Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1996 Sep;8(9):1477–1490. doi: 10.1105/tpc.8.9.1477

A novel extensin gene encoding a hydroxyproline-rich glycoprotein requires sucrose for its wound-inducible expression in transgenic plants.

J H Ahn 1, Y Choi 1, Y M Kwon 1, S G Kim 1, Y D Choi 1, J S Lee 1
PMCID: PMC161292  PMID: 8837503

Abstract

A novel hydroxyproline-rich glycoprotein (SbHRGP3) that consists of two different domains is encoded by an extensin gene from soybean. The first domain (domain 1) located at the N terminus is composed of 11 repeats of Ser-Pro4-Lys-His-Ser-Pro4-Tyr3-His, whereas the second domain (domain 2) at the C terminus contains five repeats of Ser-Pro4-Val-Tyr-Lys-Tyr-Lys-Ser-Pro4-Tyr-Lys-Tyr-Pro-Ser-Pro5-Tyr-Lys-T yr- Pro-Ser-Pro4-Val-Tyr-Lys-Tyr-Lys. These two repeat motifs are organized in an extremely well-ordered pattern in each domain, which suggests that SbHRGP3 belongs to a new group of proteins having the repeat motifs of two distinct groups of dicot extensins. The expression of the SbHRGP3 gene increased with seedling maturation, and its expression was relatively high in the mature regions of the hypocotyl and in the root of soybean seedlings. An SbHRGP3-beta-glucuronidase (SbHRGP3-GUS) chimeric gene was constructed and expressed in transgenic tobacco plants. The expression of the SbHRGP3-GUS gene was not induced by wounding alone in transgenic tobacco plants; sucrose was also required. Expression was specific to phloem tissues and cambium cells of leaves and stems. In transgenic tobacco seedlings, SbHRGP3-GUS gene expression was activated by the maturation of the primary root and then inactivated; however, reactivation was specifically at the epidermis of the zone from which the lateral root was to be initiated. Its reactivation occurred just before the lateral root initiation. These results indicate that the SbHRGP3 gene in different tissues responds to different signals.

