Plant Molecular Biology

, Volume 47, Issue 1–2, pp 95–113 | Cite as

Molecular genetics of nucleotide sugar interconversion pathways in plants

  • Wolf-Dieter Reiter
  • Gary F. Vanzin


Nucleotide sugar interconversion pathways represent a series of enzymatic reactions by which plants synthesize activated monosaccharides for the incorporation into cell wall material. Although biochemical aspects of these metabolic pathways are reasonably well understood, the identification and characterization of genes encoding nucleotide sugar interconversion enzymes is still in its infancy. Arabidopsis mutants defective in the activation and interconversion of specific monosaccharides have recently become available, and several genes in these pathways have been cloned and characterized. The sequence determination of the entire Arabidopsis genome offers a unique opportunity to identify candidate genes encoding nucleotide sugar interconversion enzymes via sequence comparisons to bacterial homologues. An evaluation of the Arabidopsis databases suggests that the majority of these enzymes are encoded by small gene families, and that most of these coding regions are transcribed. Although most of the putative proteins are predicted to be soluble, others contain N-terminal extensions encompassing a transmembrane domain. This suggests that some nucleotide sugar interconversion enzymes are targeted to an endomembrane system, such as the Golgi apparatus, where they may co-localize with glycosyltransferases in cell wall synthesis. The functions of the predicted coding regions can most likely be established via reverse genetic approaches and the expression of proteins in heterologous systems. The genetic characterization of nucleotide sugar interconversion enzymes has the potential to understand the regulation of these complex metabolic pathways and to permit the modification of cell wall material by changing the availability of monosaccharide precursors.

Arabidopsis thaliana cell wall genomics monosaccharide mutant 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Altschul, S.F., Madden, T.L., Schäffer, 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.Google Scholar
  2. Amor, Y., Haigler, C.H., Johnson, S., Wainscott, M. and Delmer, D.P. 1995. A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc. Natl. Acad. Sci. USA 92: 9353–9357.Google Scholar
  3. Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.Google Scholar
  4. Barber, G.A. 1979. Observations on the mechanism of the reversible epimerization of GDP-D-mannose to GDP-L-galactose by an enzyme from Chlorella pyrenoidosa. J. Biol. Chem. 254: 7600–7603.Google Scholar
  5. Baskin, T.I., Betzner, A.S., Hoggart, R., Cork, A. and Williamson, R.E. 1992. Root morphology mutants in Arabidopsis thaliana. Aust. J. Plant Physiol. 19: 427–437.Google Scholar
  6. Bastin, D.A. and Reeves, P.R. 1995. Sequence and analysis of the O antigen (rfb) cluster of Echerichia coli O111. Gene 164: 17–23.Google Scholar
  7. Bonin, C.P., Potter, I., Vanzin, G.F. and Reiter, W.-D. 1997. The MUR1 gene of Arabidopsis thaliana encodes an isoform of GDP-D-mannose-4,6-dehydratase, catalyzing the first step in the de novo synthesis of GDP-L-fucose. Proc. Natl. Acad. Sci. USA 94: 2085–2090.Google Scholar
