Abstract
The synthesis, modification, and breakdown of carbohydrates is one of the most fundarnentally important reactions in nature. The structural and functional diversity of glycosides is mirrored by a vast array of enzymes involved in their synthesis (glycosyltransferases), modification (carbohydrate esterases ) and breakdown (glycoside hydrolases and polysaccharide lyases). The importance of these processes is reflected in the dedication of 1–2% of an organism’s genes to glycoside hydrolases and glycosyltransferases alone. In plants, these processes are of particular importance for cell-wall synthesis and expansion, starch metabolism, defence against pathogens, symbiosis and signalling. Here we present an analysis of over 730 open reading frarnes representing the two main c1asses of carbohydrate-active enzymes, glycoside hydrolases and glycosyltransferases, in the genome of Arabidopsis thaliana. The vast importance of these enzymes in cell-wall formation and degradation is revealed along with the unexpected dominance of pectin degradation in Arabidopsis, with at least 170 open-reading frarnes dedicated solely to this task.
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References
Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.
Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25: 3389–3402.
Aoki, S. and Syno, K. 1999. Horizontal gene transfer and mutation: ngrol genes in the genome of Nicotiana glauca. Proc. Natl. Acad. Sci. USA 96: 13229–13234.
Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence ofthe fiowering plant Arabidopsis thaliana. Nature 408: 796–815.
Benhamou, N. 1995. Immunocytochernistry ofplant defense mechanisms induced upon microbial attack. Microsc. Res. Tech. 31: 63–78.
Bishop, J.G., Dean, A.M. and Mitchell-Olds, T. 2000. Rapid evolution in plant chitinases: molecular targets of selection in plant-pathogen coevolution. Proc. Natl. Acad. Sci. USA 97: 5322–5327.
Burmeister, W.P., Cottaz, S., Rollin, P., Vasella, A. and Henrissat, B. 2000. High resolution X-ray crystallography shows that ascorbate is a cofactor for myrosinase and substitutes for the function of the catalytic base. J. Biol. Chem. 275: 39385–39393.
Callebaut, I., Labesse, G., Durand, P., Poupon, A., Canard, L., Chomilier, J., Henrissat, B. and Mornon, J.P. 1997. Deciphering protein sequence information tbrough hydrophobic cluster analysis (HCA): current status and perspectives. Cell. Mol. Life Sci. 53: 621–645.
Campbell, J.A., Davies, G.J., Bulone, V. and Henrissat, B. 1997. A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. Biochem. J. 326: 929–939.
Campbell, P. and Braam, J. 1999. In vitro activities of four xyloglucan endotransglycosylases from Arabidopsis. Plant J. 18: 371–382.
Charnock, S.J., Bolam, D.N., Turkenburg, J.P., Gilbert, H.J., Ferreira, L.M., Davies, G.J. and Fontes, C.M. 2000. The X6’ thennostabilizing’ domains of xylanases are carbohydrate-binding modules: structure and biochernistry of the Clostridium thermocellum X6b domain. Biochemistry 39: 5013–5021.
Charnock, S.J. and Davies, G.J. 1999. Structure of the nucleotide-diphospho-sugar transferase, SpsA from Bacillus subtilis, in native and nucleotide-complexed fonns. Biochemistry 38: 6380–6385.
Charnock, S.J., Henrissat, B. and Davies, G. 2001. Three-dimensional structures of UDP-sugar glycosyltransferases illurninate the biosynthesis of plant polysaccharides. Plant Physiol. 125: 527–531.
Cicek, M., Blanchard, D., Bevan, D.R. and Esen, A. 2000. The aglycone specificity-deterrnining sites are different in 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA)-glucosidase (maize β-glucosidase) and dhurrinase (sorghum β-glucosidase). J. Biol. Chem. 275: 20002–20011.
Coughlan, M.P. and Hazlewood, G.P. 1993. β-1,4-D-xylandegrading enzyme systems: biochernistry, molecular biology and applications. Biotechnol. Appl. Biochem. 17: 259–289.
Coutinho, P. and Henrissat, B. 1999a. Carbohydrate-active enzymes: an integrated database approach. In: H. Gilbert, G. Davies, B. Henrissat and B. Svensson (Eds.) Recent Advances in Carbohydrate Bioengineering, Royal Society of Chemistry, Cambridge, UK, pp. 3–12.
Coutinho, P.M. and Henrissat, B. 1999b. Life with no sugars? J. Mol. Microbiol. Biotechnol. 1: 307–308.
Cui, X., Shin, H., Charlotte Song, C., Laosinchail, W., Amano, Y. and Brown, R.M. Jr. 2001. A putative plant homolog of the yeast β-1,3-glucan synthase subunit FKSI from cotton (Gossypium hirsutum L.) fibers. Planta, in press.
