N., Crowe, L.M., Tablin, F., Vierling, E., Crowe, J.H., and Vigh, L. (2002). Small heat-shock proteins regulate membrane lipid polymorphism. Proc. Natl. Acad. Sci. USA 99, 13504-13509.
43. van Tunen, A.J., Koes, R.E., Spelt, C.E., van der Krol, A.R., Stuitje, A.R., and Mol, J.N.M. (1988). Cloning of the two chalcone flavanone isomerase genes from Petunia hybrida: Coordinate, light-regulated and differential expression of flavonoid genes. EMBO J. 7, 1257-1263.
44. Wang, D., and Luthe, D.S. (2003). Heat sensitivity in a bentgrass varient. Failure to accumulate a chloroplast heat shock protein isoform implicated in heat tolerance. Plant Physiol. 133, 319-327.
45. Wehmeyer, N., Hernandez, L.D., Finkelstein, R.R., and Vierling, E. (1996). Synthesis of small heat-shock proteins is part of the developmental program of late seed maturation. Plant Physiol. 112, 747-757.