Full Text

The Full Text of this article is available as a PDF (4.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. A simple and general method for transferring genes into plants. Science. 1985 Mar 8;227(4691):1229–1231. doi: 10.1126/science.227.4691.1229. [DOI] [PubMed] [Google Scholar]
  2. Bown D. P., Bolwell G. P., Gatehouse J. A. Characterisation of potato (Solanum tuberosum L.) extensins: a novel extensin-like cDNA from dormant tubers. Gene. 1993 Dec 8;134(2):229–233. doi: 10.1016/0378-1119(93)90098-n. [DOI] [PubMed] [Google Scholar]
  3. Caelles C., Delseny M., Puigdomènech P. The hydroxyproline-rich glycoprotein gene from Oryza sativa. Plant Mol Biol. 1992 Feb;18(3):617–619. doi: 10.1007/BF00040682. [DOI] [PubMed] [Google Scholar]
  4. Carpita N. C., Gibeaut D. M. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 1993 Jan;3(1):1–30. doi: 10.1111/j.1365-313x.1993.tb00007.x. [DOI] [PubMed] [Google Scholar]
  5. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  6. Corbin D. R., Sauer N., Lamb C. J. Differential regulation of a hydroxyproline-rich glycoprotein gene family in wounded and infected plants. Mol Cell Biol. 1987 Dec;7(12):4337–4344. doi: 10.1128/mcb.7.12.4337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. De Loose M., Gheysen G., Tiré C., Gielen J., Villarroel R., Genetello C., Van Montagu M., Depicker A., Inzé D. The extensin signal peptide allows secretion of a heterologous protein from protoplasts. Gene. 1991 Mar 1;99(1):95–100. doi: 10.1016/0378-1119(91)90038-d. [DOI] [PubMed] [Google Scholar]
  8. Dolan L., Janmaat K., Willemsen V., Linstead P., Poethig S., Roberts K., Scheres B. Cellular organisation of the Arabidopsis thaliana root. Development. 1993 Sep;119(1):71–84. doi: 10.1242/dev.119.1.71. [DOI] [PubMed] [Google Scholar]
  9. Ecker J. R., Davis R. W. Plant defense genes are regulated by ethylene. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5202–5206. doi: 10.1073/pnas.84.15.5202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ertl H., Hallmann A., Wenzl S., Sumper M. A novel extensin that may organize extracellular matrix biogenesis in Volvox carteri. EMBO J. 1992 Jun;11(6):2055–2062. doi: 10.1002/j.1460-2075.1992.tb05263.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fong C., Kieliszewski M. J., de Zacks R., Leykam J. F., Lamport D. T. A gymnosperm extensin contains the serine-tetrahydroxyproline motif. Plant Physiol. 1992 Jun;99(2):548–552. doi: 10.1104/pp.99.2.548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Higgins D. G., Bleasby A. J., Fuchs R. CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci. 1992 Apr;8(2):189–191. doi: 10.1093/bioinformatics/8.2.189. [DOI] [PubMed] [Google Scholar]
  13. Hong J. C., Cheong Y. H., Nagao R. T., Bahk J. D., Cho M. J., Key J. L. Isolation and characterization of three soybean extensin cDNAs. Plant Physiol. 1994 Feb;104(2):793–796. doi: 10.1104/pp.104.2.793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hong J. C., Nagao R. T., Key J. L. Developmentally regulated expression of soybean proline-rich cell wall protein genes. Plant Cell. 1989 Sep;1(9):937–943. doi: 10.1105/tpc.1.9.937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Iiyama K., Lam TBT., Stone B. A. Covalent Cross-Links in the Cell Wall. Plant Physiol. 1994 Feb;104(2):315–320. doi: 10.1104/pp.104.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Keller B., Lamb C. J. Specific expression of a novel cell wall hydroxyproline-rich glycoprotein gene in lateral root initiation. Genes Dev. 1989 Oct;3(10):1639–1646. doi: 10.1101/gad.3.10.1639. [DOI] [PubMed] [Google Scholar]
  17. Kieliszewski M. J., Kamyab A., Leykam J. F., Lamport D. T. A Histidine-Rich Extensin from Zea mays Is an Arabinogalactan Protein. Plant Physiol. 1992 Jun;99(2):538–547. doi: 10.1104/pp.99.2.538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kieliszewski M. J., Lamport D. T. Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J. 1994 Feb;5(2):157–172. doi: 10.1046/j.1365-313x.1994.05020157.x. [DOI] [PubMed] [Google Scholar]
  19. Kim S. R., Costa M. A., An G. H. Sugar response element enhances wound response of potato proteinase inhibitor II promoter in transgenic tobacco. Plant Mol Biol. 1991 Nov;17(5):973–983. doi: 10.1007/BF00037137. [DOI] [PubMed] [Google Scholar]
