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Tissue-specific localization of heat-stress proteins during embryo development

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Abstract

We report on the stress-independent, tissue-specific expression of the heat-stress protein HSP17 in developing seeds of different plant species and on its intracellular localization. Though HSP17 expression during seed development seems to be a general phenomenon, the isoform patterns, the relative amounts in embryonic tissues and the intracellular localization show species-specific variations. In contrast to the results on the stressinduced protein forming large cytoplasmic aggregates (heat stress granules) the developmentally expressed HSP17 is mainly found in nuclei. But in addition, a considerable part is also detected in protein bodies of mature seeds of Lycopersicon esculentum and Vicia faba, but not of Zea mays. The mechanism of this transition into the vacuolar compartment remains to be investigated.

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Abbreviations

2D:

two-dimensional

HSE:

heat shock elements

HSP:

heat stress protein

References

  • Abernethy, R.H., Thiel, D.S., Petersen, N.S., Helm, K. (1989) Thermotolerance is developmental dependent in germinating wheat seed. Plant Physiol. 89, 569–576

    Google Scholar 

  • Almoguera, C., Jordano, J. (1992) Developmental and environmental concurrent expression of sunflower dry-seed-stored lowmolecular-weight heat-shock protein and Lea mRNAs. Plant Mol. Biol. 19, 781–792

    Google Scholar 

  • Arrigo, P., Tanguay, R.M. (1991) Expression of heat shock proteins during development in Drosophila. In: Heat shock and development, pp. 106–116, Hightower, L. Nover, L. eds. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Atkinson, B.G., Raizada, M., Bouchard, R.A., Frappier, J.R.H. Walden, D.B. (1993) The independent stage-specific expression of the 18-kDa heat stock protein genes during microsporogenesis in Zea mays L. Dev. Genet. 14, 15–26

    Google Scholar 

  • Bouchard, R.A. (1990) Characterization of expressed meiotic prophase repeat transcript clones of Lilium: meiosis-specific expression, relatedness, and affinities to small heat shock protein genes. Genome 33, 68–79

    Google Scholar 

  • Cheney, C.M., Shearn, A. (1983) Developmental regulation of Drosophila imaginai disk protein: Synthesis of a heat-shock protein under nonheat-shock conditions. Dev. Biol. 95, 325–330.

    Google Scholar 

  • Davies, K.M., Grierson, D. (1989) Identification of cDNA clones for tomato (Lycopersicon esculentum Mill.) mRNAs that accumulate during fruit ripening and leaf senescence in response to ethylene. Planta 179, 73–80.

    Google Scholar 

  • DeRocher, E., Vierling, E. (1994) Developmental control of small heat shock protein expression during pea seed maturation. Plant J. 5, 93–102

    Google Scholar 

  • Dietrich, P.S., Bouchard, R.A., Casey, E.S., Sinibaldi, R.M. (1991) Isolation and characterization of a small heat shock protein gene from maize. Plant Physiol. 96, 1268–1276

    Google Scholar 

  • Esen, A. (1978) A simple method for quantitative, semiquantitative, and qualitative assay of protein. Anal. Biochem. 89, 264–273

    Google Scholar 

  • Finkelstein, R.R., Tenbarge, K.M., Shumway, J.E., Crouch, M.L. (1985) Role of ABA in maturation of rape seed embryos. Plant Physiol. 78, 630–636

    Google Scholar 

  • Fischer, W., Bergfeld, R., Schopfer, P. (1987) Induction of storage protein synthesis in embryos of mature plant seeds. Naturwissenschaften 74, 86–88

    Google Scholar 

  • Fray, R.G., Lycett, G.W., Grierson, D. (1990) Nucleotide sequence of a heat-shock and ripening-related cDNA from tomato. Nucleic Acids Res. 18, 7148

    Google Scholar 

  • Györgyey, J., Gartner, A., Nemeth, K., Magyar, Z., Hirt, H., Heberlebors, E., Dudits, D. (1991) Alfalfa heat shock genes are differentially expressed during somatic embryogenesis. Plant Mol. Biol. 16, 999–1007

    Google Scholar 

  • Helm, K.W., Abernethy, R.H. (1989) Heat shock proteins and their mRNAs in dry and early imbibing embryos of wheat. Plant Physiol. 93, 1626–1633

    Google Scholar 

  • Hernandez, L.D., Vierling, E. (1993) Expression of low molecular weight heat-shock proteins under field conditions. Plant Physiol. 101, 1209–1216

    Google Scholar 

  • Horwitz, J. (1992) α-Crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. USA 89, 10449–10453

    Google Scholar 

  • Ireland, R.C., Berger, E.M. (1982) Synthesis of low molecular weight heat shock peptides stimulated by ecdysterone in a cultured Drosophila cell line. Proc. Natl. Acad. Sci. USA 79, 855–859

    Google Scholar 

  • Ireland, R.C., Berger, E.M., Sirotkin, K., Yund, M.A., Osterbur, D., Fristrom, J. (1982) Ecdysterone induces the transcription of four heat-shock genes in Drosophila S3 cells and imaginal disks. Dev. Biol. 93, 498–507

    Google Scholar 

  • Jacob, U., Gaestel, M., Engel, K., Buchner, J. (1993) Small heat shock proteins are molecular chaperons. J. Biol. Chem. 268, 1517–1520

    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 

  • Kruse, E., Liu, Z., Kloppstech, K. (1993) Expression of heat shock proteins during development of barley. Plant Mol. Biol. 23, 111–122

    Google Scholar 

  • Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685

    PubMed  Google Scholar 

  • Neumann, D., zur Nieden, U., Manteuffel, R., Walter, G., Scharf, K.-D. (1987) Intracellular localization of heat shock proteins in tomato cell cultures. Eur. J. Cell Biol. 43, 71–81

    Google Scholar 

  • Neumann, D., Nover, L., Parthier, B., Rieger, R., Scharf, K.-D., Wollgiehn, R., zur Nieden, U. (1989) Heat shock response and other stress response systems of plants. Biol. Zentralbl. 108, 1–156

    Google Scholar 

  • Nover, L. (1991) Heat shock response. CRC Press, Boca Raton

    Google Scholar 

  • Nover, L., Scharf, K.-D. (1984) Synthesis, modification and structural binding of heat shock proteins in tomato cell cultures. Eur. J. Biochem. 139, 303–313

    Google Scholar 

  • Nover, L., Scharf, K.-D., Neumann, D. (1983) Formation of cytoplasmic heat shock granules in tomato cell cultures and leaves. Mol. Cell. Biol. 3, 1648–1655

    Google Scholar 

  • Nover, L., Scharf, K.-D., Neumann, D. (1989) Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs. Mol. Cell. Biol. 9, 1298–1308

    Google Scholar 

  • O'Farrell, P.H. (1975) High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250, 4007–4021

    Google Scholar 

  • Pitto, L., LoShiavo, F., Giuliano, G., Terzi, M. (1983) Analysis of heat shock protein pattern during somatic embryogenesis of carrot. Plant Mol. Biol. 2, 231–237

    Google Scholar 

  • Ruthmann, A. (1966) Methoden der Zellforschung. Franckhsche Verlagshandlung, Stuttgart

    Google Scholar 

  • Scharf, K.-D., Materna, T., Treuter, E., Nover, L. (1994) Heat stress promoters and transcription factors. In: Plant promoters and transcription factors, pp. 121–158, Nover, L., ed. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Schrauwen, J.A.M., Reijnen, W.H., DeLeeun, H.C.G.M., van Herpen, M.M.A. (1986) Response of pollen to heat stress. Acta Bot. Neerl. 35, 321–327

    Google Scholar 

  • Tsukaya, H., Takahashi, T., Naito, S., Komeda, Y. (1992) Floral organ-specific and constitutive expression of an Arabidopsis thaliana heat-shock HSP18.2: GUS fusion gene is retained even after homeotic conversion of flowers by mutation. Mol. Gen. Genet. 237, 26–32

    Google Scholar 

  • Van Herpen, M.M.A., Reijnen, W.H., Schrauwen, J.A.M., de Groot, P.F.M., Jager, J.W.H., Wullems, G.J. (1989) Heat shock proteins and survival of germinating pollen of Lilium longiflorum and Nicotiana tabacum. J. Plant Physiol. 134, 345–351

    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 

  • Vierling, E., Sun, A. (1989) Developmental expression of heat shock proteins in higher plants. In: Environmental stress in plants, pp. 343–354, Cherry, J., ed. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Weber, E., Manteuffel, R., Neumann, D. (1978) Isolation and characterization of protein bodies of Vicia faba seeds. Biochem. Physiol. Pflanz. 172, 597–614

    Google Scholar 

  • Winter, J., Sinibaldi, R. (1991) The expression of heat shock protein and cognate genes during plant development. In: Results and problems in cell differentiation 17. Heat shock and development pp. 85–105, Hightower, L., Nover, L., eds. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Wollgiehn, R., Neumann, D., zur Nieden, U., Müsch, A., Scharf, K.-D., Nover, L. (1994) Intracellular distribution of small heat stress proteins in cultured cells of Lycopersicon peruvianum. J. Plant Physiol. 144, 491–499

    Google Scholar 

  • Xiao, C.-M., Mascarenhas, J.P. (1985) High temperature-induced thermotolerance in pollen tubes of Tradescantia and heat shock proteins. Plant Physiol. 78, 887–890

    Google Scholar 

  • Zimmerman, J.L., Apuya, N., Darwish, K., O'Carroll, C. (1989) Novel regulation of heat shock genes during carrot somatic embryo development. Plant Cell 11, 1137–1146

    Google Scholar 

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zur Nieden, U., Neumann, D., Bucka, A. et al. Tissue-specific localization of heat-stress proteins during embryo development. Planta 196, 530–538 (1995). https://doi.org/10.1007/BF00203653

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