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Heat-inducible rice hsp82 and hsp70 are not always co-regulated

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Abstract

We have characterized several heat-shock-induced genes in rice (Oryza sativa L.) and compared their expression under a variety of conditions. Three of these genes, which are analogs of the hsp82/90 family, lie within a cloned 18-kilobase (kb) region of the genome. The middle member of this cluster, designated hsp82B, has been fully sequenced. The gene uses a promoter containing six putative heat-shock elements as well as several unusual sequence motifs including a stretch of 11 thymidines alternating with 11 adenosines. The mRNA for this gene reaches its highest relative level of expression within 120 min after plants are shifted to 42° C; no other conditions induce this gene. By contrast, we found that during heat stress the expression of hsp70 correlates well with increases in internal ion concentrations, and can also be induced by excess salt or ethanol at normal growth temperatures. These results appear to indicate that whereas hsp70 is induced by all stresses that lead to protein denaturation — including heat stress — HSP82 mRNA accumulates only upon heat stress.

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Abbreviations

HSF:

heat shock factor

HSP:

heat shock protein

kb:

kilobase

References

  • Ananthan, J., Goldberg, A.L., Voellmy, R. (1986) Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science 232, 522–524

    Google Scholar 

  • Angelidis, C.E., Lazaridis, J., Pagoulatos, G.N. (1991) Constitutive expression of heat-shock protein 70 in mammalian cells confers thermoresistance. Eur. J. Biochem. 199, 35–39

    Google Scholar 

  • Ashburner, M., Bonner, J.J. (1979) The induction of gene activity in Drosophila by heat shock. Cell 17, 241–254

    Google Scholar 

  • Baler, R., Welch, W.J., Voellmy, R. (1992) Heat shock gene regulation by nascent polypeptides and denatured proteins: hsp70 as a potential autoregulatory factor. J. Cell Biol. 117, 1151–1159

    Google Scholar 

  • Bardwell, J.C.A., Craig, E.A. (1987) Eukaryotic M r 83,000 heat shock protein has a homologue in Escherichia coli. Proc. Natl. Acad. Sci. USA 84, 5177–5181

    Google Scholar 

  • Baulieu, E.-E., Binart, N., Cadepond, F., Catelli, M.-G., Chambraud, B., Garnier, J., Gasc, J.-M., Groyer-Schweizer, G., Rafestin-Oblin, M.-E., Radanyi, C., Redeuilh, G., Renoir, J.-M., Sabbah, M. (1990) Are receptor-associated nuclear proteins associated with the earliest effects of steroid hormones? In: Hormone perception and signal transduction in animals and plants (Proceedings of the Symposia of the Society for Experimental Biology, vol. 44), pp. 3–20, Roberts, J., Kirk, C., Venis, M., eds. Society for Experimental Biology, Cambridge

    Google Scholar 

  • Beckmann, R.P., Mizzen, L.A., Welch, W.J. (1990) Interactions of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly. Science 248, 850–854

    Google Scholar 

  • Benjamin, I.J., Horie, S., Greenberg, M.L., Alpern, R.J., Williams, R.S. (1992) Induction of stress proteins in cultured myogenic cells. Molecular signals for the activation of heat shock transcription factor during ischemia. J. Clin. Invest. 89, 1685–1689

    Google Scholar 

  • Blackman, R.K., Meselson, M. (1986) Interspecific nucleotide sequence comparisons used to identify regulatory and structural features of the Drosophila hsp82 gene. J. Mol. Biol. 188, 499–515

    Google Scholar 

  • Borkird, C., Simoens, C., Villarroel, R., Van Montagu, M. (1991) Gene expression associated with water-stress adaptation of rice cells and identification of two genes as hsp 70 and ubiquitin. Physiol. Plant. 82, 449–457

    Google Scholar 

  • Borkovich, K.A., Farrelly, F.W., Finkelstein, D.B., Taulien, J., Lindquist, S. (1989) hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol. Cell. Biol. 9, 3919–3930

    Google Scholar 

  • Cadepond, F., Schweizer-Groyer, G., Segard-Maurel, I., Jibard, N., Hollenberg, S.M., Giguère, V., Evans, R.M., Baulieu, E.-E. (1991) Heat shock protein 90 as a critical factor in maintaining glucocorticosteroid receptor in a nonfunctional state. J. Biol. Chem. 266, 5834–5841