Davies, G. and Henrissat, B. 1995. Structures and mechanisms of glycosyl hydrolases. Structure 3: 853–859.
Davies, G.J. 1998. Structural studies on cellulases. Biochem. Soc. Transact. 26: 167–173.
Dejardin, A, Sokolov, L.N. and Kleczkowski, L.A 1999. Sugar/osmoticum levels modulate differential abscisic acidindependent expression of two stress-responsive sucrose synthase genes in Arabidopsis. Biochem. J. 344: 503–509.
Dijkwel, P.P., Huijser, C., Weisbeek, P.J., Chua, N.H. and Smeekens, S.C. 1997. Sucrose control of phytochrome A signaling in Arabidopsis. Plant Cell 9: 583–595.
Doblin, M.S., De Melis, L., Newbigin, E., Bacic, A and Read, S.M. 2001. Pollen tubes of Nicotiana alata express two genes from different β-glucan synthase families. Plant Physiol., in press.
Dolan, L., Linstead, P. and Roberts, K. 1997. Developmental regulation of pectic polysaccharides in the root meristem of Arabidopsis. J. Exp. Bot. 48: 713–720.
Dönnann, P., Balbo, I. and Benning, C. 1999. Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD 1. Science 284: 2181–2184.
Garcia-Vallvé, S., Romeu, A. and Palau, J. 2000. Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol. Biol. Evol. 17: 352–361.
Gastinei, L.N., Cambillau, C. and Boume, Y. 1999. Crystal structures of the bovine β4galactosyltransferase catalytic domain and its complex with uridine diphosphogalactose. EMBO J. 18: 3546–3557.
Gebier, J., Gilkes, N.R, Claeyssens, M., Wilson, D.B., Beguin, P., Wakarchuk, W.W., Kilbum, D.G., Miller, R.C. Jr., Warren, R.A. and Withers, S.G. 1992. Stereoselective hydrolysis catalyzed by related β-1,4-glucanases and β-1,4-xylanases. J. Biol. Chem. 267: 12559–12561.
Ha, S., Walker, D., Shi, Y. and Walker, S. 2000. The 1.9 A crystal structure of Eseheriehia coli MurG, a membrane-associated glycosyltransferase involved in peptidoglycan biosynthesis. Protein Sci. 9: 1045–1052.
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.
Henrissat, B. and Davies, G. 1997. Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7: 637–644.
Henrissat, B. and Davies, G. 2000. Glycoside hydrolases and glycosyltransferases: families, modules and implications for genomics. Plant Physiol. 124: 1515–1520.
Hong, Z., Delauney, A.I. and Verma, D.P.S. 2001. A cell plate-specific callose synthase and its interaction with phragmoplastin. Plant Cell, in press.
Hrmova, H. and Fincher, G.B. 2001. Three-dimensional structures, substrate specificities and biological functions of β-D-glucan endo-and exohydrolases from higher plants. Plant Mol. Biol., this issue.
Jin, W., Homer, H.T., Palmer, R.G. and Shoemaker, R.C. 1999. Analysis and mapping of gene families encoding β-1,3-glucanases of soybean. Genetics 153: 445–452.
Kaiser, J. 2000. From genome to functional genomics. Science 288: 1715.
Kottom, T.J. and Limper, A.H. 2000. Cell wall assembly by Pneumocystis carinii: evidence for a unique Gsc-I subunit mediating β-1,3-glucan deposition. J. Biol. Chem. 275: 40628–40634.
Kraulis, P.J. 1991. Moiscript: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24: 946–950.
Lerouge, P., Cabanes-Macheteau, M., Rayon, C., Fischette-Laine, A.C., Gomord, V. and Faye, L. 1998. N-glycoprotein biosynthesis in plants: recent developments and future trends. Plant Mol. Biol. 38: 31–48.
Little, E., Bork, P. and Doolittle, R.F. 1994. Tracing the spread of fibronectin type III domains in bacterial glycohydrolases. J. Mol. Evol. 39: 631–643.
McCarter, J.D. and Withers, S.G. 1994. Mechanisms of enzymatic glycoside hydrolysis. Curr. Opin. Struct. Biol. 4: 885–892.
Minton, J.P., Walaszek, Z., Schooley, W., Hanausek-Walaszek M., and Webb, T.E. 1986. β-Glucuronidase levels in patients with fibrocystic breast disease. Breast Cancer Res. Treatm. 8: 217–222.
Mita, S., Murano, N., Akaike, M. and Nakamura, K. 1997. Mutants of Arabidopsis thaliana with pleiotropic effects on the expression of the gene for β-amylase and on the accumulation of anthocyanin that are inducible by sugars. Plant J. 11: 841–851.
Myers, A.M., Morell, M.K., James, M.G. and Ball, S.G. 2000. Recent progress toward understanding biosynthesis of the amylopectin crystal. Plant Physiol. 122: 989–997.
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.
Ochman, H., Lawrence, J.G. and Groisman, E.A. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299–304.
Pedersen, L.C., Tsuchida, K., Kitagawa, H., Sugahara, K., Darden, T.A. and Negishi, M. 2000. Heparan/chondroitin sulfate biosynthesis: structure and mechanism of human glucuronyltransferase I. J. Biol. Chem. 275: 34580–34585.
Perrin, R.M., DeRocher, A.E., Bar-Peled, M., Zeng, W., Norambuena, L., Orellana, A., Raikhel, N.V. and Keegstra, K. 1999. Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis. Science 284: 1976–1979.
Perrin, R., Wilkerson, C. and Keegstra, K. 2001. Golgi enzymes that synthesize plant cell wall polysaccharides: finding and evaluating candidates in the genomic era. Plant Mol. Biol., this issue.
Rask, L., Andreasson, E., Ekbom, B., Eriksson, S., Pontoppidan, B. and Meijer, J. 2000. Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol. Biol. 42: 93–113.
Reymond, P. and Farmer, E.E. 1998. Jasmonate and salicylate as global signals for defense gene expression. Curr. Opin. Plant Biol. 1: 404–411.
Richmond, T.A and Somerville, C.R 2001. Integrative approaches to determining Csl function. Plant Mol. Biol., this issue.
Sears, P. and Wong, C.H. 1998. Enzyme action in glycoprotein synthesis. Cell. Mol. Life Sci. 54: 223–252.
Shimojima, M., Ohta, H., Iwamatsu, A, Masuda, T., Shioi, Y. and Takamiya, K. 1997. Cloning of the gene for monogalactosyl-diacylglycerol synthase and its evolutionary origin. Proc. Natl. Acad. Sci. USA 94: 333–337.
Sinnott, M.L. 1990. Catalytic mechanisms of enzymic glycosyl transfer. Chem. Rev. 90: 1171–1202.
Smant, G., Stokkermans, J.P., Yan, Y., de Boer, J.M., Baum, T.J., Wang, X., Hussey, R.S., Gommers, F.J., Henrissat, B., Davis, E.L., Helder, J., Schots, A and Bakker, J. 1998. Endogenous cellulases in animals: isolation of β-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc. Natl. Acad. Sci. USA 95: 4906–4911.
Spiro, M.D., Ridley, B.L., Eberhard, S., Kates, K.A., Mathieu, Y., O’Neill, M.A., Mohnen, D., Guern, J., Darvill, A. and Albersheim, P. 1998. Biological activity of reducing-end-derivatized oligogalacturonides in tobacco tissue cultures. Plant Physiol. 116: 1289–1298.
Strasser, R., Mucha, J., Mach, L., Altrnann, F., Wilson, I.B., Glossl, J. and Steinkellner, H. 2000. Molecular cloning and functional expression of β-1,2-xylosyltransferase cDNA from Arabidopsis thaliana. FEBS Lett. 472: 105–108.
Strasser, R., Mucha, J., Schwihla, H., Altrnann, F., Glossl, J. and Steinkellner, H. 1999. Molecular cloning and characterization of cDNA coding for β-1,2-N-acetylglucosaminyltransferase I (GlcNAc-TI) from Nicotiana tabaeum. Glycobiology 9: 779–785.
Sturm, A. and Tang, G.Q. 1999. The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci. 4: 401–407.
Tukey, R. and Strassburg, C. 2000. Human UDP-glucuronosyltransferases: metabolism, expression, and disease. Annu. Rev. Pharmacol. Toxicol. 40: 581–616.
Ünligil, U., Zhou, S., Yuwaraj, S., Sarkar, M., Schachter, H. and Rini, J. 2000. X-ray crystal structure of rabbit N-acetylglucosaminyltransferase I: catalytic mechanism and a new protein superfamily. EMBO J. 19: 5269–5280.
Vrielink, A., Ruger, W., Driessen, H.P. and Freemont, P.S. 1994. Crystal structure of the DNA modifying enzyme β-glucosyltransferase in the presence and absence of the substrate uridine diphosphoglucose. EMBO J. 13: 3413–3422.
Wingler, A., Fritzius, T., Wiemken, A., Boller, T. and Aeschbacher, R.A. 2000. Trehalose induces the ADP-glucose pyrophosphorylase gene, ApL3, and starch synthesis in Arabidopsis. Plant Physiol. 124: 105–114.
Zechel, D.L. and Withers, S.G. 2000. Glycosidase mechanisms: anatomy of a finely tuned catalyst. Acc. Chem. Res. 33: 11–18.
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Henrissat, B., Coutinho, P.M., Davies, G.J. (2001). A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana. In: Carpita, N.C., Campbell, M., Tierney, M. (eds) Plant Cell Walls. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-0668-2_4
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DOI: https://doi.org/10.1007/978-94-010-0668-2_4
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