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Post-germination-induced and hormonally dependent expression of low-molecular-weight heat shock protein genes in Douglas fir

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Abstract

We have isolated and sequenced two cDNA clones (PM 18.2A;PM 18.2B) from Douglas fir (Pseudotsuga menziesii (Mirb.) Franco) which encode for the low-molecular-weight heat shock proteins (LMW HSPs) of 18.2 kDa. The predicted amino acid sequences of the two Douglas fir proteins are 97.5% identical. A phylogenetic tree of class I LMW HSPs showed that the PM LMW HSPs are found within a subgroup consisting exclusively of dicot species indicating that class I LMW HSPs evolved from a common ancestor predating the divergence of gymnosperms and angiosperms. Northern blots of RNA from dry, imbibed, stratified and germinated seeds revealed a notable induction of LMW HSP transcripts during post-germination and early seedling growth. Unlike previous reports, the expression of these HSPs appears to be primarily restricted to seedlings as mRNA transcripts were detected at very low levels during seed development and desiccation. Maximum induction of LMW HSPs in seedlings occurred during heat shock treatment at 38–40°C, whereas cold shock or wounding failed to induce HSP transcripts. The transcription of HSP genes is up regulated by GA, MeJA and auxin and is down regulated by ABA. Methyl jasmonate treatment induced expression of these genes in dormant seeds of Douglas fir. The expression of class I cytoplasmic LMW HSPs in seedlings and their regulation by plant growth regulators suggests specific roles in plant development other than desiccation tolerance.

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References

  1. Almoguera C, Jordano J: Developmental and environmental concurrent expression of sunflower dry-seed-stored low molecular weight heat shock proteins and LEA mRNAs. Plant Mol Biol 19: 781–792 (1992).

    Article  PubMed  Google Scholar 

  2. Almoguera C, Jordano J: Differential accumulation of sunflower tetraubiquitin mRNAs during zygotic embryogenesis and developmental regulation of their heat-shock response. Plant Physiol 107: 765–773 (1995).

    PubMed  Google Scholar 

  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DI: Basic local alignment search tools. J Mol Biol 215: 403–410 (1990).

    Article  PubMed  Google Scholar 

  4. Beckmann RP, Mizzen LA, Welch WJ: Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly. Science 248: 850–853 (1990).

    PubMed  Google Scholar 

  5. Benndorf R, Haye K, Ryazantsev S, Wieske M, Behike J, Lutsch G: Phoshorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J Biol Chem 269: 20780–20784 (1994).

    PubMed  Google Scholar 

  6. Berestezky V, Dathe W, Daletskaya T, Musatenko L, Sembdner G: Jasmonic acid in seed dormancy of Acer tataricum. Biochem Physiol Pflanzen 187: 13–19 (1991).

    Google Scholar 

  7. Cavener DR, Ray SC: Eukaryotic start and stop translation sites. Nucl Acids Res 19: 3185–3192 (1991).

    PubMed  Google Scholar 

  8. Coca MA, Almoguera C, Jordano J: Expression obsun-flower low molecular weight heat shock proteins during embryogenesis and persistence after germination: localization and possible functional implications. Plant Mol Biol 25: 479–492 (1994).

    PubMed  Google Scholar 

  9. Craig EA, Gambill BD, Nelson RJ: Heat shock proteins: molecular chaperones of protein biogenesis. Microbiol Rev 57: 402–414 (1993).

    PubMed  Google Scholar 

  10. Darwish K, Wang L, Hwang CH, Apuya N, Zimmerman JL: Cloning and characterization of genes encoding low molecular weight heat shock proteins from carrot. Plant Mol Biol 16: 729–731 (1991).

    Article  PubMed  Google Scholar 

  11. DeRocher A, Helm KW, Lauzon LM, Vierling E: Expression of a conserved family of cytoplasmic low molecular weight heat shock proteins during heat stress and recovery. Plant Physiol 96: 1038–1407 (1991).