    Google Scholar 

  • Catelli, M.G., Radanyi, C., Renoir, J.M., Binart, N., Baulieu, E.E. (1988) Definition of domain of HSP 90 interacting with steroid receptors. J. Cell. Biochem. Suppl. 12D, 276

    Google Scholar 

  • Cheng, L., Hirst, K., Piper, P.W. (1992) Authentic temperature-regulation of a heat shock gene inserted into yeast on a high copy number vector. Influences of overexpression of HSP90 protein on high temperature growth and thermotolerance. Biochim. Biophys. Acta 1132, 26–34

    Google Scholar 

  • Chirico, W.J., Waters, M.G., Blobel, G. (1988) 70K heat shock related proteins stimulate protein translocation into microsomes. Nature 332, 805–810

    Google Scholar 

  • Conner, T.W., LaFayette, P.R., Nagao, R.T., Key, J.L. (1990) Sequence and expression of a HSP83 from Arabidopsis thaliana. Plant Physiol. 94, 1689–1695

    Google Scholar 

  • Craig, E.A., Gross, C.A. (1991) Is hsp70 the cellular thermometer? Trends Biochem. Sci. 16, 135–140

    Google Scholar 

  • Csermely, P., Kahn, C.R. (1991) The 90-kDa heat shock protein (hsp-90) possesses an ATP binding site and autophosphorylating activity. J. Biol. Chem. 266, 4943–4950

    Google Scholar 

  • Dalley, B.K., Golomb, M. (1992) Gene expression in the Caenorhabditis elegans dauer larva: developmental regulation of Hsp90 and other genes. Dev. Biol. 151, 80–90

    Google Scholar 

  • Dellaporta, S.L., Wood, J., Hicks, J.B. (1983) A plant DNA minipreparation: version II. Plant Mol. Biol. Reporter 1, 19–21

    Google Scholar 

  • Denhardt, D. (1966) A membrane filter technique for the detection of complementary DNA. Biochem. Biophys. Res. Comm. 23, 641–646

    Google Scholar 

  • Edelman, L., Czarnecka, E., Key, J.L. (1988) Induction and accumulation of heat shock-specific poly(A+) RNAs and proteins in soybean seedlings during arsenite and cadmium treatments. Plant Physiol. 86, 1048–1056

    Google Scholar 

  • Farrelly, F.W., Finkelstein, D.B. (1984) Complete sequence of the heat shock-inducible HSP90 gene of Saccharomyces cerevisiae. J. Biol. Chem. 259, 5745–5751

    Google Scholar 

  • Felsheim, R.F., Das, A. (1992) Structure and expression of a heatshock protein 83 gene of Pharbitis nil. Plant Physiol. 100, 1764–1771

    Google Scholar 

  • Ferguson, D.L., Guikema, J.A., Paulsen, G.M. (1990) Ubiquitin pool modulation and protein degradation in wheat roots during high temperature stress. Plant Physiol. 92, 740–746

    Google Scholar 

  • Gasc, J.M., Renoir, J.M., Faber, L.E., Delahaye, F., Baulieu, E.E. (1990) Nuclear localization of two steroid receptor-associated proteins, hsp90 and p59. Exp. Cell Res. 186, 362–367

    Google Scholar 

  • Hanley, B.A., Schuler, M.A. (1988) Plant intron sequences: evidence for distinct groups of introns. Nucleic Acids Res. 16, 7159–7176

    Google Scholar 

  • Hickey, E., Brandon, S.E., Smale, G., Lloyd, D., Weber, L.A. (1989) Sequence and regulation of a gene encoding a human 89-kilodalton heat shock protein. Mol. Cell. Biol. 9, 2615–2626

    Google Scholar 

  • Hoagland, D.T., Arnon, D.I. (1938) Water culture method for growing plants without soil. Univ. Calif. Agric. Exp. Stu. Circ. 347, 1–39

    Google Scholar 

  • Jones, J.D.G., Dunsmuir, P., Bedbrook, J. (1985) High level expression of introduced chimaeric genes in regenerated transformed plants. EMBO J. 4, 2411–2418

    Google Scholar 

  • Kang, S.-M., Titus, J.S. (1989) Increased proteolysis of senescing rice leaves in the presence of NaCl and KCl. Plant Physiol. 91, 1232–1237

    Google Scholar 

  • Kobayashi, N., McEntee, K. (1990) Evidence for a heat shock transcription factor-independent mechanism for heat shock induction of transcription in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 87, 6550–6554

