Abstract
Endo-β-1,4-D-glucanases (EGases) are a widespread and vital group of glycosyl hydrolases that generally break the β-1,4-glucosyl linkages. Studies of plant EGases have mainly been concentrated on vegetative growth, while little is currently known about their role in reproductive processes. Using the GUS reporter aided analysis of promoter activities, we identified the expression patterns of two putative Arabidopsis EGases genes (At3g43860 and At4g39000) whose promoters conferred specific localization of the GUS activity in reproductive organs. We found that At3g43860, which is similar to KOR in its protein structural organization, is expressed in mature pollen and the pollen tube, implying that it may have a role in pollen and pollen tube growth. At4g39000 was found to be activated in the developing ovules and seeds, especially at the micropylar end of the inner integuments and nucellus in a proximal-distal pattern. Our results suggested that the two EGases play specific roles in Arabidopsis sexual reproduction.
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References
Cosgrove D.J. 2005. Growth of the plant cell wall. Nature. 6, 850–861.
Lerouxel O., Cavalier D.M., Liepman A.H., Keegstra K. 2006. Biosynthesis of plant cell wall polysaccharides: A complex process. Curr. Opin. Plant Biol. 9, 621–630.
Minic Z., Jouanin L. 2006. Plant glycoside hydrolases in cell wall polysaccharide degradation. Plant Physiol. Biochem. 44, 435–449.
McQueen-Mason S.J., Cosgrove D.J. 1995. Expansin mode of action on cell walls: Analysis of wall hydrolysis, stress relaxation, and binding. Plant Physiol. 107, 87–100.
Foreman J., Demidchik V., Bothwell J.H., Mylona P., Miedema H., Torres M.A., Linstead P., Costa S., Brownlee C., Jones J.D., Davies J.M., Dolan L. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature. 27, 442–446.
Urbanowicz B.R., Bennett A.B., del Campillo E., Catala C., Hayashi T., Henrissat B., Hofte H., McQueen-Mason S.J., Patterson S.E., Shoseyov O., Teeri T.T., Rose J.K.C. 2007. Structural organization and a standardized nomenclature for plant endo-1,4-beta-glucanases cellulases of glycosyl hydrolase family 9. Plant Physiol. 144, 1693–1696.
Nicol F., His I., Jauneau A., Vernhettes S., Canut H., Hofte H. 1998. A plasma membrane-bound putative endo-1,4-β-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J. 17, 5563–5576.
Zuo J., Niu Q.W., Nishizawa N., Wu Y., Kost B., Chua N.H. 2000. KORRIGAN, an Arabidopsis endo-1,4-beta-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell. 12, 1137–1152.
Carpita N.C., 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.
Rose J.C., 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.
Roberts J.A., Whitelaw C.A., Gonzalez-Carranza Z.H., McManus M.T. 2000. Cell separation processes in plants: Models, mechanisms and manipulation. Ann. Bot. 86, 223–235.
Patterson S.E. 2001. Cutting loose: Abscission and dehiscence in Arabidopsis. Plant Physiol. 126, 494–500.
Flors V., de la O. Leyva M., Vicedo B., Finiti I., Real M.D., Garcia-Agustin P., Bennett A.B., Gonzalez-Bosch Carmen. 2007. Absence of the endo-β-1,4-D-glucanases Cel1 and Cel2 reduce susceptibility to Botrytis cinerea in tomato. Plant J. 52, 1027–1040.
Libertini E., Li Y., McQueen-Mason S.J. 2004. Phylogenetic analysis of the plant endo-β-1,4-glucanase gene family. J. Mol. Evol. 58, 506–515.
Urbanowicz B.R., Catala C., Irwin D., Wilson D.B., Ripoll D.R., Rose J.K.C. 2007. A tomato endo-β-1,4-glucanase, SlCel9C1, represents a distinct subclass with a new family of carbohydrate binding modules [CBM49]. J. Biol. Chem. 282, 12066–12074.
Peng L.C., Kawagoe Y., Hogan P., Delmer D. 2002. Sitosterol-β-glucoside as primer for cellulose synthesis in plants. Science. 295, 147–150.
Molhoj M., Johansen B., Ulvskov P., Borkhardt B. 2001. 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.
Shani Z., Dekel M., Tsabary G., Shoseyov O. 1997. Cloning and characterization of elongation-specific endo-beta-1,4-glucanase (Cel1) from Arabidopsis thaliana. Plant Mol. Biol. 34, 837–842.
