Skip to main content
SpringerLink
Log in

Sequence, identification and characterization of cDNAs encoding two different members of the 18 kDa heat shock family of Zea mays L.

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Heat-shocked maize seedlings (cv. Oh43) synthesize a characteristic set of heat-shock proteins (hsps) which include an 18 kDa family containing at least six major isoelectric variants. A cDNA library was constructed from poly(A)+ RNAs isolated from the radicles of heat-shocked maize seedlings and screened with a DNA fragment from the theoretical open reading frame of a putative Black Mexican Sweet maize hsp 18 genomic clone. Two clones, cMHSP18-3 and cMHSP18-9, were isolated, and the RNA transcripts generated from them were translated into proteins which immunoreact with antibodies directed against the maize 18 kDa hsps and exhibit the same electrophoretic characteristics as two different members of the 18 kDa hsp family. Nucleotide sequence analyses of the cDNAs in these clones reveal that their 5′ and 3′ untranslated regions exhibit 33–34% identity and that their protein encoding regions share 93% identity. The deduced amino acid sequences of these clones show 90% identity, and the apparent molecular masses and isoelectric points of these proteins agree with those established for two different 18 kDa hsps, numbered 3 and 6. This report substantiates that at least two of the 18 kDa hsps in maize are products of different but related genes. Moreover, it establishes that transcripts for these proteins accumulate during heat shock and that both their nucleotide and deduced amino acid sequences share extensive similarities with the class VI small hsps in soybean and with transcripts expressed during meiosis in Lilium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Arrigo AP, Welch WJ: Characterization and purification of the small 28, 000-dalton mammalian heat shock protein. J Biol Chem 262: 15359–15369 (1987).

    PubMed  Google Scholar 

  2. Atkinson BG, Liu L, Goping IS, Walden DB: Expression of the genes encoding HSP73, HSP18 and ubiquitin in radicles of heat-shocked maize seedlings. Genome 31: 699–704 (1989).

    Google Scholar 

  3. Atkinson BG, Walden DB: Changes in Eukaryotic Gene Expression in Response to Environmental Stress. Academic Press, New York (1985).

    Google Scholar 

  4. Barker RF, Harberd NP, Jarvis MG, Flavell RB: Structure and evolution of the intergenic region in the ribosomal DNA repeat unit of wheat. J Mol Biol 201: 1–17 (1988).

    PubMed  Google Scholar 

  5. Baszczynski CL: Immunochemical analysis of heatshock protein synthesis in maize (Zea mays L.). Can J Gen Cytol 28: 1076–1087 (1988).

    Google Scholar 

  6. Baszczynski CL, Walden DB, Atkinson BG: Regulation of gene expression in corn (Zea mays L.) by heat shock. Can J Biochem 60: 569–579 (1982).

    PubMed  Google Scholar 

  7. Baszczynski CL, Walden DB, Atkinson BG: Regulation of gene expression in corn (Zea mays L.) by heat shock II. In vitro analysis of RNAs from heat-shocked seedlings. Can J Biochem 61: 393–403 (1983).

    Google Scholar 

  8. Baszczynski CL, Walden DB, Atkinson BG: Maize genome response to thermal shifts. In: Atkinson BG, Walden DB (eds) Changes in Eukaryotic Gene Expression in Response to Environmental Stress, pp. 349–875. Academic Press, New York (1985).

    Google Scholar 

  9. Berger EM, Woodward MP: Small heat shock proteins in Drosophila may confer thermal tolerance. Exp Cell Res 147: 437–442 (1983).

    PubMed  Google Scholar 

  10. Bond U, Schlesinger MJ: Heat-shock proteins and development. Adv Genet 24: 1–29 (1987).

    PubMed  Google Scholar 

  11. Bouchard RA: Characterization of expressed meiotic prophase repeat transcript clones of Lilium: meiosisspecific expression, relatedness, and affinities to small heat shock protein genes. Genome 33: 69–79 (1990).

    Google Scholar 

  12. Chan Y-L, Olivera J, Wool IG: The structure of rat 28S ribosomal ribonucleic acid inferred from the sequence of nucleotides in a gene. Nucl Acids Res 11: 7819–7831 (1983).

