Skip to main content
SpringerLink
Log in

Evolutionary origin of two genes for chloroplast small heat shock protein of tobacco

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Two different cDNA clones for the chloroplast small heat shock protein (smHSP) were isolated from tobacco (Nicotiana tabacum cv. Petit Havana SR1). One of the cDNAs (type I) has a full-length open reading frame (ORF) of the smHSP of 26.6 kDa. By contrast, the other one (type II) contains an additional nucleotide that causes the frame shift inside a putative ORF for the smHSP. If this nucleotide is neglected, type II cDNA encodes the smHSP that is 89% identical to that encoded by type I cDNA. Southern blot and polymerase chain reaction (PCR) analyses with genomic DNA indicated that tobacco has two different smHSP genes while two ancestors of tobacco, N. sylvestris and N. tomentosiformis, have a single gene that each corresponds to one of the two genes of tobacco. It was also found that one of the tobacco genes has an ORF for the smHSP disrupted by nucleotide insertion in the same way as type II cDNA, while both ancestor genes have a functional ORF. These results suggest that the two smHSP genes of tobacco had been derived from the two ancestor species, and that one of the two genes had been disrupted by nucleotide insertion during the course of the evolution of tobacco. Northern blot and reverse transcription (RT)-PCR analyses demonstrated that both the tobacco genes are expressed upon heat stress, exhibiting different dependences on temperature.

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, Landry J: Expression and function of the lowmolecular-weight heat shock proteins. In: Morimoto R, Tissieres A, Georgopolous C (eds) The Biology of Heat Shock Proteins and Molecular Chaperones, pp. 335–373. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1994).

    Google Scholar 

  2. Brown JWS: A catalogue of splice junction and putative branch point sequences from plant introns. Nucl Acids Res 14: 9549–9559 (1986).

    PubMed  Google Scholar 

  3. Chen Q, Vierling E: Analysis of conserved domains identifies a unique structural feature of a chloroplast heat shock protein. Mol Gen Genet 226: 425–431 (1991).

    PubMed  Google Scholar 

  4. Chen Q, Lauzon LM, DeRocher AE, Vierling E: Accumulation, stability, and localization of a major chloroplast heat-shock protein. J Cell Biol 110: 1873–1883 (1990).

    PubMed  Google Scholar 

  5. Chen Q, Osteryoung K, Vierling E: A 21-kDa chloroplast heat shock protein assembles into high molecular weight complexes in vivo and in organelle. J Biol Chem 269: 13216–13223 (1994).

    PubMed  Google Scholar 

  6. Dean C, Tamaki S, Dunsmuir P, Favreau M, Katayama C, Dooner H, Bedbrook J: mRNA transcripts of several plant genes are polyadenylated at multiple sites in vivo. Nucl Acids Res 14: 2229–2240 (1986).

    PubMed  Google Scholar 

  7. de Boer AD, Weisbeek PJ: Chloroplast protein topogenesis: import, sorting and assembly. Biochim Biophys Acta 1071: 221–253 (1991).

    PubMed  Google Scholar 

  8. Goodspeed TH: The Genus Nicotiana. Chronia Botanica, Waltham, MA (1954).

    Google Scholar 

  9. Gray JC, Kung SD, Wildman SG, Sheen SJ: Origin of Nicotiana tabacum L. detected by polypeptide composition of Fraction I protein. Nature 252: 226–227 (1974).

    PubMed  Google Scholar 

  10. Jakob U, Buchner J: Assisting spontaneity: the role of HSP90 and small HSPs as molecular chaperones. Trends Biochem Sci 19: 205–211 (1994).

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  12. LaFayette PR, Nagao RT, O'Grady K, Vierling E, Key JL: Molecular characterization of cDNAs encoding lowmolecular-weight heat shock proteins of soybean. Plant Mol Biol 30: 159–169 (1996).

