Skip to main content
SpringerLink
Log in

Isolation and characterization of two wound-regulated tomato extensin genes

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Extensins comprise a family of structural cell wall hydroxyproline-rich glycoproteins in plants. Two tomato genomic clones, Tom J-10 and Tom L-4, were isolated from a tomato genomic DNA library byin situ plaque hybridization with extensin DNA probes. Tom J-10 encoded an extensin with 388 amino acid residues and a predicted molecular mass of 43 kDa. The Tom J-10 encoded extensin lacked a typical signal peptide sequence, but contained two distinct protein domains consisting of 19 tandem repeats of Ser-Pro4-Ser-Pro-Lys-Tyr-Val-Tyr-Lys at the amino terminus which were directly followed by 8 tandem repeats of the consensus sequence Ser-Pro4-Tyr3-Lys-Ser-Pro4-Ser-Pro at the carboxy terminus. RNA blot hybridization analysis with the Tom J-10 extensin probe demonstrated the presence of a 4.0 kb tomato stem mRNA which accumulated markedly in response to wounding. Tom L-4 encoded an extensin with 322 amino acid residues and a predicted molecular mass of 35 kDa. The Tom L-4 encoded extensin contained a typical signal peptide sequence at the amino terminus and was followed by at least 3 distinct domains. These domains consisted of an amino terminal domain containing several Lys-Pro and Ser-Pro4 repeat units, a central domain with repeats of the consensus sequence Ser-Pro2–5-Thr-Pro-Ser-Tyr-Glu-His-Pro-Lys-Thr-Pro, and a carboxy terminal domain containing repeats of the consensus sequence Ser-Ser-Pro4-Ser-Pro-Ser-Pro4-Thr-Tyr1–3. RNA blot hybridization analysis with the Tom L-4 extensin probe demonstrated the presence of a 2.6 kb tomato stem mRNA which accumulated in response to wounding.

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. Cassab GI, Varner JE: Cell wall proteins. Annu Rev Plant Physiol Plant Mol Biol 39: 321–353 (1988).

    Article  Google Scholar 

  2. Chen J, Varner JE: Isolation and characterization of cDNA clones for carrot extensin and a proline-rich 33-kDa protein. Proc Natl Acad Sci USA 82: 4399–4403 (1985).

    Google Scholar 

  3. Chen J, Varner JE: An extracellular matrix protein in plants: characterization of a genomic clone for carrot extensin. EMBO J 4: 2145–2151 (1985).

    Google Scholar 

  4. Corbin DR, Sauer N, Lamb CJ: Differential regulation of a hydroxyproline-rich glycoprotein gene family in wounded and infected plants. Mol Cell Biol 7: 4337–4344 (1987).

    PubMed  Google Scholar 

  5. Ecker JR, Davis RW: Plant defense genes are regulated by ethylene. Proc Natl Acad Sci USA 84: 5202–5206 (1987).

    Google Scholar 

  6. Epstein L, Lamport DTA: An intramolecular linkage involving isodityrosine in extensin. Phytochemistry 23: 1241–1246 (1984).

    Article  Google Scholar 

  7. Evans IM, Gatehouse LN, Gatehouse JA, Yarwood JN, Boulter D, Croy RRD: The extensin gene family in oilseed rape (Brassica napus L.): characterization of sequences of representative members of the family. Mol Gen Genet 223: 273–287 (1990).

    PubMed  Google Scholar 

  8. Fry SC: Isodityrosine, a new cross-linking amino acid from plant cell wall glycoprotein. Biochem J 204: 449–455 (1982).

    PubMed  Google Scholar 

  9. Fry SC: Cross-linking of matrix polymers in the growing cell walls of angiosperms. Annu Rev Plant Physiol 37: 165–186 (1986).

    Google Scholar 

  10. Gatehouse LN, Evans IM, Gatehouse JA, Croy RRD: Characterization of a rape (Brassica napus L.) extensin gene encoding a polypeptide relatively rich in tyrosine. Plant Sci 71: 223–231 (1990).

    Article  Google Scholar 

  11. Haffner MH, Chin MB, Lane BG: Wheat embryo ribonucleates. XII. Formal characterization of terminal and penultimate nucleoside residues at 5′-ends of ‘capped’ RNA from imbibing wheat embryos. Can J Biochem 56: 729–733 (1978).

    PubMed  Google Scholar 

  12. Heckman JW, Terhune BT, Lamport DTA: Characterization of native and modified extensin monomers and oligomers by electron microscopy and gel filtration. Plant Physiol 86: 848–856 (1988).

    Google Scholar 

  13. Henikoff S: Unidirectional digestion with exonuclease III in DNA sequence analysis. Meth Enzymol 155: 156–165 (1987).

    PubMed  Google Scholar 

  14. Keller B, Lamb CJ: Specific expression of a novel cell wall hydroxyproline-rich glycoprotein gene in lateral root initiation. Gene Devel 3: 1639–1646 (1989).