    Google Scholar 

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

    Article  Google Scholar 

  13. Ellis RJ: Molecular chaperones: the plant connection. Science 250: 954–958 (1990).

    Google Scholar 

  14. Felsenstein J: PHYLIP-Phylogeny Interference Package (Version 3.2). Cladistics 5: 64–166 (1989).

    Google Scholar 

  15. Gaestel M, Gross B, Benndorf E, Strauss M, Schunk W-H, Draft R, Otto A, Bohm H, Stahl J, Drabsch H, Bielka H: Molecular cloning, sequencing and expression in Escherichia coli of the 25-kDa growth-related protein of Ehrlich ascites tumor and its homology to mammalian stress proteins. Eur J Biochem 179: 209–213 (1989).

    PubMed  Google Scholar 

  16. Gish W, States DJ: Identification of protein coding regions by database similarity search. Nature Genet 3: 266–272 (1993).

    Article  PubMed  Google Scholar 

  17. Gurley WB, Key JL: Transcriptional regulation of the heat shock response: a plant perspective. Biochemistry 30: 1–12 (1991).

    PubMed  Google Scholar 

  18. Gyorgyey J, Gartner A, Nemeth K, Magyar Z, Hirt H, Heberle-Bors E, Dudits D: Alfalfa heat shock genes are differentially expressed during somatic embryogenesis. Plant Mol Biol 16: 999–1007 (1991).

    PubMed  Google Scholar 

  19. Helm KW, Abernethy RH: Heat shock proteins and their mRNAs in dry and early imbibing emryos of wheat. Plant Physiol 93: 1626–1633 (1990).

    Google Scholar 

  20. Helm KW, LaFayette PR, Nagao RT, Key JL, Vierling E: Localization of small heat shock proteins to the higher plant endomembrane system. Mol Cell Biol 13: 238–247 (1993).

    PubMed  Google Scholar 

  21. Hendrick JP, Hartl F-U: Molecular chaperone functions of heat shock proteins. Annu Rev Biochem 62: 349–384 (1993).

    Article  PubMed  Google Scholar 

  22. Higgins DG, Sharp PM: Fast and sensitive multiple sequence alignments on a microcomputer. CABIOS 5: 151–153 (1989).

    PubMed  Google Scholar 

  23. Howarth C: Heat shock proteins in Sorghum bicolor and Pennistetum americanum II. Stored RNA in sorghum seed and its relationship to heat shock protein synthesis during germination. Plant Cell Environ 13: 57–64 (1990).

    Google Scholar 

  24. Howarth CJ, Ougham HJ: Genes expression under temperature stress. New Phytol 125: 1–26 (1993).

    Google Scholar 

  25. Jakob U, Buchner J: Assisting spontaneity: the role of Hsp 90 and small Hsps as molecular chaperones. Trends Biochem Sci 19: 205–211 (1994).

    Article  PubMed  Google Scholar 

  26. Jakob U, Gaestel M, Engel K, Buchner J: Small heat shock proteins are molecular chaperones. J Biol Chem 268: 1517–1520 (1993).

    PubMed  Google Scholar 

  27. Jorgensen JA, Nguyen H: Isolation, sequence and expression of cDNA encoding a class I heat shock protein (HSP 17.2) in maize. Plant Sci 97: 169–175 (1994).

    Article  Google Scholar 

  28. Kang KI, Devin J, Cadepond F, Jibard N, Guiochon-Mantel A, Baulieu E-E, Catelli M-G: In vivo functional protein-protein interaction: Nuclear targeted hsp90 shifts cytoplasmic steroid receptor mutants into the nucleus. Proc Natl Acad Sci USA 91: 340–344 (1994).

    PubMed  Google Scholar 

  29. Knauf U, Jakob U, Engel K, Buchner J, Gaestel M: Stress and mitogen-induced phosphorylation of the small heat shock protein Hsp25 by MAPKAP kinase 2 is not essential for chaperone properties and cellular thermoresistance. EMBO J 13: 54–60 (1994).

    PubMed  Google Scholar 

  30. Krishnan HB, Pueppke SG: Heat shock triggers rapid protein phosphorylation in soybean seedlings. Biochem Biophys Res Commun 148: 762–767 (1987).

    Article  PubMed  Google Scholar 

  31. Kuznetsov VIV, Roshchupkin BV: Stress responses in Nicotiana sylvestris cells to salinity and high temperature. 2. synthesis of heat shock proteins and polypeptide phosphorylation. Russ J Plant Physiol 41: 566–572 (1994).