    PubMed  Google Scholar 

  13. Lawrence SD, Cline K, Moore GA: Chromoplast development in ripening tomato fruit: identification of cDNAs for chromoplast-targeted proteins and characterization of a cDNA encoding a plastid-localized low-molecular-weight heat shock protein. Plant Mol Biol 33: 483–492 (1997).

    PubMed  Google Scholar 

  14. 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 

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

    Article  PubMed  Google Scholar 

  16. Lütcke 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 

  17. McGookin R: RNA extraction by the guanidine thiocyanate procedure. In: Walker JM (ed) Methods in Molecular Biology, vol. 2, pp. 113–116. Humana Press, New Jersey (1984).

    Google Scholar 

  18. Murray MG, Tompson WF: Rapid isolation of high molecular weight plant DNA. Nucl Acids Res 8: 4321–4325 (1980).

    PubMed  Google Scholar 

  19. Nguyen HT, Weng J, Joshi CP: A wheat (Triticum aestivum) cDNA clone encoding a plastid-localized heat-shock protein. Plant Physiol 103: 675–676 (1993).

    PubMed  Google Scholar 

  20. Obokata J, Mikami K, Hayashida N, Nakamura M, Sugiura M: Molecular heterogeneity of photosystem I. psaD, psaE, psaF, psaH, and psaL are all present in isoforms in Nicotiana spp. Plant Physiol 102: 1259–1267 (1993).

    PubMed  Google Scholar 

  21. 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 

  22. Osteryoung KW, Sundberg H, Vierling E: Poly(A) tail length of a heat shock protein RNA is increased by severe heat stress, but intron splicing is unaffected. Mol Gen Genet 239: 323–333 (1993).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  25. Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    PubMed  Google Scholar 

  26. Schöffl F, Raschke E, Nagao RT: The DNA sequence analysis of soybean heat-shock genes and identification of possible regulatory promoter elements. EMBO J 3: 2491–2497 (1984).

    Google Scholar 

  27. Sheen SJ: Isozymic evidence bearing on the origin of Nicotiana tabacum L. Evolution 26: 143–154 (1972).

    Google Scholar 

  28. Sperisen C, Ryals J, Meins F: Comparison of cloned genes provides evidence for intergenomic exchange of DNA in the evolution of a tobacco glucan endo-1,3-β-glucosidase gene family. Proc Natl Acad Sci USA 88: 1820–1824 (1991).

    PubMed  Google Scholar 

  29. Tanaka Y, Matsuoka M, Yamamoto N, Ohashi Y, Kano-Murakami Y, Ozeki Y: Structure and characterization of a cDNA clone for phenylalanine ammonia-lyase from cutinjured roots of sweet potato. Plant Physiol 90: 1403–1407 (1989).

    Google Scholar 

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

    Article  Google Scholar 

  31. Vierling E, Nagao RT, DeRocher 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 

  32. Waters ER: The molecular evolution of the small heat-shock proteins in plants. Genetics 141: 785–795 (1995).

    PubMed  Google Scholar 

  33. Waters ER, Lee GJ, Vierling E: Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot 47: 325–338 (1996).

    Google Scholar 

Download references

Author information

Author notes

  1. Toshisuke Iwasaki

    Present address: Department of Biology, Niigata University, Niigata, 950-21, Japan

Authors and Affiliations

  1. Department of Plant Physiology and, USA

    Byung-Hyun Lee, Yoshiyuki Tanaka, Toshisuke Iwasaki, Naoki Yamamoto & Mitsue Miyao

  2. Department of Biotechnology, National Institute of Agrobiological Resources (NIAR), 305, Japan

    Toshiaki Kayano

Authors
  1. Byung-Hyun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yoshiyuki Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Toshisuke Iwasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Naoki Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Toshiaki Kayano
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mitsue Miyao
    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

Lee, BH., Tanaka, Y., Iwasaki, T. et al. Evolutionary origin of two genes for chloroplast small heat shock protein of tobacco. Plant Mol Biol 37, 1035–1043 (1998). https://doi.org/10.1023/A:1006067817058

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006067817058

Search

Navigation