  20. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  21. Leach J. E., Cantrell M. A., Sequeira L. Hydroxyproline-rich bacterial agglutinin from potato : extraction, purification, and characterization. Plant Physiol. 1982 Nov;70(5):1353–1358. doi: 10.1104/pp.70.5.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Li X. B., Kieliszewski M., Lamport D. T. A chenopod extensin lacks repetitive tetrahydroxyproline blocks. Plant Physiol. 1990 Feb;92(2):327–333. doi: 10.1104/pp.92.2.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mellon J. E., Helgeson J. P. Interaction of a hydroxyproline-rich glycoprotein from tobacco callus with potential pathogens. Plant Physiol. 1982 Aug;70(2):401–405. doi: 10.1104/pp.70.2.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Memelink J., Swords K. M., de Kam R. J., Schilperoort R. A., Hoge J. H., Staehelin L. A. Structure and regulation of tobacco extensin. Plant J. 1993 Dec;4(6):1011–1022. doi: 10.1046/j.1365-313x.1993.04061011.x. [DOI] [PubMed] [Google Scholar]
  25. Parmentier Y., Durr A., Marbach J., Hirsinger C., Criqui M. C., Fleck J., Jamet E. A novel wound-inducible extensin gene is expressed early in newly isolated protoplasts of Nicotiana sylvestris. Plant Mol Biol. 1995 Oct;29(2):279–292. doi: 10.1007/BF00043652. [DOI] [PubMed] [Google Scholar]
  26. Qi X., Behrens B. X., West P. R., Mort A. J. Solubilization and partial characterization of extensin fragments from cell walls of cotton suspension cultures. Evidence for a covalent cross-link between extensin and pectin. Plant Physiol. 1995 Aug;108(4):1691–1701. doi: 10.1104/pp.108.4.1691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Raz R., Crétin C., Puigdomènech P., Martínez-Izquierdo J. A. The sequence of a hydroxyproline-rich glycoprotein gene from Sorghum vulgare. Plant Mol Biol. 1991 Feb;16(2):365–367. doi: 10.1007/BF00020571. [DOI] [PubMed] [Google Scholar]
  28. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  29. Salts Y., Kenigsbuch D., Wachs R., Gruissem W., Barg R. DNA sequence of the tomato fruit expressed proline-rich protein gene TPRP-F1 reveals an intron within the 3 untranslated transcript. Plant Mol Biol. 1992 Jan;18(2):407–409. doi: 10.1007/BF00034968. [DOI] [PubMed] [Google Scholar]
  30. Sheng J., D'Ovidio R., Mehdy M. C. Negative and positive regulation of a novel proline-rich protein mRNA by fungal elicitor and wounding. Plant J. 1991 Nov;1(3):345–354. doi: 10.1046/j.1365-313x.1991.t01-3-00999.x. [DOI] [PubMed] [Google Scholar]
  31. Showalter A. M. Structure and function of plant cell wall proteins. Plant Cell. 1993 Jan;5(1):9–23. doi: 10.1105/tpc.5.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Showalter A. M., Zhou J., Rumeau D., Worst S. G., Varner J. E. Tomato extensin and extensin-like cDNAs: structure and expression in response to wounding. Plant Mol Biol. 1991 Apr;16(4):547–565. doi: 10.1007/BF00023421. [DOI] [PubMed] [Google Scholar]
  33. Templeton M. D., Dixon R. A., Lamb C. J., Lawton M. A. Hydroxyproline-Rich Glycoprotein Transcripts Exhibit Different Spatial Patterns of Accumulation in Compatible and Incompatible Interactions between Phaseolus vulgaris and Colletotrichum lindemuthianum. Plant Physiol. 1990 Nov;94(3):1265–1269. doi: 10.1104/pp.94.3.1265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Van Dam M. E., Wuenschell G. E., Arnold F. H. Metal affinity precipitation of proteins. Biotechnol Appl Biochem. 1989 Oct;11(5):492–502. [PubMed] [Google Scholar]
  35. Wyatt R. E., Nagao R. T., Key J. L. Patterns of soybean proline-rich protein gene expression. Plant Cell. 1992 Jan;4(1):99–110. doi: 10.1105/tpc.4.1.99. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wycoff K. L., Powell P. A., Gonzales R. A., Corbin D. R., Lamb C., Dixon R. A. Stress activation of a bean hydroxyproline-rich glycoprotein promoter is superimposed on a pattern of tissue-specific developmental expression. Plant Physiol. 1995 Sep;109(1):41–52. doi: 10.1104/pp.109.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Ye Z. H., Varner J. E. Tissue-Specific Expression of Cell Wall Proteins in Developing Soybean Tissues. Plant Cell. 1991 Jan;3(1):23–37. doi: 10.1105/tpc.3.1.23. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Zhou J., Rumeau D., Showalter A. M. Isolation and characterization of two wound-regulated tomato extensin genes. Plant Mol Biol. 1992 Oct;20(1):5–17. doi: 10.1007/BF00029144. [DOI] [PubMed] [Google Scholar]
  39. von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. doi: 10.1093/nar/14.11.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES