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Photosynthetic Thermotolerance is Quantitatively and Positively Correlated with Production of Specific Heat-shock Proteins Among Nine Genotypes of Lycopersicon (Tomato)

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Photosynthetica

Abstract

We recently showed that the chloroplast small heat-shock protein (herein referred to as chlp Hsp24) protects photosystem 2 (PS2) during heat stress, and phenotypic variation in production of chlp Hsp24 is positively related to PS2 thermotolerance. However, the importance of chlp Hsp24 or other Hsps to other aspects of photosynthesis and overall photosynthetic thermotolerance is unknown. To begin investigating this and the importance of genetic variation in Hsp production to photosynthetic thermotolerance, the production of several prominent Hsps and photosynthetic thermotolerance were quantified in nine genotypes of Lycopersicon, and then the relationships between thermotolerance of net photosynthetic rate (P N) and production of each Hsp were examined. The nine genotypes exhibited wide variation in P N thermotolerance and production of each of the Hsps examined (chlp Hsp70, Hsp60, and Hsp24, and cytosol Hsp70). No statistically significant relationship was observed between production of chlp Hsp70 and P N thermotolerance, and only a weak positive relationship between cytosolic Hsp70 and P N was detected. However, significant positive relationships were observed between production of chlp Hsp24 and Hsp60 and P N thermotolerance. Hence natural variation in production of chlp Hsp24 and Hsp60 is important in determining variation in photosynthetic thermotolerance. This is perhaps the first evidence that chlp Hsp60 is involved in photosynthetic thermotolerance, and these in vivo results are consistent with previous in vitro results showing that chlp Hsp24 protects PS2 during heat stress.

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References

  • Bonk, M., Hoffman, B., Von Lintig, J., Schledz, M., Al-Babili, S., Hobeika, E., Kleinig, H., Beyer, P.: Chloroplast import of four carotenoid biosynthetic enzymes in vitro reveals differential fates prior to membrane binding and oligomeric assembly.-Eur. J. Biochem. 247: 942-950, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Bonk, M., Tadros, M., Vandekerckhove, J., Al-Babili, S., Beyer, P.: Purification and characterization of chaperonin 60 and heat-shock protein 70 from chromoplasts of Narcissus pseudonarcissus.-Plant Physiol. 111: 931-939, 1996.

    Article  PubMed  CAS  Google Scholar 

  • Clarke, A.K., Critchley, C.: Characterisation of chloroplast heat shock proteins in young leaves of C4 monocotyledons.-Physiol. Plant. 92: 118-130, 1994.

    Article  CAS  Google Scholar 

  • Cloney, L.P., Bekkaoui, D.R., Feist, G.L., Lane, W.S., Hemmingsen, S.M.: Brassica napus plastid and mitochondrial chaperonin-60 proteins contain multiple distinct polypeptides.-Plant Physiol. 105: 233-241, 1994.

    Article  PubMed  CAS  Google Scholar 

  • Coleman, J.S., Heckathorn, S.A., Hallberg, R.L.: Heat-shock proteins and thermotolerance: linking molecular and ecological perspectives.-Trends Ecol. Evol. 10: 305-306, 1995.

    Article  PubMed  CAS  Google Scholar 

  • Downs, C.A., Coleman, J.S., Heckathorn, S.A.: The chloroplast 22-Ku heat-shock protein: a lumenal protein that associates with the oxygen evolving complex and protects Photosystem II during heat stress.-J. Plant Physiol. 155: 477-487, 1999a.

    CAS  Google Scholar 

  • Downs, C.A., Heckathorn, S.A.: 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.

    Article  PubMed  CAS  Google Scholar 

  • Downs, C.A., Heckathorn, S.A., Bryan, J.K., Coleman, J.S.: 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.

    Article  CAS  Google Scholar 

  • Downs, C.A., Ryan, S.L., Heckathorn, S.A.: The chloroplast small heat-shock protein: evidence for a general role in protecting Photosystem II against oxidative stress and photoinhibition.-J. Plant Physiol. 155: 488-496, 1999b.

    CAS  Google Scholar 

  • Fender, S.E., O'Connell, M.A.: Heat shock protein expression in thermotolerant and thermosensitive lines of cotton.-Plant Cell Rep. 8: 37-40, 1989.

    Article  CAS  Google Scholar 

  • Fender, S.E., O'Connell, M.A.: Expression of heat-shock response in a tomato interspecific hybrid is not intermediate between the two parental responses.-Plant Physiol. 93: 1140-1146, 1990.

