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. 1998 Oct 1;17(19):5563–5576. doi: 10.1093/emboj/17.19.5563

A plasma membrane-bound putative endo-1,4-beta-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis.

F Nicol 1, I His 1, A Jauneau 1, S Vernhettes 1, H Canut 1, H Höfte 1
PMCID: PMC1170885  PMID: 9755157

Abstract

Endo-1,4-beta-D-glucanases (EGases) form a large family of hydrolytic enzymes in prokaryotes and eukaryotes. In higher plants, potential substrates in vivo are xyloglucan and non-crystalline cellulose in the cell wall. Gene expression patterns suggest a role for EGases in various developmental processes such as leaf abscission, fruit ripening and cell expansion. Using Arabidopsis thaliana genetics, we demonstrate the requirement of a specialized member of the EGase family for the correct assembly of the walls of elongating cells. KORRIGAN (KOR) is identified by an extreme dwarf mutant with pronounced architectural alterations in the primary cell wall. The KOR gene was isolated and encodes a membrane-anchored member of the EGase family, which is highly conserved between mono- and dicotyledonous plants. KOR is located primarily in the plasma membrane and presumably acts at the plasma membrane-cell wall interface. KOR mRNA was found in all organs examined, and in the developing dark-grown hypocotyl, mRNA levels were correlated with rapid cell elongation. Among plant growth factors involved in the control of hypocotyl elongation (auxin, gibberellins and ethylene) none significantly influenced KOR-mRNA levels. However, reduced KOR-mRNA levels were observed in det2, a mutant deficient for brassinosteroids. Although the in vivo substrate remains to be determined, the mutant phenotype is consistent with a central role for KOR in the assembly of the cellulose-hemicellulose network in the expanding cell wall.