  8. Bonin, C.P. and Reiter, W.-D. 2000. A bifunctional epimerasereductase acts downstream of the MUR1 gene product and completes the de novo synthesis of GDP-L-fucose in Arabidopsis. Plant J. 21: 445–454.Google Scholar
  9. Burget, E.G. and Reiter, W.-D. 1999. The mur4 mutant of Ara-bidopsis is partially defective in the de novo synthesis of uridine diphospho L-arabinose. Plant Physiol. 121: 383–389.Google Scholar
  10. 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.Google Scholar
  11. Chang, S., Duerr, B. and Serif, G. 1988. An epimerasereductase in L-fucose synthesis. J. Biol. Chem. 263: 1693–1697.Google Scholar
  12. Cobbett, C.S., Medd, J.M. and Dolezal, O. 1992. Suppressors of an arabinose-sensitive mutant of Arabidopsis thaliana.Aust.J. Plant Physiol. 19: 367–375.Google Scholar
  13. Conklin, P.L., Pallanca, J.E., Last, R.L. and Smirnoff, N. 1997. L-Ascorbic acid metabolism in the ascorbate-deficient Arabidopsis mutant vtc1. Plant Physiol. 115: 1277–1285.Google Scholar
  14. Conklin, P.L., Norris, S.R., Wheeler, G.L., Williams, E.H., Smirnoff, N. and Last, R.L. 1999. Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. Proc. Natl. Acad. Sci. USA 96: 4198–4203.Google Scholar
  15. Dalessandro, G. and Northcote, D.H. 1977. Possible control sites of polysaccharide synthesis during cell growth and wall expansion of pea seedlings (Pisum sativum L.). Planta 134: 39–44.Google Scholar
  16. Delmer, D.P. and Amor, Y. 1995. Cellulose biosynthesis. Plant Cell 7: 987–1000.Google Scholar
  17. Ding, L. and Zhu, J.-K. 1997. A role for arabinogalactan-proteins in root epidermal cell expansion. Planta 203: 289–294.Google Scholar
  18. Dolezal, O. and Cobbett, C.S. 1991. Arabinose kinase-deficient mutant of Arabidopsis thaliana. Plant Physiol. 96: 1255–1260.Google Scholar
  19. Dörmann, P. and Benning, C. 1996. Functional expression of uridine 5-diphospho-glucose 4-epimerase (EC from Arabidopsis thaliana in Saccharomyces cerevisiae and Escherichia coli. Arch. Biochem. Biophys. 327: 27–34.Google Scholar
  20. Dörmann, P. and Benning, C. 1998. The role of UDP-glucose epimerase in carbohydrate metabolism of Arabidopsis.PlantJ. 13: 641–652.Google Scholar
  21. Feingold, D.S. and Avigad, G. 1980. Sugar nucleotide transformations in plants. In: P.K. Stumpf and E.E. Conn (Eds.) The Biochemistry of Plants: A Comprehensive Treatise, Vol. 3, Academic Press, New York, pp. 101–170Google Scholar
  22. Feingold, D.S. and Barber, G.A. 1990. Nucleotide sugars. In: P.M. Dey and J.B. Harborne (Eds.) Methods in Plant Biochemistry, Vol. 2: Carbohydrates, Academic Press, New York, pp. 39–78.Google Scholar
  23. Fleischer, A., O'Neill, M.A. and Ehwald, R. 1999. The pore size of non-graminaceous plant cell walls is rapidly decreased by borate ester cross-linking of the pectic polysaccharide rhamnogalacturonan II. Plant Physiol. 121: 829–838.Google Scholar
  24. Gibeaut, D.M. 2000. Nucleotide sugars and glycosyltransferases for synthesis of cell wall matrix polysaccharides. Plant Physiol. Biochem. 38: 69–80.Google Scholar
  25. Ginsburg, V. 1961. Studies on the biosynthesis of guanosine diphosphate L-fucose. J. Biol. Chem. 236: 2389–2393.Google Scholar
  26. Hart, D.A. and Kindel, P.K. 1970. Isolation and partial characterization of apiogalacturonans from the cell wall of Lemna minor. Biochem. J. 116: 569–579.Google Scholar