Shani Z., Dekel M., Tsabary G., Goren R., Shoseyov O. 2004. Growth enhancement of transgenic plants by overexpression of Arabidopsis thaliana endo1,4-β-glucanase (Cel1). Plant Mol. Biol. 14, 321–330.
Shani Z., Dekel M., Roiz L., Horowitz M., Kolosovski N., Lapidot S., Alkan S., Koltai H., Tsabary G., Goren R., Shoseyov Oded. 2006. Expression of endo-1,4-endoglucanase (Cel1) in Arabidopsis thaliana is associated with plant growth, xylem development and cell wall thickening. Plant Cell Rep. 25, 1067–1074.
Tsabary G., Shani Z., Roiz L., Levy I., Riov J., Shoseyov O. 2003. Abnormal ‘wrinkled’ cell walls and retarded development of transgenic Arabidopsis thaliana plants expressing endo-1,4-β-glucanase (Cel1) antisense. Plant Mol. Biol. 51, 213–224.
del Campillo E., Abdel-Aziz A., Crawford D., Patterson S.E. 2004. Root cap specific expression of an endo-β-1,4-D-glucanase cellulase, a new marker to study root development in Arabidopsis. Plant Mol. Biol. 56, 309–323.
Murashige T., Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15, 473–497.
Jefferson R.A., Kavanagh T.A., Bevan M.W. 1987. GUS fusions, beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907.
Clough S.J., Bent A.F. 1998. Floral dip, a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743.
Li H., Lin Y., Heath R.M., Zhu M.X., Yang Z. 1999. Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell. 11, 1731–1742.
Palanivelu R., Brass L., Edlund A.F., Pruess D. 2003. Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell. 114, 47–59.
Smyth D.R., Bowman J.L., Meyerowitz E.M. 1990. Early flower development in Arabidopsis. Plant Cell. 2, 755–767.
Schneitz K., Hulskamp M., Pruitt R.E. 1995. Wild-type ovule development in Arabidopsis thaliana: A light microscope study of cleared whole-mount tissue. Plant J. 7, 731–749.
Winter D., Vinegar B., Nahal H., Ammar R., Wilson G.V., Provart N.J. 2007. An ‘electronic fluorescent pictograph’ browser for exploring and analyzing large-scale biological data sets. PloS ONE. 2, e718.
Yu H.J., Hogan P., Sundaresan V. 2005. Analysis of the female gametophyte transcriptome of Arabidopsis by comparative expression profiling. Plant Physiol. 139, 1853–1869.
Tung C.W., Dwyer K.G., Nasrallah M.E., Nasrallah J.B. 2005. Genome-wide identification of genes expressed in Arabidopsis pistils specifically along the path of pollen tube growth. Plant Physiol. 138, 977–989.
Jiang L., Yang S.L., Xie L.F., Puah C.S., Zhang X.Q., Yang W.C., Sundaresan V., Ye D. 2005. VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell. 17, 584–596.
Takahashi J., Rudsander U.J., Hedenstrom M. 2009. KORRIGAN1 and its aspen homolog PttCel9A1 decrease cellulose crystallinity in Arabidopsis stems. Plant Cell Physiol. 50, 1099–1115.
Skinner D.J., Hill T.A., Gasser C.S. 2004. Regulation of ovule development. Plant Cell. 16, S32–S45.
Pagnussat G.C., Alandete-Saez M., Bowman J.L., Sundaresan V. 2009. Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science. 324, 1684–1689.
Yang W.C., Shi D.Q., Chen Y.H. 2010. Female gametophyte development in flowering plants. Annu. Rev. Plant Biol. 61, 27.1–27.20.
Coimbra S., Almeida J., Junqueira V., Costa M., Pereira L.G. 2007. Arabinogalactan proteins as molecular markers in Arabidopsis thaliana sexual reproduction. J. Exp. Bot. 58, 4027–4035.
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Xie, XJ., Huang, JJ., Gao, HH. et al. Expression patterns of two Arabidopsis endo-β-1,4-glucanase genes (At3g43860, At4g39000) in reproductive development. Mol Biol 45, 458–465 (2011). https://doi.org/10.1134/S0026893311030204
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DOI: https://doi.org/10.1134/S0026893311030204