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Tomato Heat Shock Protein 21

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Tomato Heat Shock Protein 21
The Plant Cell, Vol. 17, 1829–1838, June 2005, www.plantcell.org ª 2005 American Society of Plant Biologists

Dual Role for Tomato Heat Shock Protein 21: Protecting
Photosystem II from Oxidative Stress and Promoting
Color Changes during Fruit Maturation
Inbal Neta-Sharir,a Tal Isaacson,b Susan Lurie,c and David Weissa,1 a Robert

H. Smith Institute of Plant Sciences and Genetics in Agriculture, Faculty of Agricultural, Food, and Environmental
Quality Sciences, Hebrew University of Jerusalem, Rehovot 76100, Israel b Department of Genetics, Hebrew University of Jerusalem, Jerusalem 91904, Israel c Department of Postharvest Science, Agricultural Research Organization, Volcani Center, Bet Dagan 50250, Israel

The tomato (Lycopersicon esculentum) chloroplast small heat shock protein (sHSP), HSP21, is induced by heat treatment in leaves, but also under normal growth conditions in developing fruits during the transition of chloroplasts to chromoplasts.
We used transgenic tomato plants constitutively expressing HSP21 to study the role of the protein under stress conditions and during fruit maturation. Although we did not find any effect for the transgene on photosystem II (PSII) thermotolerance, our results show that the protein protects PSII from temperature-dependent oxidative stress. In addition, we found direct evidence of the protein’s role in fruit reddening and the conversion of chloroplasts to chromoplasts. When plants were grown under normal growth temperature, transgenic fruits accumulated carotenoids earlier than controls. Furthermore, when detached mature green fruits were stored for 2 weeks at 28C and then transferred to room temperature, the natural accumulation of carotenoids was blocked. In a previous study, we showed that preheat treatment, which induces HSP21, allowed fruit color change at room temperature, after a cold treatment. Here, we show that mature green transgenic fruits constitutively expressing HSP21 do not require the heat treatment to



References: Allen, D.J., and Ort, D.R. (2001). Impacts of chilling temperatures on photosynthesis in warm-climate plants Almoguera, C., Prieto-Dapena, P., and Jordano, J. (1998). Dual regulation of a heat shock promoter during embryogenesis: Stagedependent role of heat shock elements Andersson, B., and Aro, E.-M. (2001). Photodamage and D1 protein turnover in photosystem II Asada, K. (1996). Radical production and scavenging in the chloroplasts. In Molecular Biology of Free Radical Scavenging Systems, Vol. Broido, S., Loyter, A., and Vainstein, A. (1991). Expression of plant genes in transfected mammalian cells: Accumulation of recombinant Chen, Q., and Vierling, E. (1991). Analysis of conserved domains identifies a unique structural feature of a chloroplast heat shock 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. Comai, L., Moran, P., and Maslyar, D. (1990). Novel and useful properties of a chimeric plant promoter combining CaMV 35S and Gillaspy, G., Ben-David, H., and Gruissem, W. (1993). Fruits: A developmental perspective in chloroplast small heat shock protein results in loss of redoxresponse but retained chaperone-like activity. Protein Sci. 10, 1785– 1793. (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. 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. Ha¨rndahl, U., and Sundby, C. (2001). Does the chloroplast small heat shock protein protect photosystem II during heat stress in vitro? (1998). The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress Hurkman, W.J., and Tanaka, C.K. (1986). Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis Inoglia, T., and Craig, E. (1982). Four small Drosophila heat shock proteins are related to each other and to mammalian a-crystallin. Proc. Natl. Acad. Sci. USA 79, 2360–2364. 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 Jofre, A., Molinas, M., and Pla, M. (2003). A 10-kDa class-CI sHsp protects E Krause, G.H., and Weis, E. (1991). Chlorophyll fluorescence and photosynthesis—The basics Lawrence, S.D., Cline, K., and Moore, G.A. (1997). Chromoplast development in ripening tomato fruit: Identification of cDNAs for 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 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 Levine, R.L., Mosoni, L., Berlett, B.S., and Stadtman, E.R. (1996). Natl. Acad. Sci. USA 93, 15036–15040. Lichtenthaler, H.K. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic membranes. Methods Enzymol. 148, 350–382. Livne, A., and Gepstein, S. (1988). Abundance of the major chloroplast polypeptides during development and ripening of tomato fruits 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

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