  27. Ishii, T. and Matsunaga, T. 1996. Isolation and characterization of a boron-rhamnogalacturonan-II complex from cell walls of sugar beet pulp. Carbohydrate Res. 284: 1–9.Google Scholar
  28. Ishii, T., Matsunaga, T., Pellerin, P., O'Neill, M.A., Darvill, A. and Albersheim, P. 1999. The plant cell wall polysaccharide rhamnogalacturonan II self-assembles into a covalently cross-linked dimer. J. Biol. Chem. 274: 13098–13104.Google Scholar
  29. Joersbo, M., Pedersen, S.G., Nielsen, J.E., Marcussen, J. and Brunstedt, J. 1999. Isolation and expression of two cDNA clones encoding UDP-galactose epimerase expressed in developing seeds of the endospermous legume guar. Plant Sci. 142: 147–154.Google Scholar
  30. John, K.V., Schutzbach, J.S. and Ankel, H. 1977. Separation and allosteric properties of two forms of UDP-glucuronate carboxylyase. J. Biol. Chem. 252: 8013–8017.Google Scholar
  31. Joyard, J., Teyssier, E., Miège, C., Berny-Seigneurin, D., Maréchal, E., Block, M.A., Dorne, A.-J., Rolland, N., Ajlani, G. and Douce, R. 1998. The biochemical machinery of plastid envelope membranes. Plant Physiol. 118: 715–723.Google Scholar
  32. Kaplan, C.P., Tugal, H.B. and Baker, A. 1997. Isolation of a cDNA encoding an Arabidopsis galactokinase by functional expression in yeast. Plant Mol. Biol. 34: 497–506.Google Scholar
  33. Keller, R., Springer, F., Renz, A. and Kossmann, J. 1999. Antisense inhibition of the GDP-mannose pyrophosphorylase reduces the ascorbate content in transgenic plants leading to developmental changes during senescence. Plant J. 19: 131–141.Google Scholar
  34. Kindel, P.K. and Watson, R.R. 1973. Synthesis, characterization and properties of uridine 5′-(α-D-apio-D-furanosyl pyrophosphate). Biochem. J. 133: 227–241.Google Scholar
  35. Kobayashi, M., Matoh, T. and Azuma, J. 1996. Two chains of rhamnogalacturonan II are crosslinked by borate-diol ester bonds in higher plant cell walls. Plant Physiol. 110: 1017–1020.Google Scholar
  36. Lake, M.R., Williamson, C.L. and Slocum, R.D. 1998. Molecular cloning and characterization of a UDP-glucose-4-epimerase gene (galE) and its expression in pea tissues. Plant Physiol. Biochem. 36: 555–562.Google Scholar
  37. Levy, S., York, W.S., Stuike-Prill, R., Meyer, B. and Staehelin, L.A. 1991. Simulations of the static and dynamic molecular conformations of xyloglucan. The role of the fucosylated sidechain in surface-specific sidechain folding. Plant J. 1: 195–215.Google Scholar
  38. Levy, S., Maclachlan, G. and Staehelin, L.A. 1997. Xyloglucan sidechains modulate binding to cellulose during in vitro binding assays as predicted by conformational dynamics simulations. Plant J. 11: 373–386.Google Scholar
  39. Liao, T.-H. and Barber, G.A. 1971. The synthesis of guanosine-5-diphosphate L-fucose by enzymes of a higher plant. Biochim. Biophys. Acta 230: 64–71.Google Scholar
  40. Liljebjelke, K., Adolphson, R., Baker, K., Doong, R.L. and Mohnen, D. 1995. Enzymatic synthesis and purification of uri dine diphosphate [14C]galacturonic acid: a substrate for pectin biosynthesis. Anal. Biochem. 225: 296–304.Google Scholar
  41. Loewus, F., Chen, M.-S. and Loewus, M.W. 1973. The myo-inositol oxidation pathway to cell wall polysaccharides. In: F. Loewus (Ed.) Biogenesis of Plant Cell Wall Polysaccharides, Academic Press, New York, pp. 1–27.Google Scholar