    PubMed  Google Scholar 

  13. Craig EA: The heat shock response, CRC Critical Rev Biochem 18: 239–280 (1985).

    Google Scholar 

  14. Devereux J, Haeberli P, Smithies O: A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387–416 (1984).

    PubMed  Google Scholar 

  15. Dietrich PS, Bouchard RA, Silva EM, Sinibaldi RM: The complete sequence of a maize 18 kd heat shock gene. J Cell Biol 105: 245a (1987).

    Google Scholar 

  16. Fransolet S, Deltour R, Bronchart R, van de Walle C: Changes in ultra-structure and transcription induced by elevated temperatures in Zea mays embryonic root cells. Planta 146: 7–18 (1979).

    Google Scholar 

  17. Georgiev OI, Nikeleav N, Hadjiolov AA: The structure of the yeast ribosomal RNA genes. 4. Complete sequence of the 25S rRNA gene from Saccharomyces cerevisiae. Nucl Acids Res 9: 6953–6958 (1981).

    PubMed  Google Scholar 

  18. Helm KW, Vierling E: An Arabidopsis thaliana cDNA clone encoding a low molecular weight heat shock protein. Nucl Acids Res 17: 7995 (1989).

    PubMed  Google Scholar 

  19. Hopp TP, Woods KR: Prediction of protein antigenic determinants from amino acid sequences. Proc Natl Acad Sci USA 78: 3824–8828 (1981).

    PubMed  Google Scholar 

  20. Ingolia TD, Craig EA: Four small Drosophila heat shock proteins are related to each other and to mammalian α-crystallin. Proc Natl Acad Sci USA 79: 2360–2364 (1982).

    PubMed  Google Scholar 

  21. Jain SK, Crampton J, Gonzalez IL, Schmickel RD, Drysdale JW: Complementarity between ferritin H mRNA and 28S ribosomal RNA. Biochem Biophys Res Comm 131: 863–867 (1985).

    PubMed  Google Scholar 

  22. Key JL, Kimpel JA, Lin CY, Nagao RT, Vierling E, Czarnecka E, Gurley WB, Roberts JK, Mansfield MA, Edelman L: The heat shock response in soybean. In: Key JL, Kosuge T (eds). Molecular Biology of Plant Stress, pp. 161–179. Alan R. Liss, New York (1985).

    Google Scholar 

  23. Kolosha VO, Kryukov VM, Fodor I: Sequence analysis of Citrus limon DNA coding for 26S rRNA. Evidence of heterogeneity in the 3′-region. FEBS Lett 197: 89–92 (1986).

    Article  Google Scholar 

  24. Kurtz S, Rossi J, Petko L, Lindquist S: An ancient developmental induction: heat shock protein induced in sporulation and oogenesis. Science 231: 1154–1157 (1986).

    PubMed  Google Scholar 

  25. Landry J, Chrétien P, Lambert H, Hickey E, Weber LA: Heat shock resistance conferred by expression of the human HSP27 gene in rodent cells. J Cell Biol 108: 7–15 (1989).

    Article  Google Scholar 

  26. Leicht BG, Biessmann H, Palter KB, Bonner JJ: Small heat shock proteins of Drosophila associate with the cytoskeleton. Proc Natl Acad Sci USA 83: 90–94 (1986).

    PubMed  Google Scholar 

  27. Lin CY, Roberts JK, Key JL: Acquisition of thermotolerance in soybean seedlings. Plant Physiol 74: 152–160 (1984).

    Google Scholar 

  28. Lindquist S: The heat-shock response. Ann Rev Biochem 55: 1151–1191 (1986).

    Article  PubMed  Google Scholar 

  29. Loomis WF, Wheeler SA: Heat shock response of Dictostelium. Develop Biol 90: 412–418 (1982).

    Article  PubMed  Google Scholar 

  30. Lutcke HA, Chow KC, Mickel FS, Moss KA, Kern HF, Scheele GA: Selection of AUG initiation codons differs in plants and animals. EMBO J 6: 43–48 (1987).

    PubMed  Google Scholar 

  31. Maniatis T, Fritsch EG, Sambrook J. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York (1982).

    Google Scholar 

  32. Mansfield MA, Key JL: Synthesis of the low molecular weight heat shock proteins in plants. Plant Physiol 84: 1007–1017 (1087).

    Google Scholar 

  33. Mascarenhas JP: The male gametophytre of flowering plants. Plant Cell 1: 657–664 (1989).

    Article  PubMed  Google Scholar 

  34. McMullen MD, Hunter B, Phillips RL, Rubenstein I: The structure of the maize ribosomal DNA spacer region. Nucl Acids Res 14: 4953–4968 (1986).

    PubMed  Google Scholar 

  35. 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).

    PubMed  Google Scholar 

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

    Google Scholar 

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

    PubMed  Google Scholar 

  38. Pearson WR, Lipman DJ: Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85: 2444–2448 (1988).

    PubMed  Google Scholar 

  39. Puissant C, Houdebine L-M: An improvement of the single-step method of RNA isolation by acid guandinium thiocyanate-phenol-chloroform extraction. Biotechniques 8: 148–149 (1990).

    PubMed  Google Scholar 

  40. Raschke E, Baumann G, Schöffl F: Nucleotide sequence analysis of soybean small heat shock protein genes belonging to different multigene families. J Mol Biol 199: 549–557 (1988).

    PubMed  Google Scholar 

  41. Ricciardi RP, Miller JS, Roberts BE: Purification and mapping of specific mRNAs by hybridization-selection and cellfree translation. Proc Natl Acad Sci USA 76: 4927–4931 (1979).

    PubMed  Google Scholar 

  42. Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463 (1977).

    PubMed  Google Scholar 

  43. Shah DM, Rochester DE, Krivi GG, Hironaka CM, Mozer TJ, Fraley RT, Tiemeier DC: Structure and expression of maize HSP70 genes. In: Key JL, Kosuge T (eds) Cellular and Molecular Biology of Plant Stress, pp. 181–200. Alan R. Liss, New York (1985).

    Google Scholar 

  44. Shine J, Dalgarno L: The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: Complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 71: 1342–1346 (1974).

    PubMed  Google Scholar 

  45. Southgate R, Mirault ME, Ayme A, Tissières A: Organization, sequences, and induction of heat shock genes. In: Atkinson BG, Walden DB (eds) Changes in Eukaryotic Gene Expression in Response to Environmental Stress, pp. 3–30. Academic Press, New York (1985).

    Google Scholar 

  46. Takaiwa F, Oono K, Iida Y, Sugiura Y: The complete nucleotide sequence of a rice 25S rRNA gene. Gene 37: 255–259 (1985).

    Article  PubMed  Google Scholar 

  47. Vierling E, Nagao RT, De Rocher AE, Harris LM: A heat shock protein localized to chloroplasts is a member of a eukaryotic superfamily of heat shock proteins. EMBO J 7: 575–581 (1988).

    PubMed  Google Scholar 

  48. Wistow G: Domain structure and evolution in α-crystallin and small heat shock proteins. FEBS Lett 181: 1–6 (1985).

    Article  PubMed  Google Scholar 

  49. Zimmerman JL, Petri W, Meselson M: Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock. Cell 32: 1161–1170 (1983).

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of Western Ontario, N6A 5B7, London, Ontario, Canada

    Ing Swie Goping, J. Roger H. Frappier & Burr G. Atkinson

  2. Department of Plant Sciences, University of Western Ontario, N6A 5B7, London, Ontario, Canada

    David B. Walden

Authors
  1. Ing Swie Goping
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Roger H. Frappier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David B. Walden
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Burr G. Atkinson
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goping, I.S., Frappier, J.R.H., Walden, D.B. et al. Sequence, identification and characterization of cDNAs encoding two different members of the 18 kDa heat shock family of Zea mays L.. Plant Mol Biol 16, 699–711 (1991). https://doi.org/10.1007/BF00023434

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00023434

Key words

Search

Navigation