Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1993 Jul;5(7):809–820. doi: 10.1105/tpc.5.7.809

Isodityrosine cross-linking mediates insolubilization of cell walls in Chlamydomonas.

S Waffenschmidt 1, J P Woessner 1, K Beer 1, U W Goodenough 1
PMCID: PMC160318  PMID: 7689882

Abstract

Enzymatic removal of the cell wall induces vegetative Chlamydomonas reinhardtii cells to transcribe wall genes and synthesize new hydroxyproline-rich glycoproteins (HRGPs) related to the extensins found in higher plant cell walls. A cDNA expression library made from such induced cells was screened with antibodies to an oligopeptide containing the (SP)x repetitive domains found in Chlamydomonas wall proteins. One of the selected cDNAs encodes an (SP)x-rich polypeptide that also displays a repeated YGG motif. Ascorbate, a peroxidase inhibitor, and tyrosine derivatives were shown to inhibit insolubilization of both the vegetative and zygotic cell walls of Chlamydomonas, suggesting that oxidative cross-linking of tyrosines is occurring. Moreover, insolubilization of both walls was concomitant with a burst in H2O2 production and in extracellular peroxidase activity. Finally, both isodityrosine and dityrosine were found in hydrolysates of the insolubilized vegetative wall layer. We propose that the formation of tyrosine cross-links is essential to Chlamydomonas HRGP insolubilization.

Full Text

The Full Text of this article is available as a PDF (1.6 MB).