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Selected References

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  1. Albersheim P. The walls of growing plant cells. Sci Am. 1975 Apr;232(4):80–95. doi: 10.1038/scientificamerican0475-80. [DOI] [PubMed] [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  3. Arioli T., Peng L., Betzner A. S., Burn J., Wittke W., Herth W., Camilleri C., Höfte H., Plazinski J., Birch R. Molecular analysis of cellulose biosynthesis in Arabidopsis. Science. 1998 Jan 30;279(5351):717–720. doi: 10.1126/science.279.5351.717. [DOI] [PubMed] [Google Scholar]
  4. Becker D. Binary vectors which allow the exchange of plant selectable markers and reporter genes. Nucleic Acids Res. 1990 Jan 11;18(1):203–203. doi: 10.1093/nar/18.1.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brummell D. A., Catala C., Lashbrook C. C., Bennett A. B. A membrane-anchored E-type endo-1,4-beta-glucanase is localized on Golgi and plasma membranes of higher plants. Proc Natl Acad Sci U S A. 1997 Apr 29;94(9):4794–4799. doi: 10.1073/pnas.94.9.4794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Canut H., Brightman A., Boudet A. M., Morré D. J. Plasma membrane vesicles of opposite sidedness from soybean hypocotyls by preparative free-flow electrophoresis. Plant Physiol. 1988 Feb;86(2):631–637. doi: 10.1104/pp.86.2.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Canut H., Brightman A., Boudet A. M., Morré D. J. Tonoplast vesicles of opposite sidedness from soybean hypocotyls by preparative free-flow electrophoresis. Plant Physiol. 1990 Nov;94(3):1149–1156. doi: 10.1104/pp.94.3.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Carpita Nicholas C. STRUCTURE AND BIOGENESIS OF THE CELL WALLS OF GRASSES. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):445–476. doi: 10.1146/annurev.arplant.47.1.445. [DOI] [PubMed] [Google Scholar]
  10. Cass L. G., Kirven K. A., Christoffersen R. E. Isolation and characterization of a cellulase gene family member expressed during avocado fruit ripening. Mol Gen Genet. 1990 Aug;223(1):76–86. doi: 10.1007/BF00315799. [DOI] [PubMed] [Google Scholar]
  11. Chauvaux S., Béguin P., Aubert J. P. Site-directed mutagenesis of essential carboxylic residues in Clostridium thermocellum endoglucanase CelD. J Biol Chem. 1992 Mar 5;267(7):4472–4478. [PubMed] [Google Scholar]
  12. Cosgrove D. J. Relaxation in a high-stress environment: the molecular bases of extensible cell walls and cell enlargement. Plant Cell. 1997 Jul;9(7):1031–1041. doi: 10.1105/tpc.9.7.1031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Creusot F., Fouilloux E., Dron M., Lafleuriel J., Picard G., Billault A., Le Paslier D., Cohen D., Chabouté M. E., Durr A. The CIC library: a large insert YAC library for genome mapping in Arabidopsis thaliana. Plant J. 1995 Nov;8(5):763–770. doi: 10.1046/j.1365-313x.1995.08050763.x. [DOI] [PubMed] [Google Scholar]
  14. Delarue M., Prinsen E., Onckelen H. V., Caboche M., Bellini C. Sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis. Plant J. 1998 Jun;14(5):603–611. doi: 10.1046/j.1365-313x.1998.00163.x. [DOI] [PubMed] [Google Scholar]
  15. Desnos T., Orbović V., Bellini C., Kronenberger J., Caboche M., Traas J., Höfte H. Procuste1 mutants identify two distinct genetic pathways controlling hypocotyl cell elongation, respectively in dark- and light-grown Arabidopsis seedlings. Development. 1996 Feb;122(2):683–693. doi: 10.1242/dev.122.2.683. [DOI] [PubMed] [Google Scholar]
  16. Dubreucq B., Grappin P., Caboche M. A new method for the identification and isolation of genes essential for Arabidopsis thaliana seed germination. Mol Gen Genet. 1996 Aug 27;252(1-2):42–50. doi: 10.1007/BF02173203. [DOI] [PubMed] [Google Scholar]
  17. Ferrarese L., Trainotti L., Moretto P., Polverino de Laureto P., Rascio N., Casadoro G. Differential ethylene-inducible expression of cellulase in pepper plants. Plant Mol Biol. 1995 Nov;29(4):735–747. doi: 10.1007/BF00041164. [DOI] [PubMed] [Google Scholar]
  18. Fujioka S., Li J., Choi Y. H., Seto H., Takatsuto S., Noguchi T., Watanabe T., Kuriyama H., Yokota T., Chory J. The Arabidopsis deetiolated2 mutant is blocked early in brassinosteroid biosynthesis. Plant Cell. 1997 Nov;9(11):1951–1962. doi: 10.1105/tpc.9.11.1951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gendreau E., Traas J., Desnos T., Grandjean O., Caboche M., Höfte H. Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 1997 May;114(1):295–305. doi: 10.1104/pp.114.1.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Guzmán P., Ecker J. R. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell. 1990 Jun;2(6):513–523. doi: 10.1105/tpc.2.6.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hayashi T., Maclachlan G. Pea xyloglucan and cellulose : I. Macromolecular organization. Plant Physiol. 1984 Jul;75(3):596–604. doi: 10.1104/pp.75.3.596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Henrissat B., Claeyssens M., Tomme P., Lemesle L., Mornon J. P. Cellulase families revealed by hydrophobic cluster analysis. Gene. 1989 Sep 1;81(1):83–95. doi: 10.1016/0378-1119(89)90339-9. [DOI] [PubMed] [Google Scholar]
  23. Hoson T., Nevins D. J. beta-d-Glucan Antibodies Inhibit Auxin-Induced Cell Elongation and Changes in the Cell Wall of Zea Coleoptile Segments. Plant Physiol. 1989 Aug;90(4):1353–1358. doi: 10.1104/pp.90.4.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Höfte H., Chrispeels M. J. Protein sorting to the vacuolar membrane. Plant Cell. 1992 Aug;4(8):995–1004. doi: 10.1105/tpc.4.8.995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Inouhe M., Nevins D. J. Inhibition of auxin-induced cell elongation of maize coleoptiles by antibodies specific for cell wall glucanases. Plant Physiol. 1991 Jun;96(2):426–431. doi: 10.1104/pp.96.2.426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jauneau A., Morvan C., Lefebvre F., Demarty M., Ripoll C., Thellier M. Differential extractability of calcium and pectic substances in different wall regions of epicotyl cells in young flax plants. J Histochem Cytochem. 1992 Aug;40(8):1183–1189. doi: 10.1177/40.8.1377735. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Lashbrook C. C., Gonzalez-Bosch C., Bennett A. B. Two divergent endo-beta-1,4-glucanase genes exhibit overlapping expression in ripening fruit and abscising flowers. Plant Cell. 1994 Oct;6(10):1485–1493. doi: 10.1105/tpc.6.10.1485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lin M., Turpin D. H., Plaxton W. C. Pyruvate kinase isozymes from the green alga, Selenastrum minutum. I. Purification and physical and immunological characterization. Arch Biochem Biophys. 1989 Feb 15;269(1):219–227. doi: 10.1016/0003-9861(89)90103-3. [DOI] [PubMed] [Google Scholar]
  30. Moore P. J., Darvill A. G., Albersheim P., Staehelin L. A. Immunogold localization of xyloglucan and rhamnogalacturonan I in the cell walls of suspension-cultured sycamore cells. Plant Physiol. 1986 Nov;82(3):787–794. doi: 10.1104/pp.82.3.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pear J. R., Kawagoe Y., Schreckengost W. E., Delmer D. P., Stalker D. M. Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12637–12642. doi: 10.1073/pnas.93.22.12637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tucker M. L., Milligan S. B. Sequence analysis and comparison of avocado fruit and bean abscission cellulases. Plant Physiol. 1991 Mar;95(3):928–933. doi: 10.1104/pp.95.3.928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Vogel J. P., Woeste K. E., Theologis A., Kieber J. J. Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4766–4771. doi: 10.1073/pnas.95.8.4766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wu S. C., Blumer J. M., Darvill A. G., Albersheim P. Characterization of an endo-beta-1,4-glucanase gene induced by auxin in elongating pea epicotyls. Plant Physiol. 1996 Jan;110(1):163–170. doi: 10.1104/pp.110.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. del Campillo E., Bennett A. B. Pedicel breakstrength and cellulase gene expression during tomato flower abscission. Plant Physiol. 1996 Jul;111(3):813–820. doi: 10.1104/pp.111.3.813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]

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