Abstract
Soybean, like many other organisms, responds to an increase in growth temperature by producing a set of new proteins, heat shock proteins. The heat shock proteins have been classified into several categories according to their molecular weight. Data are presented on the isolation, sequence characterization, and expression of a 70 kDa heat shock protein gene from soybean. A cDNA clone was isolated using a Drosophila hsp70 clone as a heterologous probe, and the cDNA was used for isolation of the soybean gene corresponding to the cDNA. The structure of this soybean is very similar to the hsp70 genes from other organisms. It has several sequences in the 5′ untranscribed region that are similar to the well characterized heat shock consensus element found in other organisms. These heat shock consensus elements have the expected position relative to the start of transcription. Unlike hsp70-like genes previously isolated from other plants, this gene does not have an intron. This protein shows high amino acid sequence similarity to other hsp70 proteins from such diverse organisms as Drosophila, rat, and Xenopus. This soybean gene is only expressed during heat shock. In addition to the hsp70 gene isolated here, there is evidence for many other hsp70-like genes in soybean.
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Amin J, Ananthan J, Voellmy R: Key features of heat shock regulatory elements. Mol Cell Biol 8: 3761–3769 (1988).
Barker RF, Idler KB, Thompson DV, Kemp JD: Nucleotide sequence of the T-DNA region from the Agrobacterium tumefaciens octopine Ti Plasmid pTi 15955. Plant Mol Biol 2: 335–350 (1983).
Baumann G, Raschke E, Bevan M, Schöffl F: Functional analysis for sequences required for transcriptional activation of a soybean heat shock gene in transgenic tobacco plants. EMBO J 6: 1161–1166 (1987).
Beachy RN, Barton KA, Thompson JF, Madison JT: In vitro synthesis of the α and α′ subunits of the 7S storage protein (conglycinin) of soybean seeds. Plant Physiol 65: 990–994 (1980).
Beckmann RP, Mizzen LA, Welch WJ: Interaction of hsp70 with newly synthesized proteins: Implications for protein folding and assembly. Science 248: 850–854 (1990).
Bienz M: Developmental control of the heat shock response in Xenopus. Proc Natl Acad Sci USA 81: 3138–3142 (1984).
Bond U: Heat chock but not other stress inducers leads to the disruption of a sub-set of snRNP and inhibition of in vitro splicing in HeLa cells. EMBO J 7: 3509–3518 (1989).
Chappell TG, Welch WJ, Schlossman DM, Palter KB, Schlesinger MJ, Rothman JE: Uncoating ATPase is a member of the 70 kilodalton family of stress proteins. Cell 45: 3–13 (1986).
Chirico W, Waters MG, Blobel G: 70Kd heat shock related proteins stimulate protein translocation into microsomes. Nature 332: 805–810 (1988).
Collier NC, Heuser J, Levy MA, Schlesinger MJ: Ultrastructural and biochemical analysis of the stress granule in chicken embryo fibroblasts. J Cell Biol 106: 1131–1139 (1988).
Craig EA, The heat shock response. CRC Crit Rev Biochem 18: 239–280 (1985).
Craig EA, Ingolia TD, Manseau LJ: Expression of Drosophila heat-shock cognate genes during heat shock and development. Dev Biol 99: 418–426 (1983).
Craig EA, Jacobsen K: Mutations in cognate genes of Saccharomyces cerevisiae hsp70 result in reduced growth rate at low temperatures. Mol Cell Biol 5: 3517–3524 (1985).
Czarnecka E, Gurley WB, Nagao RT, Mosquera LA, Key JL: DNA sequence and transcript mapping of a soybean gene encoding a small heat shock protein. Proc Natl Acad Sci USA 82: 841–849 (1985).
Czarnecka E, Nagao RT, Key JL, Gurley WB: Characterization of Gmhsp26-A, a stress gene encoding a divergent heat shock protein of soybean: heavy metal induced inhibition of intron processing. Mol Cell Biol 8: 1113–1122 (1998).
Deshaies RJ, Koch BD, Werner-Washburne M, Craig EA, Schekman R: A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature 332: 800–805 (1988).
Ellwood MS, Craig EA: Differential regulation of the 70k heat shock and related genes in Saccharomyces cerevisiae. Mol Cell Biol 4: 1454–1459 (1984).