  42. Lukowitz, W., Nickle, T.C., Meinke, D.W., Last, R.L., Conklin, P.L. and Somerville, C.R. 2001.Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis. Proc. Natl. Acad. Sci. USA 98: 2262–2267.Google Scholar
  43. Maitra, U.S. and Ankel, H. 1971. Uridine diphosphate-4-keto-glucose, an intermediate in the uridine diphosphate-galactose 4-epimerase reaction. Proc. Natl. Acad. Sci. USA 68: 2660–2663.Google Scholar
  44. Maretzki, A. and Thom, M. 1978. Characteristics of a galactoseadapted sugarcane cell line grown in suspension culture. Plant Physiol. 61: 544–548.Google Scholar
  45. Matern, U. and Grisebach, H. 1977. DP-apiose/UDP-xylose synthase. Eur. J. Biochem. 74: 303–312.Google Scholar
  46. McDougall, G.J. and Fry, S.C. 1989. Structure-activity relationships for xyloglucan oligosaccharides with antiauxin activity. Plant Physiol. 89: 883–887.Google Scholar
  47. Mohnen, D. 1999. Biosynthesis of pectins and galactomannans. In: B.M. Pinto (Ed.) Comprehensive Natural Products Chemistry, Vol. 3: Carbohydrates and Their Derivatives Including Tannins, Cellulose, and Related Lignins, Elsevier, Amsterdam, pp. 497–527.Google Scholar
  48. Muños, P., Norambuena, L. and Orellana, A. 1996. Evidence for a UDP-glucose transporter in Golgi apparatus-derived vesicles from pea and its possible role in polysaccharide biosynthesis. Plant Physiol. 112: 1585–1594.Google Scholar
  49. Muños, R., Lópex, R., de Frutos, M. and García, E. 1999. First molecular characterization of a uridine diphosphate galacturonate 4-epimerase: an enzyme required for capsular biosynthesis in Streptococcus pneumoniae type 1. Mol. Microbiol. 31: 703–713.Google Scholar
  50. Nickle, T.C. and Meinke, D.W. 1998. A cytokinesisdefective mutant of Arabidopsis (cyt1) characterized by embryonic lethality, incomplete cell walls, and excessive callose accumulation. Plant J. 15: 321–332.Google Scholar
  51. O'Neill, M.A., Warrenfeltz, D., Kates, K., Pellerin, P., Doco, T., Darvill, A.G. and Albersheim, P. 1996. Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cell, forms a dimer that is covalently cross-linked by a borate ester. J. Biol. Chem. 271: 22923–22930.Google Scholar
  52. Rayon, C., Cabanes-Macheteau, M., Loutelier-Bourhis, C., Salliot-Maire, I., Lemoine, J., Reiter, W.-D., Lerouge, P. and Faye, L. 1999. Characterization of N-glycans from Arabidopsis thaliana. Application to a fucose-deficient mutant. Plant Physiol. 119: 725–733.Google Scholar
  53. Reeves, P.R., Hobbs, M., Valvano, M.A., Skurnik, M., Whitfield, C., Coplin, D., Kido, N., Klena, J., Maskell, D., Raetz, C.R.H. and Rick, P.D. 1996. Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol. 4: 495–503.Google Scholar
  54. Reiter, W.-D., Chapple, C.C.S. and Somerville, C.R. 1993. Altered growth and cell walls in a fucose-deficient mutant of Arabidopsis. Science 261: 1032–1035.Google Scholar
  55. Reiter, W.-D., Chapple, C. and Somerville, C.R. 1997. Mutants of Arabidopsis thaliana with altered cell wall polysaccharide composition. Plant J. 12: 335–345.Google Scholar
  56. Reiter, W.-D. 1998. The molecular analysis of cell wall components. Trends Plant Sci. 3: 27–32.Google Scholar
  57. Salo, W.L., Nordin, J.H., Petersen, D.R., Bevill, R.D. and Kirkwood, S. 1968. The specificity of UDP-glucose 4-epimerase from the yeast Saccharomyces fragilis. Biochim. Biophys. Acta 151: 484–492.Google Scholar
