Abstract
The plant cell wall is of supermolecular architecture, and is composed of various types of heterogeneous polymers. A few thousand enzymes and structural proteins are directly involved in the construction processes, and in the functional aspects of the dynamic architecture in Arabidopsis thaliana. Most of these proteins are encoded by multigene families, and most members within each family share significant similarities in structural features, but often exhibit differing expression profiles and physiological functions. Thus, for the molecular dissection of cell wall dynamics, it is necessary to distinguish individual members within a family of proteins. As a first step towards characterizing the processes involved in cell wall dynamics, we have manufactured a gene-specific 70-mer oligo microarray that consists of 765 genes classified into 30 putative families of proteins that are implicated in the cell wall dynamics of Arabidopsis. By using this array system, we identified several sets of genes that exhibit organ preferential expression profiles. We also identified gene sets that are expressed differentially at certain specific growth stages of the Arabidopsis inflorescence stem. Our results indicate that there is a division of roles among family members within each of the putative cell wall-related gene families.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- PME:
-
pectin methyleaterase
- RT-PCR:
-
reverse transcription-polymerase chain reaction
- XTH:
-
xyloglucan endotransglucosylase/hydrolase
References
Arabidopsis Genome Initiative 2000. Analysis to the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.
Ariizumi, T., Amagai, M., Shibata, D., Hatakeyama, K., Watanabe, W. and Toriyama, K. 2002. Comparative study of promoter activity of three anther-specific genes encoding lipid transfer protein, xyloglucan endotransglucosylase/hydrolase and polygalacturonase in transgenic Arabidopsis thaliana. Plant Cell Rep. 21: 90–96.
Baumberger, N., Steiner, M., Ryser, U., Keller, B. and Ringli, C. 2003. Synergistic interaction of the two paralogous Arabidopsis genes LRX1 and LRX2 in cell wall formation during root hair development. Plant J. 35: 71–81.
Bourquin, V., Nishikubo, N., Abe, H., Brumer, H., Denmen, S., Eklund, M., Christiermin, M., Teeri, T.T., Sundberg, B. and Mellerowicz, E.J. 2002. Xyloglucan endotransglycosylases have a function during the formation of secondary cell walls of vascular tissues. Plant Cell 14: 3073–3088.
Brownleader, M.D., Hopkins, J., Mobasheri, A., Dey, P.M., Jackson, P. and Trevan, M. 2000. Role of extensin peroxidase in tomato (Lycopersicon esculentum Mill) cells in suspension culture. Planta 191: 457–469.
Buell, C.R. 2002. Current status of the sequence of the rice genome and prospects for finishing the first monocot genome. Plant Physiol. 130: 1585–1586.
Carpin, S., Crèvecoeur, M., Greppin, H. and Penel, C. 1997. Molecular cloning and tissue-specific expression of an anionic peroxidase in zucchini. Plant Physiol. 120: 799–810.
Cho, H.T. and Cosgrove, D.J. 2002. Regulation of root hair initiation and expansin gene expression in Arabidopsis. Plant Cell 14: 3237–3253.
Cho, H.T. and Kende, H. 1997. Expression of expansin genes is correlated with growth in deepwater Rice. Plant Cell 9: 1661–1671.
Choi, D., Lee, Y., Cho, H.T. and Kende, H. 2003. Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15: 1386–1398.
Córdoba-Pedregosa, M.d.C, González-Reyes, J.A., Canadillas M.d.S., Navas, P. and Cordoba, F. 1996. Role of apoplastic and cell-wall peroxidases on the stimulation of root elongation by ascorbate. Plant Physiol. 112: 1119–1125.
Córdoba-Pedregosa M.d.C, Córdoba, F., Villalba, J.M. and González-Reyes, J.A. 2003. Zonal changes in ascorbate and hydrogen peroxide contents, peroxidase, and ascorbate-related enzyme activities in onion roots. Plant Physiol. 131: 697–706.
Coutinho, P.M. and Henrissat, B. 1999. Carbohydrate-active enzymes: an integrated database approach. In: H.J. Glbert, G. Davies, B. Henrissat and B. Svensson (Eds.), “Recent Advances in Carbohydrate Bioengineering”, The Royal Society of Chemistry. Cambridge, pp. 3–12.
de la Torre, F., Sampedro, J., Zarra, I. and Revilla, G. 2002. AtFXG1, an Arabidopsis gene encoding α-l-fucosidase active against fucosylated xyloglucan oligosaccharides. Plant Physiol. 128: 247–255.
de Oliveira, D.E., Seurinck, J., Inze, D., Montagu, M.V. and Botterman, J. 2000. Differential expression of five Arabidopsis genes encoding glycine-rich proteins. Plant Cell 2: 427–436.
Dong, X., Mindrinos, M., Daviqb, K.R. and Asubel, F.M. 1991. Induction of Arabidopsis defense genes by virulent and avirulent Psudomonas syringae strains and by a cloned avirulence gene. Plant Cell 65: 57–60.