Selected References

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

  1. Adair W. S., Apt K. E. Cell wall regeneration in Chlamydomonas: accumulation of mRNAs encoding cell wall hydroxyproline-rich glycoproteins. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7355–7359. doi: 10.1073/pnas.87.19.7355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Biggs K. J., Fry S. C. Solubilization of covalently bound extensin from capsicum cell walls. Plant Physiol. 1990 Jan;92(1):197–204. doi: 10.1104/pp.92.1.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bradley D. J., Kjellbom P., Lamb C. J. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell. 1992 Jul 10;70(1):21–30. doi: 10.1016/0092-8674(92)90530-p. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Chen C. G., Cornish E. C., Clarke A. E. Specific expression of an extensin-like gene in the style of Nicotiana alata. Plant Cell. 1992 Sep;4(9):1053–1062. doi: 10.1105/tpc.4.9.1053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chen J., Varner J. E. An extracellular matrix protein in plants: characterization of a genomic clone for carrot extensin. EMBO J. 1985 Sep;4(9):2145–2151. doi: 10.1002/j.1460-2075.1985.tb03908.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Claes H. Autolyse der Zellwand bei den Gemeten von Chlamydomonas reinhardii. Arch Mikrobiol. 1971;78(2):180–188. [PubMed] [Google Scholar]
  9. Cooper J. B., Varner J. E. Cross-linking of soluble extensin in isolated cell walls. Plant Physiol. 1984 Oct;76(2):414–417. doi: 10.1104/pp.76.2.414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cooper J. B., Varner J. E. Insolubilization of hydroxyproline-rich cell wall glycoprotein in aerated carrot root slices. Biochem Biophys Res Commun. 1983 Apr 15;112(1):161–167. doi: 10.1016/0006-291x(83)91811-9. [DOI] [PubMed] [Google Scholar]
  11. Datta K., Schmidt A., Marcus A. Characterization of two soybean repetitive proline-rich proteins and a cognate cDNA from germinated axes. Plant Cell. 1989 Sep;1(9):945–952. doi: 10.1105/tpc.1.9.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Didierjean L., Frendo P., Burkard G. Stress responses in maize: sequence analysis of cDNAs encoding glycine-rich proteins. Plant Mol Biol. 1992 Feb;18(4):847–849. doi: 10.1007/BF00020034. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Ertl H., Mengele R., Wenzl S., Engel J., Sumper M. The extracellular matrix of Volvox carteri: molecular structure of the cellular compartment. J Cell Biol. 1989 Dec;109(6 Pt 2):3493–3501. doi: 10.1083/jcb.109.6.3493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Everdeen D. S., Kiefer S., Willard J. J., Muldoon E. P., Dey P. M., Li X. B., Lamport D. T. Enzymic cross-linkage of monomeric extensin precursors in vitro. Plant Physiol. 1988 Jul;87(3):616–621. doi: 10.1104/pp.87.3.616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Foerder C. A., Shapiro B. M. Release of ovoperoxidase from sea urchin eggs hardens the fertilization membrane with tyrosine crosslinks. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4214–4218. doi: 10.1073/pnas.74.10.4214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fry S. C. Isodityrosine, a new cross-linking amino acid from plant cell-wall glycoprotein. Biochem J. 1982 May 15;204(2):449–455. doi: 10.1042/bj2040449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Goldman M. H., Pezzotti M., Seurinck J., Mariani C. Developmental expression of tobacco pistil-specific genes encoding novel extensin-like proteins. Plant Cell. 1992 Sep;4(9):1041–1051. doi: 10.1105/tpc.4.9.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Goodenough U. W., Gebhart B., Mecham R. P., Heuser J. E. Crystals of the Chlamydomonas reinhardtii cell wall: polymerization, depolymerization, and purification of glycoprotein monomers. J Cell Biol. 1986 Aug;103(2):405–417. doi: 10.1083/jcb.103.2.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Goodenough U. W., Heuser J. E. The Chlamydomonas cell wall and its constituent glycoproteins analyzed by the quick-freeze, deep-etch technique. J Cell Biol. 1985 Oct;101(4):1550–1568. doi: 10.1083/jcb.101.4.1550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Imam S. H., Buchanan M. J., Shin H. C., Snell W. J. The Chlamydomonas cell wall: characterization of the wall framework. J Cell Biol. 1985 Oct;101(4):1599–1607. doi: 10.1083/jcb.101.4.1599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jaenicke L., Kuhne W., Spessert R., Wahle U., Waffenschmidt S. Cell-wall lytic enzymes (autolysins) of Chlamydomonas reinhardtii are (hydroxy)proline-specific proteases. Eur J Biochem. 1987 Dec 30;170(1-2):485–491. doi: 10.1111/j.1432-1033.1987.tb13725.x. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Kirk M. M., Kirk D. L. Translational regulation of protein synthesis, in response to light, at a critical stage of Volvox development. Cell. 1985 Jun;41(2):419–428. doi: 10.1016/s0092-8674(85)80015-5. [DOI] [PubMed] [Google Scholar]
  25. Lei M., Wu R. A novel glycine-rich cell wall protein gene in rice. Plant Mol Biol. 1991 Feb;16(2):187–198. doi: 10.1007/BF00020551. [DOI] [PubMed] [Google Scholar]
  26. Miller D. H., Lamport D. T., Miller M. Hydroxyproline heterooligosaccharides in Chlamydomonas. Science. 1972 May 26;176(4037):918–920. doi: 10.1126/science.176.4037.918. [DOI] [PubMed] [Google Scholar]
  27. Minami S. A., Goodenough U. W. Novel glycopolypeptide synthesis induced by gametic cell fusion in Chlamydomonas reinhardtii. J Cell Biol. 1978 Apr;77(1):165–181. doi: 10.1083/jcb.77.1.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. O'Neill M. A., Selvendran R. R. Glycoproteins from the cell wall of Phaseolus coccineus. Biochem J. 1980 Apr 1;187(1):53–63. doi: 10.1042/bj1870053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Roberts K., Gurney-Smith M., Hills G. J. Structure, composition and morphogenesis of the cell wall of Chlamydomonas reinhardi. I. Ultrastructure and preliminary chemical analysis. J Ultrastruct Res. 1972 Sep;40(5):599–613. doi: 10.1016/s0022-5320(72)80046-7. [DOI] [PubMed] [Google Scholar]
  31. Rochaix J. D. Genetic analysis of photosynthesis in prokaryotes and lower eukaryotes. Curr Opin Genet Dev. 1992 Oct;2(5):785–791. doi: 10.1016/s0959-437x(05)80140-6. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Sogin M. L. Early evolution and the origin of eukaryotes. Curr Opin Genet Dev. 1991 Dec;1(4):457–463. doi: 10.1016/s0959-437x(05)80192-3. [DOI] [PubMed] [Google Scholar]
  34. Stiefel V., Ruiz-Avila L., Raz R., Pilar Vallés M., Gómez J., Pagés M., Martínez-Izquierdo J. A., Ludevid M. D., Langdale J. A., Nelson T. Expression of a maize cell wall hydroxyproline-rich glycoprotein gene in early leaf and root vascular differentiation. Plant Cell. 1990 Aug;2(8):785–793. doi: 10.1105/tpc.2.8.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Su X., Kaska D. D., Gibor A. Induction of cytosine-rich poly(A)+ RNAs in Chlamydomonas reinhardtii by cell wall removal. Exp Cell Res. 1990 Mar;187(1):54–58. doi: 10.1016/0014-4827(90)90115-q. [DOI] [PubMed] [Google Scholar]
  36. Woessner J. P., Goodenough U. W. Molecular characterization of a zygote wall protein: an extensin-like molecule in Chlamydomonas reinhardtii. Plant Cell. 1989 Sep;1(9):901–911. doi: 10.1105/tpc.1.9.901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. von Heijne G. Signal sequences. The limits of variation. J Mol Biol. 1985 Jul 5;184(1):99–105. doi: 10.1016/0022-2836(85)90046-4. [DOI] [PubMed] [Google Scholar]

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

RESOURCES