  58. von Schaewen, A., Sturm, A., O'Neill, J. and Chrispeels, M.J. 1993. Isolation of a mutant Arabidopsis plant that lacks N-acetyl glucosaminyl transferase I and is unable to synthesize Golgi-modified complex N-linked glycans. Plant Physiol. 102: 1109–1118.Google Scholar
  59. Schiefelbein, J.W. and Somerville, C. 1990. Genetic control of root hair development in Arabidopsis thaliana. Plant Cell 2: 235–243.Google Scholar
  60. Seitz, B., Klos, C., Wurm, M. and Tenhaken, R. 2000. Matrix polysaccharide precursors in Arabidopsis cell walls are synthesized by alternate pathways with organ-specific expression patterns. Plant J. 21: 537–546.Google Scholar
  61. Sherson, S., Gy, I., Medd, J., Schmidt, R., Dean, C., Kreis, M., Lecharny, A. and Cobbett, C. 1999. The arabinose kinase, ARA1, gene of Arabidopsis is a novel member of the galactose kinase gene family. Plant Mol. Biol. 39: 1003–1012.Google Scholar
  62. Smirnoff, N. and Wheeler, G.L. 2000. Ascorbic acid in plants: biosynthesis and function. Crit. Rev. Biochem. Mol. Biol. 35: 291–314.Google Scholar
  63. Stevenson, G., Neal, B., Liu, D., Hobbs, M., Packer, N.H., Batley, M., Redmond, J.W., Lindquist, L. and Reeves, P. 1994. Structure of the O antigen of Escherichia coli K-12 and the sequence of its rfb gene cluster. J. Bact. 176: 4144–4156.Google Scholar
  64. Tenhaken, R. and Thulke, O. 1996. Cloning of an enzyme that synthesizes a key nucleotide sugar precursor of hemicellulose biosynthesis from soybean: UDP-glucose dehydrogenase. Plant Physiol. 112: 1127–1134.Google Scholar
  65. Wellmann, E. and Grisebach, H. 1971. Purification and properties of an enzyme preparation from Lemna minor L. catalyzing the synthesis of UDP-apiose and UDP/-D-xylose from UDP-D-glucuronic acid. Biochim. Biophys. Acta 235: 389–397.Google Scholar
  66. Wheeler, G.L., Jones, M.A. and Smirnoff, N. 1998. The biosynthetic pathway of vitamin C in higher plants. Nature 393: 365–369.Google Scholar
  67. Willats, W.G.T. and Knox, J.P. 1996. A role for arabinogalactanproteins in plant cell expansion: evidence from studies on the interaction of β-glucosyl Yariv reagent with seedlings of Arabidopsis thaliana. Plant J. 9: 919–925.Google Scholar
  68. Wilson, D.B. and Hogness, D.S. 1964. The enzymes of the galactose operon in Escherichia coli. I. Purification and characterization of uridine diphosphogalactose 4-epimerase. J. Biol. Chem. 239: 2469–2481.Google Scholar
  69. Yamamoto, R., Inouhe, M. and Masuda, Y. 1988. Galactose inhibition of auxin-induced growth of mono-and dicotyledonous plants. Plant Physiol. 86: 1223–1227.Google Scholar
  70. Yariv, J., Rapport, M.M. and Graf, L. 1962. The interaction of glycosides and saccharides with antibody to the corresponding phenylazo glycosides. Biochem. J. 85: 383–388.Google Scholar
  71. York, W.S., Darvill, A.G. and Albersheim, P. 1984. Inhibition of 2,4-dichlorophenoxyacetic acid-stimulated elongation of pea stem segments by a xyloglucan oligosaccharide. Plant Physiol. 75: 295–297.Google Scholar
  72. Zablackis, E., York, W.S., Pauly, M., Hantus, S., Reiter, W.-D., Chapple, C.C.S., Albersheim, P. and Darvill, A. 1996. Substitution of L-fucose by L-galactose in cell walls of Arabidopsis mur1. Science 272: 1808–1810.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Wolf-Dieter Reiter
    • 1
  • Gary F. Vanzin
    • 1
  1. 1.Department of Molecular and Cell BiologyUniversity of ConnecticutStorrsUSA

Personalised recommendations