Feinberg AP, Vogelstein B: A technique for labeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6–13 (1983).
Gubler U, Hoffman BJ: A simple and very efficient method for generating cDNA libraries. Gene 25: 263–269 (1983).
Gurley WB, Bruce WB, Czarnecka E, Bandyopadhysy R, Nagao RT, Key JL: CIS-regulatory elements in heat shock and T-DNA promoters. In: Plant Gene Systems and Their Biology, pp. 279–288. Alan R. Liss New York (1987).
Gurley WB, Czarnecka E, Nagao RT, Key JL: Upstream sequences required for efficient expression of a soybean heat shock gene. Mol Cell Biol 6: 559–565 (1986).
Hightower LE, White FP: Cellular responses to stress: Comparison of a family of 71–73 kilodalton proteins rapidly synthesized in rat tissue slices and canavaninetreated cells in culture. J Cell Physiol 108: 261–275 (1981).
Holmgren R, Livak K, Morimoto R, Freund R, Meselson M: Studies of cloned sequences from four Drosophila heat shock loci. Cell 18: 1359–1370 (1979).
Ingolia TD, Craig EA: Drosophila gene related to the major heat shock-induced gene is transcribed at normal temperature and not induced by heat shock. Proc Natl Acad Sci USA 79: 525–529 (1982).
Ingolia TD, Craig EA, McCarthy B: Sequence of three copies of the gene for the major Drosophila heat shock induced protein and their flanking regions. Cell 21: 669–679 (1980).
Key JL, Czarnecka E, Lin CY, Kimpel J, Mothershed C, Schöffl F: A comparative analysis of the heat shock response in crop plants. In: Randall DD, Blevins DG, Larson LL, Rapp BJ (eds) Current Topics in Plant Biochemistry and Physiology, pp. 107–118. The Interdisciplinary Plant Biochemistry and Physiology Program, University of Missouri, Columbia, MO (1983).
Labhart P, Reeder RH: Heat shock stabilizes highly unstable transcripts of the Xenopus ribosomal gene spacer. Proc Natl Acad Sci USA 84: 56–60 (1987).
Leonen DTA, Blattner FR: Lambda Charon vectors (Ch32,33,34 and 35) adapted for DNA cloning in recombination-deficient hosts. Gene 26: 171–179 (1983).
Lewis MJ, Pelham HRB: Involvement of ATP in the nuclear and nucleolar functions of the 70 kd heat shock protein. EMBO J 4: 3137–3143 (1985).
Lindquist S: The heat shock response. Ann Rev Biochem 55: 1151–1191 (1986).
Lipman DJ, Pearson WR: Rapid and sensitive protein similarity searches. Science 227: 1435–1441 (1985).
Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).
Mansfield MA, Key JL: Synthesis of the low molecular weight heat shock proteins in plants. Plant Physiol 84: 1007–1017 (1987).
Maxam AM, Gilbert W: Sequencing and-labeled DNA with base-specific chemical cleavages. Methods Enzymol 65: 449–560 (1980).
Munro S, Pelham HRB: An hsp70-like protein in the ER: Identity with the 78 kd glucose-regulated protein immunoglobulin heavy chain binding protein. Cell 46: 291–300 (1986).
Murray M: Mungbean nuclease mapping. Anal Biochem 158: 165–170 (1986).
Nagao RT, Czarnecka E, Gurley WB, Schöffl F, Key JL: Genes for low-molecular-weight heat shock proteins of soybeans: sequence analysis of a multigene family. Mol Cell Biol 5: 3417–3428 (1985).
Nagao RT, Kimpel JA, Vierling E, Key JL: The heat shock response: A comparative analysis. In Miflin BJ (ed) Oxford Surveys of Plant Molecular & Cell Biology, pp. 385–438. Oxford University Press, Oxford (1986).
Nagao RT, Shah DM, Eckenrode VK, Meagher RB: Multigene family of actin-related sequences isolated from a soybean genomic library. DNA 1: 1–9 (1981).
Nover L: Expression of heat shock genes in homologous and heterologous systems. In May SW, Spier RE (eds) Enzyme and Microbial Technology, vol. 9, pp. 129–192. Butterworth Scientific, London (1987).