    Google Scholar 

  15. Lamport DTA: Structure, biosynthesis and significance of cell wall glycoproteins. Recent Adv Phytochem 11: 79–115 (1977).

    Google Scholar 

  16. Leach JE, Cantrell MA, Sequeira L: A hydroxyproline-rich bacterial agglutinin from potato: extraction, purification, and characterization. Plant Physiol 70: 1353–1358 (1982).

    Google Scholar 

  17. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring HarborNY (1982).

    Google Scholar 

  18. Mellon JE, Helgeson JP: Interaction of a hydroxyproline-rich glycoprotein from tobacco callus with potential pathogens. Plant Physiol 70: 401–405 (1982).

    Google Scholar 

  19. Mierendorf RC, Pfeffer D: Direct sequencing of denatured plasmid DNA. Meth Enzymol 152: 556–562 (1987).

    PubMed  Google Scholar 

  20. Promega Corporation: Promega Protocols and Applications Guide. Promega Corporation, Madison, WI (1989).

    Google Scholar 

  21. Queen C, Korn LJ: A comprehensive sequence analysis program for the IBM personal computer. Nucl Acids Res 12: 581–599 (1984).

    PubMed  Google Scholar 

  22. Rivin CI, Zimmer EA, Walbot V: Isolation of DNA and DNA recombinants from maize. In: Sheridan WF (ed) Maize for Biological Research, pp. 161–164. Plant Molecular Biology Association, Charlottesville, VA (1982).

    Google Scholar 

  23. 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 

  24. Sauer N, Corbin DR, Keller B, Lamb CJ: Cloning and characterization of a wound-specific hydroxyproline-rich glycoprotein inPhaseolus vulgaris. Plant Cell Environ 13: 257–266 (1990).

    Google Scholar 

  25. Showalter AM, Butt AD, Kim SH: Molecular details of tomato extensin and glycine-rich protein gene expression. Plant Mol Biol 19: 205–215 (1992).

    Article  PubMed  Google Scholar 

  26. Showalter AM, Rumeau D: Molecular biology of the plant cell wall hydroxyproline-rich glycoproteins. In: Adair WS, Mecham RP (eds) Organization and Assembly of Plant and Animal Extracellular Matrix, pp 247–281. Academic Press. New York (1990).

    Google Scholar 

  27. Showalter AM, Bell JN, Cramer CL, Bailey JA, Varner JE, Lamb CJ: Accumulation of hydroxyproline-rich glycoprotein mRNAs in response to fungal elicitor and infection. Proc Natl Acad Sci USA 82: 6551–6555 (1985).

    Google Scholar 

  28. Showalter AM, Varner JE: Plant hydroxyproline-rich glycoproteins. In: Marcus A (ed) The Biochemistry of Plants, Vol 15, pp. 485–520. Academic Press, New York (1989).

    Google Scholar 

  29. Showalter AM, Zhou J, Rumeau D, Worst SG, Varner JE: Tomato extensin and extensin-like cDNAs: structure and expression in response to wounding. Plant Mol Biol 16: 547–565 (1991).

    PubMed  Google Scholar 

  30. Showalter AM, Varner JE: Molecular details of plant cell wall hydroxyproline-rich glycoprotein expression during wounding and infection. In: Arntzen CJ, Ryan C (eds) Molecular Strategies for Crop Protection, pp. 375–392. Alan R. Liss, New York (1987).

    Google Scholar 

  31. Smith JJ, Muldoon EP, Willard JJ, Lamport DTA: Tomato extensin precursors P1 and P2 are highly periodic structures. Phytochemistry 25: 1021–1030 (1986).

    Article  Google Scholar 

  32. Smith JJ, Muldoon EP, Lamport DTA: Isolation of extensin precursors by direct elution of intact tomato cell suspension cultures. Phytochemistry 23: 1233–1239 (1984).

    Article  Google Scholar 

  33. Stafstrom JP, Staehelin LA: Cross-linking patterns in salt-extractable extensin from carrot cell walls. Plant Physiol 81: 234–241 (1986).

    Google Scholar 

  34. van Holst GJ, Varner JE: Reinforced polyproline II conformation in a hydroxyproline-rich cell wall glycoprotein from carrot root. Plant Physiol 74: 247–251 (1984).

    Google Scholar 

  35. von Heijne G: Transcending the impenetrable: how proteins come to terms with membranes. Biochim Biophys Acta 947: 307–333 (1988).

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany, Molecular and Cellular Biology Program, Ohio University, 45701, Athens, OH, USA

    Jin Zhou & Allan M. Showalter

  2. Centre Physiologie Végétale, Université Paul Sabatier, 118, route de Narbonne, 31062, Toulouse Cedex, France

    Dominique Rumeau

Authors
  1. Jin Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dominique Rumeau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Allan M. Showalter
    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

Zhou, J., Rumeau, D. & Showalter, A.M. Isolation and characterization of two wound-regulated tomato extensin genes. Plant Mol Biol 20, 5–17 (1992). https://doi.org/10.1007/BF00029144

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00029144

Key words

Search

Navigation