    Google Scholar 

  32. Lavoie JN, Hickey E, Weber LA, Landry J: Modulation of actin microfilament dynamics and fluid phase ninocytosis by phosphorylation of heat shock protein 27. J Biol Chem 268: 24210–24214 (1993).

    PubMed  Google Scholar 

  33. Leadem CL: The role of plant growth regulators in the germination of forest tree seeds. In: Kossult SV, Ross SD (eds) Hormonal Control of Tree Growth, pp. 61–93. Martinus Nijhoff, Dordrecht (1987).

    Google Scholar 

  34. Leal I, Misra S, Attree SM, Fowke LC: Effect of abscisic acid, osmoticum and desiccation on 11S storage protein gene expression in somatic embryos of white spruce. Plant Sci 106: 121–128 (1995).

    Article  Google Scholar 

  35. Leal I, Misra S: Developmental gene expression in conifer embryogenesis and germination. III. Analysis of crystalloid protein mRNAs and desiccation protein mRNAs in the developing embryo and megagametophyte of white spruce (Picea glauca (Moench) Voss). Plant Sci 88: 25–37 (1993).

    Article  Google Scholar 

  36. Leal I, Misra S: Molecular cloning and characterization of legumin-like storage protein cDNA of Douglas fir seeds. Plant Mol Biol 21: 709–715 (1993).

    PubMed  Google Scholar 

  37. Lee GJ, Pokala N, Vierling E: Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea. J Biol Chem 270: 10432–10438 (1995).

    Article  PubMed  Google Scholar 

  38. Lenne C, Douce R: A low molecular mass heat shock protein is localized to higher plant mitochondria. Plant Physiol 105: 1255–1261 (1994).

    PubMed  Google Scholar 

  39. Lindquist S, Craig EA: The heat shock proteins. Annu Rev Genet 22: 631–677 (1988).

    Article  PubMed  Google Scholar 

  40. McElwain EF, Spiker S: A wheat cDNA clone which is homologous to the 17 kDa heat-shock protein gene family of soybean. Nucl Acids Res 17: 1764 (1989).

    PubMed  Google Scholar 

  41. Minowada G, Welch W: Variation in the expression and/or phosphorylation of the human low molecular weight stress protein during in vitro cell differentiation. J Biol Chem 270: 7047–7054 (1995).

    PubMed  Google Scholar 

  42. Misra S: Conifer zygotic embryogenesis, somatic embryogenesis and seed germination: biochemical and molecular advances. Seed Sci Res 4: 357–384 (1994).

    Google Scholar 

  43. Muller-Uri F, Parthier B, Nover L: Jasmonate-induced alteration of gene expression in barley leaf segements analyzed by in vivo and in vitro protein synthesis. Planta 176: 241–247 (1988).

    Google Scholar 

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

    PubMed  Google Scholar 

  45. O'Connell MA: Heat shock proteins and thermotolerance. In: Basra AS (ed) Stress-Induced Gene Expression in Plants, pp. 163–183. Harwood Academic Publishers, Switzerland (1994).

    Google Scholar 

  46. Osteryoung KW, Vierling E: Dynamics of small heat shock protein distribution within the chloroplasts of higher plants. J Biol Chem 269: 28676–28682 (1994).

    PubMed  Google Scholar 

  47. Parsell DA, Lindquist S: The function of heat shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27: 437–496 (1993).

    Article  PubMed  Google Scholar 

  48. Pratt WB: The role of heat shock proteins in regulating the function, folding and trafficking of the glucocorticoid receptor. J Biol Chem 268: 21455–21458 (1993).

    PubMed  Google Scholar 

  49. Reinbothe S, Mollenhauer B, Reinbothe C: JIPs and RIPs: The regulation of plant gene expression by jasmonates in response to environmental cues and pathogens. Plant Cell 6: 1197–1209 (1994).

    Article  PubMed  Google Scholar 

  50. Reinbothe S, Reinbothe C, Lehmann J, Parthier B: Differential accumulation of methyl jasmonate-induced mRNAs in response to abscisic acid and desiccation in barley (Hordeum vulgare). Physiol Plant 86: 49–56 (1992).