Faik, A., Price, N.J., Raikhel, N.V. and Keegstra, K. 2002. An Arabidopsis gene encoding an α-xylosyltransferase involved in XyG biosynthesis. Proc. Natl. Acad. Sci. USA 99: 7797–7802.
Fry, F.C. 1986. Cross-linking of matrix polymers in the growing cell walls of angiosperms. Annu. Rev. Plant. Physiol. 37: 165–186.
He, Z.H., Cheeseman, I., He, D. and Kohorn, B.D. 1999. A cluster of five cell wall-associated receptor kinase genes, Wak1–5, are expressed in specific organs of Arabidopsis. Plant. Mol. Biol. 39: 1189–1196.
Holland, N., Holland, D., Helentjaris, T., Dhugga, K.S., Xoconostle-Cazares, B. and Delmer, D.P. 2000. A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol. 123: 1313–1323.
Hong, Z., Zhang, Z., Olson, J.M. and Verma, D.P.S. 2001. A novel UDP-glucose transferase is part of the callose synthase complex and interacts with phragmoplastin at the forming cell plate. Plant Cell 13: 769–780.
Hyodo, H., Yamakawa, S., Takeda, Y., Tsuduki, M., Yokota, A., Nishitani, K. and Kohchi, T. 2003. Active gene expression of a xyloglucan endotransglucosylase/hydrolase gene, XTH9, in inflorescence apices is related to cell elongation in Arabidopsis thaliana. Plant Mol. Biol. 52: 473–482.
Johnson K.L., Jones B.J., Schultz C.J. and Bacic A. 2003. Nonenzyme cell wall (glyco)proteins. In: J.K.C. Rose (Ed.) The Plant Cell Wall (ISBN 0-8493-2811-X) CRC Press LLC, FL, USA, pp. 111–154.
Keegstra, K. and Raikhel, N. 2001. Plant glycosyltransferases. Curr. Opin. Plant Biol. 4: 219–24.
Li, Y., Darley, C.P., Ongaro, V., Fleming, A., Schipper, O., Baldauf, S.L. and McQueen-Mason, S.J. 2002. Plant expansins are a complex multigene family with an ancient evolutionary origin. Plant Physiol. 128: 854–864.
Llorente, F., Lopez-Cobollo, R.M., Catalá, R., Martínez-Zapater, J.M. and Salinas, J. 2002. A novel cold-inducible gene from Arabidopsis, RCI3, encodes a peroxidase that constitutes a component for stress tolerance. Plant J. 32: 13–24.
McQueen-Mason, S., Durachko, D.M. and Cosgrove, D.J. 1992. Two endogenous proteins that induce cell wall extension in plants. Plant Cell. 4: 1425–1433.
Mayfield, J.A., Fiebig, A., Johnstone, S.E. and Preuss, D. 2001. Gene families from the Arabidopsis thaliana pollen coat proteome. Nature 292: 2482–2485.
Micheli, F. 2001. Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trend Plant Sci. 6: 414–419.
Mølhøj, M., Pagant, S. and Höfte, H. 2002. Towards understanding the role of membrane-bound endo-β-1,4-glucanases in cellulose biosynthesis. Plant Cell Physiol. 43: 1399–1406.
Murashige, T. and Skoog, F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15: 473–496.
Nakamura Yokoyama Tomita, T. R. E. and Nishitani, K 2003. Two azuki bean XTH genes, VaXTH1 and VaXTH2, with similar tissue specific expression profiles, are differentlty regulated by auxin. Plant. Cell Physiol. 44: 16–24.
Nicol, F., His, I., Jauneau, A., Vernhettes, S., Canut, H. and 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:.
Nishitani, K. and Tominaga, R. 1992. Endoxyloglucan 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.
Ori, N., Sessa, G., Lotan, T., Himmelhoch, S. and Fluhr, R. 1990. A major stylar matrix polypeptide (sp41) is a member of the pathogenesis-related protein superclass. EMBO J. 9: 3429–3436.
Park, Y.W., Tominaga, R., Sugiyama, J., Furuta, Y., Tanimoto, E., Samejima, M., Sakai, F. and Hayashi, T. 2003. Enhancement of growth by expression of poplar cellulase in Arabidopsis thaliana. Plant J. 33: 1099–1106:.
Peterson, M., Sander, L., Child, R., Onckelen, H. Van, Ulvskov, P. and Borkhardt, B. 1996. Isolation and characterization of a pod dehiscence zone-specific polygalacturonase from Brassica napus.. Plant Mol. Biol. 31: 517–527.
Price, N.J., Pinheiro, C., Soares, CM., Ashford, D.A., Ricardo, C.P. and Jackson, P.A. 2003. A biochemical and molecular characterization of LEP1, an extensin peroxidase from lupin. J. Biol. Chem. 278: 41389–41399.
Rose, J.K.C., Braam, J., Fry, S.C and Nishitani, K 2002. The XTH family of enzymes involved in xyloglucan endotrans-glucosylase and endohydrolysis, current perspectives and new unifying nomenclature. Plant Cell Physiol. 43: 1421–1435.
