Abstract
The Arabidopsis KOR gene encodes a membrane-anchored endo-1,4-β-D-glucanase involved in cell wall assembly. To obtain a more detailed knowledge of the small gene family encoding membrane-anchored endo-1,4-β-D-glucanases in Arabidopsis thaliana, we have characterized two additional membrane-anchored endo-1,4-β-D-glucanase genes. Sequence comparison indicates that KOR2 is distantly related to KOR and other plant membrane-anchored endo-1,4-β-D-glucanases. The expression of KOR2 and KOR3 was followed by the β-glucuronidase (gusA) reporter-gene method. While the KOR gene is most often expressed throughout the plant, KOR2::gusA and KOR3::gusA are active only in restricted cell types. We demonstrate that KOR2::gusA is expressed very early in the development of root hairs within the root differentiation zone (specialization zone) but not in the root-hair-bearing epidermal cells at the root/shoot junction (transition zone). Furthermore, KOR2::gusA is expressed in the proximal parts of leaves and floral organs (rosette and cauline leaves, sepals, petals and stamens), and in trichomes, as they develop at the tip of young leaves and later in more basal regions of the leaf blade. The KOR3::gusA construct is expressed in the trichome support cells that form a ring at the base of each trichome and in the bundle sheath cells which surround the vascular bundle within the leaf mesophyll tissue. Reverse transcription-polymerase chain reaction of Arabidopsis RNA confirmed the expression of KOR2::gusA and KOR3::gusA. In conclusion, although KOR2 and KOR3 have more restricted expression patterns than the previously characterized KOR gene, they are expressed in cell types at time points where cell wall assembly is likely to occur and, interestingly, differentially expressed in leaf trichomes and their support cells.
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Beguin, P., Millet, J., Chauvaux, S., Salamitou, S., Tokatlidis, K., Navas, J., Fujino, T., Lemaire, M., Raynaud, O. and Daniel, M.K. 1992. Bacterial cellulases. Biochem. Soc. Trans. 20: 42–46.
Bernhardt, C. and Tierney, M.L. 2000. Expression of AtPRP3, a proline-rich structural cell wall protein from Arabidopsis,is regulated by cell-type-specific developmental pathways involved in root hair formation. Plant Physiol. 122: 705–714.
Brummell, D.A., Catala, C., Lashbrook, C.C. and Bennett, A.B. 1997. A membrane-anchored E-type endo-1,4-β-glucanase is localized on golgi and plasma membranes of higher plants. Proc. Natl. Acad. Sci. USA 94: 4794–4799.
Byrne, K.A., Lehnert, S.A., Johnson, S.E. and Moore, S.S. 1999. Isolation of a cDNA encoding a putative cellulase in the red claw crayfish Cherax quadricarinatus. Gene 239: 317–324.
Cassab, G.I. 1998. Plant cell wall proteins. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 281–309.
Church, G.M. and Gilbert, W. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81: 1991–1995.
Davies, G. and Henrissat, B. 1995. Structures and mechanisms of glycosyl hydrolases. Structure 3: 853–859.
del Campillo, E. 1999. Multiple endo-1,4-β-D-glucanase (cellulase) genes in Arabidopsis. Curr. Top. Dev. Biol. 46: 39–61.
Dolan, L., Janmaat, K., Willemsen, V., Linstead, P., Poethig, S., Roberts, K. and Scheres, B. 1993. Cellular organisation of the Arabidopsis thaliana root. Development 119: 71–84.
d'souza, S.E., Ginsberg, M.H. and Plow, E.F. 1991. Arginyl-glycyl-aspartic acid (RGD): a cell adhesion motif. Trends Biochem. Sci. 16: 246–250.
Hajdukiewicz, P., Svab, Z. and Maliga, P. 1994. The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25: 989–994.
Haughn, G.W. and Somerville, C.R. 1988. Genetic control of morphogenesis in Arabidopsis. Dev. Genet. 9: 73–89.
Henrissat, B. 1991. A classification of glycosyl hydrolases based on amino-acid sequence similarities. Biochem. J. 280: 309–316.
Henrissat, B. and Bairoch, A. 1993. New families in the classification of glycosyl hydrolases based on amino-acid sequence similarities. Biochem. J. 293: 781–788.
Henrissat, B. and Bairoch, A. 1996. Updating the sequence-based classification of glycosyl hydrolases. Biochem. J. 316: 695–696.
Hirsinger, C., Salva, I., Marbach, J., Durr, A., Fleck, J. and Jamet, E. 1999. The tobacco extensin gene Ext 1.4 is expressed in cells submitted to mechanical constraints and in cells proliferating under hormone control. J. Exp. Bot. 50: 343–355.
Hülskamp, M., Miséra, S. and Jürgens, G. 1994. Genetic dissection of trichome cell development in Arabidopsis. Cell 76: 555–566.
Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. 1987. GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901–3907.
Kinsman, E.A. and Pyke, K.A. 1998. Bundle sheath cells and cell-specific plastid development in Arabidopsis leaves. Development 125: 1815–1822.
Lashbrook, C.C., Gonzalez-Bosch, C. and Bennett, A.B. 1994. Two divergent endo-β-1,4-glucanase genes exhibit overlapping expression in ripening fruit and abscising flowers. Plant Cell 6: 1485–1493
Marks, M.D. and Esch, J. 1992. Trichome formation in Arabidopsis thaliana as a genetic model system for studying cell expansion. In: D.D. Randall (Ed.) Current Topics in Plant Biochemistry and Physiology, Interdisciplinary Plant Biochemistry and Physiology Program 11, University of Missouri, Columbia, MO, pp. 131–142.
Marks, M.D., Esch, J., Herman, P., Sivakumaran, S. and Oppenheimer, D. 1991. A model for cell-type determination and differentiation in plants. In: G. Jenkins and W. Schuch (Eds.) Molecular Biology of Plant Development, The Company of Biologists, Cambridge, UK, pp. 77–87.
Masucci, J.D. and Schiefelbein, J.W. 1994. The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin-and ethylene-associated process. Plant Physiol. 106: 1335–1346.
Matthysse, A.G., White, S. and Lightfoot, R. 1995a. Genes required for cellulose synthesis in Agrobacterium tumefaciens. J. Bact. 177: 1069-1075.
Matthysse, A.G., Thomas, D.L. and White, A.R. 1995b. Mechanism of cellulose synthesis in Agrobacterium tumefaciens. J. Bact. 177: 1076–1081.
Miller, D.D., de Ruijter, N.C. and Emons, A.M. 1997. From signal to form: aspects of the cytoskeleton-plasma membrane-cell wall continuum in root hair tips. J. Exp. Bot. 48: 1881–1896.
Mølhøj, M., Johansen, B., Ulvskov, P. and Borkhardt, B. 2001. The expression of a membrane-anchored endo-1,4-â-glucanase from Brassica napus, orthologous to KOR from Arabidopsis thaliana, is inversely correlated to elongation in light-grown plants. Plant Mol. Biol. 45: 93–105.
Nicol, F., His, I., Jauneau, A., Vernhettes, S., Canut, H. and Höfte, H. 1998. A plasma membrane-bound putative endo-1,4-â-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J. 17: 5563–5576.
Pitts, R.J., Cernac, A. and Estelle, M. 1998. Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J. 16: 553–560.
Pyke, K.A., Marrison, J.L. and Leech, R.M. 1991. Temporal and spatial development of the cells of the expanding first leaf of Arabidopsis thaliana (L.) Heynh. J. Exp. Bot. 42: 1407–1416.
Quaedvlieg, N.E.M., Schlaman, H.R.M., Admiraal, P.C., Wijting, S.E., Stougaard, J. and Spaink, H.P. 1998. Fusions between green fluorescent protein and â-glucuronidase as sensitive and vital bifunctional reporters in plants. Plant Mol. Biol. 37: 715–727.
Rosso, M.N., Favery, B., Piotte, C., Arthaud, L., de Boer, J.M., Hussey, R.S., Bakker, J., Baum, T.J. and Abad, P. 1999. Isolation of a cDNA encoding a â-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita and expression analysis during plant parasitism. Mol. Plant-Microbe. Interact. 12: 585–591.
Ruoslahti, E. and Pierschbacher, M.D. 1986. Arg-Gly-Asp: a versatile cell recognition signal. Cell 44: 517–518.
Schneider, K., Wells, B., Dolan, L. and Roberts, K. 1997. Structural and genetic analysis of epidermal cell differentiation in Arabidopsis primary roots. Development 124: 1789–1798.
Schulein, M. 1998. Kinetics of fungal cellulases. Biochem. Soc. Trans. 26: 164–167.
Shani, Z., Dekel, M., Tsabary, G. and Shoseyov, O. 1997. Cloning and characterization of elongation specific endo-1,4-â-glucanase (cel1) from Arabidopsis thaliana. Plant Mol. Biol. 34: 837–842.
Shirsat, A.H., Bell, A., Spence, J. and Harris, J.N. 1996. The Bras-sica napus extA extensin gene is expressed in regions of the plant subject to tensile stresses. Planta 199: 618–624.
Sieburth, L.E. 1999. Auxin is required for leaf vein pattern in Arabidopsis. Plant Physiol. 121: 1179–1190.
Tanimoto, M., Roberts, K. and Dolan, L. 1995. Ethylene is a positive regulator of root hair development in Arabidopsis thaliana.Plant J. 8: 943–948.
Taylor, J.E., Coupe, S.A., Ploton, S. and Roberts, J.A. 1994. Characterization and accumulation pattern of an mRNA encoding an abscission-related endo-â-1,4-glucanase from leaflets of Sambucus nigra. Plant Mol. Biol. 24: 961–964.
Trainotti, L., Spolaore, S., Pavanello, A., Baldan, B. and Casadoro, G. 1999. A novel E-type endo-â-1,4-glucanase with a putative cellulose-binding domain is highly expressed in ripening strawberry fruits. Plant Mol. Biol. 40: 323–332.
Tucker, M.L., Durbin, M.L., Clegg, M.T. and Lewis, L.N. 1987. Avocado cellulase: nucleotide sequense of a putative full-length cDNA clone and evidence for a small gene family. Plant Mol. Biol. 9: 197–203.
Watanabe, H., Noda, H., Tokuda, G., Lo, N. 1998. A cellulase gene of termite origin. Nature 394: 330–331.
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Mølhøj, M., Jørgensen, B., Ulvskov, P. et al. Two Arabidopsis thaliana genes, KOR2 and KOR3, which encode membrane-anchored endo-1,4-β-D-glucanases, are differentially expressed in developing leaf trichomes and their support cells. Plant Mol Biol 46, 263–275 (2001). https://doi.org/10.1023/A:1010688726755
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DOI: https://doi.org/10.1023/A:1010688726755