O'Farrell PH: High resolution two-dimensional electrophoresis of proteins. J Biol Chem 10: 4007–4007 (1975).
O'Malley K, Mauron A, Barchas JD, Kedes L: Constitutively expressed rat mRNA encoding a 79-Kilodalton heat-shock-like protein. Mol Cell Biol 5: 3476–3483 (1985).
Palter KB, Watanabe M, Stinson L, Mahowald AP, Craig EA: Expression and localization of Drosophila melanogaster hsp70 cognate proteins. Mol Cell Biol 6: 1187–1203 (1986).
Pelham HRB: Activation of heat-shock genes in eukaryotes. Trends Genet 1: 31–35 (1985).
Pelham HRB: Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 46: 959–961 (1986).
Pelham HRB: Coming in from the cold. Nature 332: 776–777 (1988).
Pustell J, Kafatos C: A convenient and adaptable package of DNA sequence analysis programs. Nucl Acids Res 10: 51–59 (1982).
Roberts BE, Paterson BM: Efficient translation of tobacco mosaic virus RNA and rabbit globin 9S RNA from commercial wheat germ. proc Natl Acad Sci USA 70: 2330–2334 (1973).
Rochester DE, Winter JA, Shah DM: The structure and expression of maize genes encoding the major heat shock protein hsp70. EMBO J 5: 451–458 (1986).
Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).
Schöffl F, Key JL: An analysis of mRNA for a group of heat shock proteins of soybean using cloned cDNAs. J Mol Appl gen 1: 301–314 (1982).
Snutch TP, Mark FP, Ballie DL: The Caenorhabditis elegans hsp70 gene family: a molecular characterization. Gene 64: 241–255 (1988).
Sollner-Webb B, Reeder RH: The nucleotide sequence of the initiation sites for ribosomal RNA transcription in X. laevis. Cell 18: 485–499 (1979).
Sorger PK, Pelham HRB: Cloning and expression of a gene encoding hsc73, the major hsp70-like protein in unstressed rat cells. EMBO J 6: 993–998 (1987).
Tabor S, Richardson CC: DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci USA 84: 4767–4771 (1987).
Ungewickell E: The 70-kd mammalian heat shock proteins are structurally and functionally related to the uncoating protein that releases clathrin triskelia from coated vesicles. EMBO J 4: 3385–3391 (1985).
Voellmy R, Ahmed A, Schiller P, Bromley P, Rungger D: Isolation and functional analysis of a human 70000-dalton heat shock protein gene segment. Proc Natl Acad Sci USA 82: 4949–4953 (1985).
Welch WJ, Feramisco JR: Nuclear and nucleolar localization of the 72000-dalton heat shock protein in heat-shock mammalian cells. J Biol Chem 259: 4501–4513 (1984).
Welch WJ, Garrels JI, Feramisco JR: The mammalian stress proteins. In: Schlesinger MJ, Ashburner M, Tissieres A (eds) Heat Shock from Bacteria to Man, pp. 251–256. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).
Werner-Washburne M, Stone DE, Craig EA: Complex interactions among members of an essential subfamily of hsp70 genes in Saccharomyces cerevisiae. Mol Cell Biol 7: 2568–2577 (1987).
Winter JA, Wright R, Duck N, Gasser C, Fraley R, Shah D: The inhibition of pentunia hsp70 mRNA processing during CdCl2 stress. Mol Gen Genet 211: 315–319 (1988).
Wu CH, Casper T, Browse J, Lindquist S, Somerville C: Characterization of an HSP70 cognate gene family in Arabidopsis. Plant Physiol 88: 731–740 (1988).
Xiao H, Lis JT: Germline transformation used to define key features of heat-shock response elements. Science 239: 1139–1141 (1988).
Yost HJ, Lindquist S: RNA splicing is interrupted by heat shock and is rescued by heat shock protein synthesis. Cell 45: 185–193 (1986).
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Roberts, J.K., Key, J.L. Isolation and characterization of a soybean hsp70 gene. Plant Mol Biol 16, 671–683 (1991). https://doi.org/10.1007/BF00023431
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DOI: https://doi.org/10.1007/BF00023431