    Google Scholar 

  • Koning, A.J., Rose, R., Comai, L. (1992) Developmental expression of tomato heat-shock cognate protein 80. Plant Physiol. 100, 801–811

    Google Scholar 

  • Kouzarides, T., Ziff, E. (1989) Leucine zippers of fos, jun and GCN4 dictate dimerization specificity and thereby control DNA binding. Nature 340, 568–571

    Google Scholar 

  • Koyasu, S., Nishida, E., Kadowaki, T., Matsuzaki, F., Iida, K., Harada, F., Kasuga, M., Sakai, H., Yahara, I. (1986) Two mammalian heat shock proteins, HSP90 and HSP100, are actinbinding proteins. Proc. Natl. Acad. Sci. USA 83, 8054–8058

    Google Scholar 

  • Landschulz, W.H., Johnson, P.F., McKnight, S.L. (1988) The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 240, 1759–1764

    Google Scholar 

  • Li, G.C., Li, L., Liu, R.Y., Rehman, M., Lee, W.M.F. (1992) Heat shock protein hsp70 protects cells from thermal stress even after deletion of its ATP-binding domain. Proc. Natl. Acad. Sci. USA 89, 2036–2040

    Google Scholar 

  • Lindquist, S. (1980) Varying patterns of protein synthesis during heat shock; implications for regulation. Dev. Biol. 77, 463–419

    Google Scholar 

  • Lindquist, S., Craig, E.A. (1988) The heat-shock proteins. Annu. Rev. Genet. 22, 631–677

    Google Scholar 

  • Loenen, W.A.M., Blattner, F.R. (1983) Lambda Charon vectors (Ch32, 33, 34 and 35) adapted for DNA cloning in recombination-deficient hosts. Gene 26, 171–179

    Google Scholar 

  • Maniatis, T., Fritsch, E.F., Sambrook, J., eds. (1982) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Maxam, A.M., Gilbert, W. (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 65, 499–559

    Google Scholar 

  • Melton, D.A., Krieg, P.A., Rebagliati, M.R., Maniatis, T., Zinn, K., Green, M.R. (1984) Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 12, 7035–7056

    Google Scholar 

  • Miyata, Y., Yahara, I. (1992) The 90-kDa heat shock protein, HSP90, binds and protect casein kinase II from self-aggregation and enhances its kinase activity. J. Biol. Chem. 267, 7042–7047

    Google Scholar 

  • Murashige, T., Skoog, F. (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473–4197

    Google Scholar 

  • Nover, L., Neumann, D., Scharf, K.-D., eds. (1990) Heat shock and other stress response systems of plants. Results and problems in cell differentiation, vol. 16. Springer-Verlag, Berlin

    Google Scholar 

  • Olazabal, U.E., Pfaff, D.W., Mobbs, C.V. (1992) Estrogenic regulation of heat shock protein 90 kDa in the rat ventromedial hypothalamus and uterus. Mol. Cell. Endocrinol. 84, 175–183

    Google Scholar 

  • Peattie, D.A., Harding, M.W., Fleming, M.A., DeCenzo, M.T., Lippke, J.A., Livingston, D.J., Benasutti, M. (1992) Expression and characterization of human FKBP52, an immunophilin that associates with the 90-kDa heat shock protein and is a component of steroid receptor complexes. Proc. Natl. Acad. Sci. USA 89, 10974–10978

    Google Scholar 

  • Pelham, H.R.B. (1982) A regulatory upstream promoter element in the Drosophila Hsp 70 heat-shock gene. Cell 30, 517–528

    Google Scholar 

  • Perdew, G.H. (1988) Association of the Ah receptor with the 90-kDa heat shock protein. J. Biol. Chem. 263, 13802–13805

    Google Scholar 

  • Picard, D., Khursheed, B., Garabedian, M.J., Fortin, M.G., Lindquist, S., Yamamoto, K.R. (1990) Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 348, 166–168

    Google Scholar 

  • Rebbe, N.F., Hickman, W.S., Ley, T.J., Stafford, D.W., Hickman, S. (1989) Nucleotide sequence and regulation of a human 90-kDa heat shock protein gene. J. Biol. Chem. 264, 15006–15011

    Google Scholar 

  • Rose, D.W., Wettenhall, R.E.H., Kudlicki, W., Kramer, G., Hardesty, B. (1987) The 90-kilodalton peptide of the heme-regulated eIF-2α kinase has sequence similarity with the 90-kilodalton heat shock protein. Biochemistry 26, 6583–6587

