Abstract
Transgenic Arabidopsis thaliana plants expressing cell antisense exhibit reduced levels of cell mRNA and protein compared with wild-type plants. The former display significant alterations in their phenotype. cell antisense plants have shorter stems and roots and are mechanically weaker than their wild-type counterparts. In cell antisense plants, the cell wall structure is markedly disrupted: both fluorescent confocal microscopy and scanning electron microscopy revealed `wrinkled' cell walls, thus indicating that CEL1 plays an important role in cell wall relaxation during cell growth and expansion. In cell antisense plants, the number of xylem elements per bundle is smaller than in the wild-type. In addition, both xylem elements and interfascicular fibers are significantly less lignified in the former. It is suggested that in A. thaliana, abnormal cell wall deposition affected by CEL1 depletion is associated not only with cell growth, but also with the differentiation process in the vascular and supporting tissues.
References
An, G. 1987. Binary Ti vector for plant transformation and promoter analysis. Methods Enzymol. 153: 292–305.
Bechtold, N. and Pelletier, G. 1998. In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. In: J.M. Martinez-Zapater and J. Sali-nas (Eds), Methods in Molecular Biology, vol. 82: Arabidopsis Protocols, Humana Press Inc., Totowa, pp. 259–266.
Broido, S., Loyter, A. and Vainstein, A. 1993. Transient expression of photosynthetic genes in transfected albinoid petunia proto-plasts and correct processing of newly synthesized chloroplast-destined polypeptides. Physiol. Plant. 88: 259–266.
Carpita, N.C. and Gibeaut, D.M. 1993. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 3: 1–30.
Cass, L.G., Kirven, K. A. and Christoffersen, R.E. 1990. Isola-tion and characterization of a cellulase gene family member expressed during avocado fruit ripening. Mol. Gen. Genet. 223: 76–86.
Cosgrove, D.J. 1997. Relaxation in a high-stress environment: the molecular bases of extensible cell walls and cell enlargement. Plant Cell. 9: 1031–1041.
del Campillo, E. 1999. Multiple endo-1, 4-beta-D-glucanase (cellu-lase) genes in Arabidopsis. Curr. Top. Dev. Biol. 46: 39–61.
del Campillo, E. and Bennett, A.B. 1996. Pedicel break strength and cellulase gene expression during tomato flower abscission. Plant Physiol. 111: 813–820.
Delmer, D.P. and Amor, Y. 1995. Cellulose biosynthesis. Plant Cell. 7: 987–1000.
Doyel, J.J. and Doyel, J.L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19: 11–15.
Ferrarese, L., Trainotti, L., Moretto, P., Polverino de Laureto, P., Rascio, N. and Casadoro, G. 1995. Differential ethylene-inducible expression of cellulase in pepper plants. Plant Mol. Biol. 29: 735–747.
Fry, S.C., Smith, R.C., Renwick, K.F., Martin, D.J., Hodge, S.K. and Matthews, K.J. 1992. Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem. J. 282: 821–828.
Fukada, H. 1992. Tracheary element formation as a model system for cell differentiation. Int. Rev. Cytol. 136: 289–332.
Gallie, D.R., Sleat, D.E., Wattes, J.W., Turner, P.C., Michael, T. and Wilson, A. 1987. The 5-leader sequence of tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and in vivo. Nucleic Acids Res. 15: 3257–3273.
Goodhew P., Keyse J., Lorimer G., Garrett-Reed A. (1998). Intro-duction to scanning transmition electron microscopy. Springer Verlag. Heidelberg, Germany.
Guilley, H., Dudley, R.K., Jonard, G., Balazs, E. and Richards, K.E. 1982. Transcription of cauliflower mosaic virus DNA: detection of promoter sequences, and characterization of transcripts. Cell. 30: 763–773.
Houtman, C.J. and Atalla, R.H. 1995 Cellulose-lignin interactions. a computational study. Plant Physiol. 107: 977–984.
Johansen, D.A. 1940. Plant microtechnique. McGraw Hill, New York.
Kokubo, A., Sakurai, N., Kuraishi, S. and Takeda, K. 1991. Culm brittleness of barley (Hordeum vulgare L.) mutants is caused by smaller number of cellulose molecules in cell wall. Plant Physiol. 97: 509–514.
Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature. 227: 680–685.
Lashbrook, C.C., Gonzales-Bosch, C. and Bennett, A.B. 1994. Two divergent endo-beta-1, 4-glucanase genes exhibit overlapping ex-pression in ripening fruit and abscission flowers. Plant Cell. 6: 1485–1493.
McQueen-Mason, S.J. and Cosgrove, D.J. 1995 Expansin mode of action on cell walls. Plant Physiol. 107: 87–100
Nicol, F., His, I., Jauneau, A., Vernhettes, S., Cannut, H. and Hofte, H. 1998. A plasma membrane-bound putative endo-1, 4-beta-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J. 17: 5563–5576.