    Article  PubMed  CAS  Google Scholar 

  • Frova, C., Gorla, M.S.: Quantitative expression of maize HSPs: genetic dissection and association with thermotolerance.-Theor. appl. Genet. 86: 213-220, 1993.

    Article  CAS  Google Scholar 

  • Gatenby, A.A., Ellis, R.J.: Chaperone function: the assembly of ribulose bisphosphate carboxylase-oxygenase.-Annu. Rev. Cell Biol. 6: 125-149, 1990.

    Article  PubMed  CAS  Google Scholar 

  • Gatenby, A.A., Viitanen, P.V.: Structural and functional aspects of chaperonin-mediated protein folding.-Annu. Rev. Plant Physiol. Plant mol. Biol. 45: 469-491, 1994.

    Article  CAS  Google Scholar 

  • Ghosh, S., Gepstein, S., Heikkila, J.J., Dumbroff, E.B.: Use of a scanning densitometer or an ELISA plate reader for measurement of nanogram amounts of protein in crude extracts from biological tissues.-Anal. Biochem. 169: 227-233, 1998.

    Article  Google Scholar 

  • Goloubinoff, P., Christeller, J.T., Gatenby, A.A., Lorimer, G.H.: Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfolded state depends on two chaperonin proteins and Mg-ATP.-Nature 342: 884-889, 1989.

    Article  PubMed  CAS  Google Scholar 

  • Hartl, F.U.: Molecular chaperones in cellular protein folding.-Nature 381: 571-580, 1996.

    Article  PubMed  CAS  Google Scholar 

  • Heckathorn, S.A., Downs, C.A., Coleman, J.S.: Small heat-shock proteins protect electron transport in chloroplasts and mitochondria during stress.-Amer. Zoologist 39: 865-876, 1999.

    CAS  Google Scholar 

  • Heckathorn, S.A., Downs, C.A., Sharkey, T.D., Coleman, J.S.: The small, methionine-rich chloroplast heat-shock protein protects Photosystem II electron transport during heat stress.-Plant Physiol. 116: 439-444, 1998.

    Article  PubMed  CAS  Google Scholar 

  • Heckathorn, S.A., Poeller, G.J., Coleman, J.S., Hallberg, R.L.: Nitrogen availability alters patterns of accumulation of heat stress-induced proteins in plants.-Oecologia 105: 413-418, 1996a.

    Article  Google Scholar 

  • Heckathorn, S.A., Poeller, G.J., Coleman, J.S., Hallberg, R.L.: Nitrogen availability and vegetative development influence the response of ribulose 1,5-bisphosphate carboxylase/oxygenase, phosphoenolpyruvate carboxylase, and heat-shock protein content to heat stress in Zea mays L.-Int. J. Plant Sci. 157: 546-553, 1996b.

    Article  CAS  Google Scholar 

  • Höll-Neugebauer, B., Rudolph, R., Schmidt, M., Bucher, J.: Reconstitution of a heat shock effect in vitro: influence of GroE on the thermal aggregation of α-glucosidase from yeast.-Biochemistry 30: 11609-11614, 1991.

    Article  PubMed  Google Scholar 

  • Howarth, C.J., Ougham, H.J.: Gene expression under temperature stress.-New Phytol. 125: 1-26, 1993.

    Article  CAS  Google Scholar 

  • Joshi, C.P., Klueva, N.Y., Morrow, K.J., Nguyen, H.T.: Expression of a unique plastid-localized heat-shock protein is genetically linked to acquired thermotolerance in wheat.-Theor. appl. Genet. 95: 834-841, 1997.

    Article  CAS  Google Scholar 

  • Krebs, R.A., Feder, M.E.: Natural variation in the expression of the heat-shock protein HSP70 in a population of Drosophila melanogaster and its correlation with tolerance of ecologically relevant thermal stress.-Evolution 51: 173-179, 1997.

    Article  Google Scholar 

  • Krishnan, M., Nguyen, H.T., Burke, J.L.: Heat shock protein synthesis and thermal tolerance in wheat.-Plant Physiol. 90: 140-145, 1989.

    Article  PubMed  CAS  Google Scholar 

  • Lubben, T.H., Donaldson, G.K., Viitanen, P.V., Gatenby, A.A.: Several proteins imported into chloroplasts form stable complexes with the groEL-related chloroplast molecular chaperone.-Plant Cell 1: 1223-1230, 1989.

    Article  PubMed  CAS  Google Scholar 

  • Marshall, J.S., DeRocher, A.E., Keegstra, K., Vierling, E.: Identification of heat shock protein hsp70 homologues in chloroplasts.-Proc. nat. Acad. Sci. USA 87: 374-378, 1990.