    Article  Google Scholar 

  51. Reinbothe S, Reinbothe C, Parthier B: Methyl jasmonate represses translation initiation of a specific set of mRNAs in barley. Plant J 4: 459–467 (1993).

    Article  Google Scholar 

  52. Reinbothe S, Reinbothe C, Parthier B: Methyl jasmonateregulated translation of nuclear-encoded chloroplast proteins in barley. J Biol Chem 268: 10606–10611 (1993).

    PubMed  Google Scholar 

  53. Sambrook J, Fitsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  54. Schmid D, Baici A, Gehring H, Christen P: Kinetics of molecular chaperone action. Science 263: 971–973 (1994).

    PubMed  Google Scholar 

  55. Smith TF, Waterman MS: Identification of common molecular subsequences. J Mol Biol 147: 195–197 (1981).

    Article  PubMed  Google Scholar 

  56. Takahashi T, Komeda Y: Characterization of two genes encoding small heat shock proteins in Arabidopsis thaliana. Mol Gen Genet 219: 365–372 (1989).

    Article  PubMed  Google Scholar 

  57. Taylor MA, Davies HV, Smith SB, Abruzzese A, Gosling PG: Cold-induced changes in gene expression during dormancy breakage in seeds of Douglas fir (Pseudotsuga menziesii). J Plant Physiol 142: 120–123 (1993).

    Google Scholar 

  58. Tranbarger TJ, Misra S: The molecular characterization of a set of cDNAs differentially expressed during Douglas-fir germination and early seeding development. Physiol Plant 95: 456–464 (1995).

    Article  Google Scholar 

  59. Tseng TS, Yeh KW, Yeh CH, Chang FC, Chen YM, Lin CY: Two rice (Oryza sativa) full-length cDNA encoding low molecular weight heat shock proteins. Plant Mol Biol 18: 963–965 (1992).

    PubMed  Google Scholar 

  60. Verwoerd TC, Dekker BMM, Hoekema A: A small scale procedure for the rapid isolation of plant RNAs. Nucl Acids Res 17: 2362 (1989).

    PubMed  Google Scholar 

  61. Vierling E, Sun A: Developmental expression of heat shock proteins in higher plants. In: Cherry JH (ed) Environmental Stress in Plants: Biochemical and Physiological Considerations. pp. 354–354. Springer-Verlag, New York (1989).

    Google Scholar 

  62. Vierling E: The role of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42: 579–620 (1991).

    Article  Google Scholar 

  63. Waters R, Lee GJ, Vierling E: Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot (in press).

  64. Weng J, Wang Z-F, Nguyen HT: Molecular cloning and sequence analysis of cDNAs encoding cytoplasmic low molecular weight heat shock proteins in hexaploid wheat. Plant Sci 92: 35–46 (1993).

    Article  Google Scholar 

  65. Wiech H, Buchner J, Zimmermann R, Jakob U: Hsp90 chaperone protein folding in vitro. Nature 358: 169–170 (1992).

    Article  PubMed  Google Scholar 

  66. Wynn RM, Davie JR, Cox RP, Chuang DT: Molecular chaperones: heat shock proteins, foldases and match-makers. J Lab Clin Med 124: 31–36 (1994).

    PubMed  Google Scholar 

  67. Zarsky V, Garrido D, Eller N, Tupy J, Vicente O, Schoffl F, Heberle-Bors E: The expression of a small heat shock gene is activated during induction of tobacco pollen embryogenesis by starvation. Plant Cell Environ 18: 139–147 (1995).

    Google Scholar 

  68. Zimmerman JL, Apuya N, Darwish K, O'Carroll C: Novel regulation of heat shock genes during carrot somatic embryo development. Plant Cell 1: 1137–1146 (1989).

    Article  PubMed  Google Scholar 

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  1. Department of Biochemistry and Microbiology, University of Victoria, P.O.Box 3055, V8W 3P6, Victoria, B.C., Canada

    Karia H. Kaukinen, Timothy J. Tranbarger & Santosh Misra

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  1. Karia H. Kaukinen
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Kaukinen, K.H., Tranbarger, T.J. & Misra, S. Post-germination-induced and hormonally dependent expression of low-molecular-weight heat shock protein genes in Douglas fir. Plant Mol Biol 30, 1115–1128 (1996). https://doi.org/10.1007/BF00019546

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