Nishitani, K. and Tominaga, R. 1992 Endo-xyloglucan transferase, a novel class of glycosyltransferase that catalyzes transfer of a segment of xyloglucan molecule to another xyloglucan molecule. J. Biol. Chem. 267: 21058–21064
Raven, J.A. 1977. The Evolution of Vascular Land Plants in Relation to Supracellular Transport Processes. In: H.W. Woolhouse (Ed.), Advances in Botanical Research, Academic Press, London, pp. 153–219.
Roberts, K. 1994. The plant extracellular matrix: in a new expansive mood. Curr. Opin. Cell Biol. 6: 688–694.
Rose, J.K.C. and Bennett, A.B. 1999. Cooperative disassembly of the cellulose-xyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. Trends Plant Sci. 4: 176–183.
Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, New York.
Sass, J.E. 1958. Botanical Microtechnique, 3rd ed. Iowa State College Press, Iowa.
Shani, Z. 2001. The effect of endo 1, 4-b-glucanase and a cellulose binding protein on plant cell elongation. Ph.D. Dissertation, The Hebrew University of Jerusalem, Rehovot, Israel.
Shani, Z., Dekel, M., Tsabary, G. and Shoseyov, O. 1997. Cloning and chracterization of elongation specific endo-1, 4-beta-glucanase (cell1) from Arabidopsis thaliana. Plant Mol. Biol. 34: 837–842.
Shani, Z., Dekel, M., Jensen, C.S., Tzfira, T., Goren, R., Altman, A. and Shoseyov, O. 2000. Arabidopsis thaliana endo-1, 4-beta-glucanase (cell1) promoter mediates uidA expression in elongat-ing tissues of aspen (Populus tremula). J. Plant Physiol. 156: 118–120.
Smart, C.C. and Amrhein, N. 1985. The influence of lignifica-tion on the development of vascular tissue in Vigna radiata L. Protoplasma. 124: 87–95.
Southern, E.M. 1975. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol Biol. 98: 503–517.
Staehelin, L.A. and Moore, I. 1995. The plant golgi apparatus: struc-ture, functional organization and trafficking mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46: 261–288.
Taylor, G.J., Owen, T.P., Koonce, L.T. and Haigler, C.H. 1992. Dispersed lignin in tracheary elements treated with cellulose synthesis inhibitors provides evidence that molecules of the secondary cell wall mediate wall patterning. Plant J. 2: 959–970.
Taylor, N.G., Scheible, W.R., Cutler, S., Somerville, C.R. and Turner, S.R. 1999. The irregular xyle m3 locus of Arabidopsis encodes a cellulose synthase required for secondery cell wall synthesis. Plant Cell. 11: 769–779.
Tsabary, G. 2001. Hormonal regulation and functional analysis of Arabidopsis thaliana endo-1, 4-â-glucanase (cell1). Ph.D. Disser-tation, The Hebrew Univiversity of Jerusalem, Rehovot, Israel.
Tucker, M.L. and Milligan, S.B. 1991. Sequence analysis and com-parison of avocado fruit and bean abscission cellulases. Plant Physiol. 95: 928–933.
Turner, S.R. and Somerville, C.R. 1997. Collapsed xylem phe-notype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondery cell wall. Plant Cell. 9: 689–701.
Van Soest, P.J., Robertson, J.B. and Lewis, B.A. 1991. Meth-ods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74: 3583–3597
Verma, D.P.S., Maclachlan, G.A., Byrne, H. and Edwings, D. 1975. Regulation and in vitro translation of messenger ribonucleic acid for cellulase from auxin-treated pea epicotyls. J. Biol. Chem. 250: 1019–1026.
Woolley, L.C., James, D.J. and Manning, K. 2001. Purification and properties of an endo-â-1, 4-glucanase from strawberry and down-regulation of the corresponding gene, cell1. Planta 214: 11–21.
Zuo J, Niu QW, Nishizawa N, Wu Y, Kost B, Chua NH. 2000. KO-RRIGAN, anArabidopsis endo-1, 4-â-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell. 12: 1137–1152.
Author information
Authors and Affiliations
Corresponding author
Additional information
Equal contributors
Rights and permissions
About this article
Cite this article
Tsabary, G., Shani, Z., Roiz, L. et al. Abnormal `wrinkled' cell walls and retarded development of transgenic Arabidopsis thaliana plants expressing endo-1,4-β-glucanase (cell) antisense. Plant Mol Biol 51, 213–224 (2003). https://doi.org/10.1023/A:1021162321527
Issue Date:
DOI: https://doi.org/10.1023/A:1021162321527