    Article  PubMed  CAS  Google Scholar 

  • O'Connell, M.A.: Heat shock proteins and thermotolerance.-In: Basra, A.S. (ed.): Stress-Induced Gene Expression in Plants. Pp. 163-183. Harwood, Chur 1994.

    Google Scholar 

  • Ougham, H.J., Stoddart, J.L.: Synthesis of heat-shock protein and acquisition of thermotolerance in high-temperature tolerant and high-temperature susceptible lines of sorghum.-Plant Sci. 44: 163-167, 1986.

    Article  CAS  Google Scholar 

  • Park, S.Y., Shivaji, R., Krans, J.V., Luthe, D.S.: Heat-shock response in heat-tolerant and nontolerant variants of Agrostis palustris Huds.-Plant Physiol. 111: 515-524, 1996.

    PubMed  CAS  Google Scholar 

  • Parsell, D.A., Lindquist, S.: Heat shock proteins and stress tolerance.-In: Morimoto, R.I., Tissieres, A., Georgopoulos, C. (ed.): The Biology of Heat Shock Proteins and Molecular Chaperones. Pp. 457-494. Cold Spring Harbor Laboratory Press, Plainview 1994.

    Google Scholar 

  • Ristic, Z., Williams, G., Yang, G., Martin, B., Fullerton, S.: Dehydration, damage to cellular membranes, and heat-shock proteins in maize hybrids from different climates.-J. Plant Physiol. 149: 424-432, 1996.

    CAS  Google Scholar 

  • Schroda, M., Vallon, O., Wollman, F.A., Beck, C.F.: A chloroplast-targeted heat-shock protein 70 (HSP70) contributes to the protection and repair of photosystem II during and after photoinhibition.-Plant Cell 11: 1-15, 1999.

    Article  Google Scholar 

  • Schröder, H., Langer, T., Hartl, F.U., Bukau, B.: DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage.-EMBO J. 12: 4137-4144, 1993.

    PubMed  Google Scholar 

  • Showyra, D., Georgopoulos, C., Zylicz, M.: The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner.-Cell 62: 939-944, 1990.

    Article  Google Scholar 

  • Stapel, D., Kruse, E., Kloppstech, K.: The protective effect of heat shock proteins against photoinhibition under heat shock in barley (Hordeum vulgare).-J. Photochem. Photobiol. B21: 211-218, 1993.

    Google Scholar 

  • Vierling, E.: The roles of heat shock proteins in plants.-Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 579-620, 1991.

    Article  CAS  Google Scholar 

  • Viitanen, P.V., Schmidt, M., Buchner, J., Suzuki, T., Vierling, E., Dickson, R., Lorimer, G.H., Gatenby, A., Soll, J.: Functional characterization of the higher plant chloroplast chaperonins.-J. biol. Chem. 270: 18158-18164, 1995.

    Article  PubMed  CAS  Google Scholar 

  • Wang, H.S., Goffreda, M., Leustek, T.: Characteristics of an Hsp70 homolog localized in higher plant chloroplasts that is similar to DnaK, the Hsp70 of prokaryotes.-Plant Physiol. 102: 843-850, 1993.

    Article  PubMed  CAS  Google Scholar 

  • Waters, E.R., Lee, G.J., Vierling, E.: Evolution, structure and function of the small heat-shock proteins in plants.-J. exp. Bot. 47: 325-338, 1996.

    Article  CAS  Google Scholar 

  • Yalovsky, S., Paulsen, H., Michaeli, D., Chitnis, P.R., Nechushtai, R.: Involvement of a chloroplast Hsp70 heat shock protein in the integration of a protein (light-harvesting complex protein precursor) into the thylakoid membrane.-Proc. nat. Acad. Sci. USA 89: 5616-5619, 1992.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Syracuse University, 130 College Place, Syracuse, NY, 13244, USA

    P.J. Preczewski, C.A. Downs & J.S. Coleman

  2. Department of Biology, Syracuse University, 130 College Place, Syracuse, NY, 13244, USA

    S.A. Heckathorn

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  1. P.J. Preczewski
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  2. S.A. Heckathorn
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  3. C.A. Downs
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  4. J.S. Coleman
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Preczewski, P., Heckathorn, S., Downs, C. et al. Photosynthetic Thermotolerance is Quantitatively and Positively Correlated with Production of Specific Heat-shock Proteins Among Nine Genotypes of Lycopersicon (Tomato). Photosynthetica 38, 127–134 (2000). https://doi.org/10.1023/A:1026760311255

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