Samuels, A.L., Giddings, T.H. Jr. and Staehelin, A.L 1995. Cytokinesis in Tobacco BY-2 and Root Tip Cells: A new model of cell plate formation in higher plants. J. Cell. Biol. 130: 1345–1357.
Sampedro, J., Sieiro, C., Revilla, G., Gonzøaez-Villa, T. and Zarra, I. 2001. Cloning and expression pattern of a gene encoding an α-xylosidase active against xyloglucan oligosaccharides from Arabidopsis. Plant Physiol. 126: 910–920.
Sander, L., Child, R., Ulvskov, P., Albrechtsen, M. and Borkhardt, B. 2001. Analysis of dehiscence zone endopolygalacturonase in oil seed rape (Brassica napus) and Arabidopsis thaliana: evidence for roles in cell separation in dehiscence and abscission zones, and in stylar tissues during pollen tube growth. Plant Mol. Biol. 46: 469–479.
Sarria, R., Wagner, T.A., O’Neill, M.A., Faik, A., Wilkerson, C.G., Keegstra, K. and Raikhel, N.V. 2001. Characterization of a family of Arabidopsis genes related to xyloglucan fucosyltransferase 1. Plant Physiol 127: 1595–1606.
Schultz, C.J., Johnson, K.L., Currie, G. and Bacic, A. 2000. The Classical arabinogalactan protein gene family of Arabidopsis. Plant Cell 12: 1751–1768.
Schultz, C.J., Rumsewicz, M.P., Johnson, K.L., Jones, B.J., Gaspar, Y.M. and Basic, A. 2002. Using genomic resources to guide research directions: The arabinogalactan protein gene family as a test case. Plant Physiol. 129: 1448–1463.
Shani, Z., Dekel, M., Tsabary, G. and Shoseyov, O. 1997. Cloning and characterization of elongation specific endo-1,4-β-glucanase (cel1) from Arabidopsis thaliana. Plant Mol. Biol. 34: 837–842.
Taylor, N.G., Scheible, W.R., Cutler, S., Somerville, C.R. and Turner, S.R. 1999. The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11: 769–780.
Taylor, N.G., Laurie, S. and Turner, S.R. 2000. Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12: 2529–2540.
Taylor, N.G., Howells, R.M., Huttly, A.K., Vickers, K. and Turner, S.R. 2003. Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc. Natl. Acad. Sci. USA 100: 1450–1455.
Tsukaya, H., Osguma, T., Naito, S., Chino, M. and Komeda, Y. 1991. Sugar-dependent expression of the CHS-A gene for chalcone synthase from Petunia in transgenic Arabidopsis.. Plant Physiol 97: 1414–1421.
Vissenberg, K., Oyama, M., Osato, Y., Yokoyama, R., Verbelen, J-P and Nishitani, K. 2005. Differential expression of AtXTH17, -18, -19 and -20 genes in Arabidopsis roots. Physiological roles in specification in cell wall construction. Plant Cell Physiol. 46: 192–200.
Wolf, S., Grsic-Rausch, S., Rausch, T. and Greiner, S. 2003. Identification of pollen-expressed pectin methylesterase inhibitors in Arabidopsis. FEBS Lett. 555: 551–555.
Yokoyama, R. and Nishitani, K. 2001a. A comprehensive expression analysis of all members of a gene family encoding cell-wall enzymes allowed us to predict cis-regulatory regions involved in cell-wall construction in specific organs of Arabidopsis. Plant Cell Physiol. 42: 1025–1033.
Yokoyama, R. and Nishitani, K. 2001b. Endoxyloglucan transferase is localized both in the cell plate and in the secretory pathway destined for the apoplast in tobacco cells. Plant Cell Physiol. 42: 292–300.
Yokoyama, R. and Nishitani, K. 2004. Genomic basis for cell-wall diversity in plants. A comparative approach to gene families in rice and Arabidopsis.. Plant Cell Physiol. 45: 1111–1121.
Yokoyama, R., Rose, J.K.C. and Nishitani, K. 2004. A surprising diversity and abundance of XTHs (xyloglucan endotransglucosylase/hydrolases) in rice: classification and expression analysis. Plant Physiol. 134: 1088–1099.
Zhang, Y., Brown, G., Whetten, R., Loopstra, C.A., Neale, D., Kieliszewski, M.J. and Sederoff, R.R 2003. An arabinogalactan protein associated with secondary cell wall formation in, differentiating xylem of loblolly pine. Plant Mol. Biol. 52: 91–102.
Zhong, R.Q., Kays, S.J., Schroeder, B.P. and Ye, Z.H. 2002. Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 14: 165–179.
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Material
Rights and permissions
About this article
Cite this article
Imoto, K., Yokoyama, R. & Nishitani, K. Comprehensive approach to genes involved in cell wall modifications in Arabidopsis thaliana . Plant Mol Biol 58, 177–192 (2005). https://doi.org/10.1007/s11103-005-5344-7
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11103-005-5344-7