    Google Scholar 

  • Rose, D.W., Welch, W.J., Kramer, G., Hardesty, B. (1989) Possible involvement of the 90-kDa heat shock protein in the regulation of protein synthesis. J. Biol. Chem. 264, 6239–6244

    Google Scholar 

  • Saiki, R.K., Scharf, S., Faloona, F., Mullis, K.B., Horn, G.T., Erlich, H.A., Arnheim, N. (1985) Enzymatic amplification of β-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230, 1350–1354

    CAS  PubMed  Google Scholar 

  • Sanchez, E.R., Toft, D.O., Schlesinger, M.J., Pratt, W.B. (1985) Evidence that the 90-kDa phosphoprotein associated with the untransformed L-cell glucocorticoid receptor is a murine heaft shock protein. J. Biol. Chem. 260, 12398–12401

    Google Scholar 

  • Scharf, K.-D., Rose, S., Zott, W., Schöff, F., Nover, L. (1990) Three tomato genes code for heat stress transcription factors with a region of remarkable homology to the DNA-binding domain of the yeast HSF. EMBO J. 9, 4495–4501

    Google Scholar 

  • Scherrer, L.C., Dalman, F.C., Massa, E., Meshinchi, S., Pratt, W.B. (1990) Structural and functional reconstitution of the glucocorticoid receptor-Hsp90 complex. J. Biol. Chem. 265, 21397–21400

    Google Scholar 

  • Schwartz, J.A., Mizukami, H., Skafar, D.F. (1993) A metal-linked gapped zipper model is proposed for the hsp90-glucocorticoid receptor interaction. FEBS Lett. 315, 109–113

    Google Scholar 

  • Takahashi, T., Naito, S., Komeda, Y. (1992) Isolation and analysis of the expression of two genes for the 81-kilodalton heat-shock proteins from Arabidopsis. Plant Physiol. 99, 383–390

    Google Scholar 

  • Tsang, E.W.T., Bowler, C., Hérouart, D., Van Camp, W., Villarroel, R., Genetello, C., Van Montagu, M., Inzé, D. (1991) Differential regulation of superoxide dismutases in plants exposed to environmental stress. Plant Cell 3, 783–792

    Article  CAS  PubMed  Google Scholar 

  • Vierling, E. (1991) The roles of heat shock proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 579–620

    Google Scholar 

  • von Gromoff, E.D., Treier, U., Beck, C.F. (1989) Three light-inducible heat shock genes of Chlamydomonas reinhardtii. Mol. Cell. Biol. 9, 3911–3918

    Google Scholar 

  • Wiech, H., Buchner, H., Zimmermann, R., Jakob, Y. (1992) Hsp90 chaperones protein folding in vitro. Nature 358, 169–170

    Google Scholar 

  • Yanisch-Perron, C., Vieira, J., Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33, 103–119

    Article  CAS  PubMed  Google Scholar 

  • Ziemiecki, A., Catelli, M.-G., Joab, I., Moncharmont, B. (1986) Association of the heat shock protein hsp90 with steroid hormone receptors and tyrosine kinase oncogene products. Biochem. Biophys. Res. Comm. 138, 1298–1307

    Google Scholar 

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The authors thank R. Villarroel (Laboratorium voor Genetica, Universiteit Gent, Gent, Belgium) for help with the sequencing, both Dr. Van Der Straeten and D. Van den Broeck (Laboratorium voor Genetica, Universiteit Gent, Gent, Belgium) for critical reading of the manuscript, Martine De Cock for typing it, and Karel Spruyt and Vera Vermaercke for drawings and photographs. This work was supported by grants from the Belgian Programme on Interuniversity Poles of Attraction (Prime Minister's Office, Science Policy Programming #38), the Commission of the European Communities TS2-0053-B (GDF), and the Rockefeller Foundation (FR 86058 #59). A.B.G. is indebted to Conselho Nacional de Desenvolvimento Científico e Tecnológico (Brasil; RHAE proc. no. 260015188.1) for a predoctoral fellowship.

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Van Breusegem, F., Dekeyser, R., Garcia, A.B. et al. Heat-inducible rice hsp82 and hsp70 are not always co-regulated. Planta 193, 57–66 (1994). https://doi.org/10.1007/BF00191607

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