Glycosyltransferases of Small Molecules: Their Roles in Plant Biology

Dianna Bowles, University of York, York, UK
Eng‐Kiat Lim, University of York, York, UK

Published online: April 2010

DOI: 10.1002/9780470015902.a0021537

Abstract

Glycosyltransferases are enzymes that transfer sugars from nucleotide sugars to a wide range of small molecule acceptors, from hormones and secondary metabolites to biotic and abiotic chemicals. This alters the hydrophilicity of the acceptors, their stability and chemical properties, their subcellular localization and often their bioactivity. Glycosyltransferases form a large multigene family in the plant kingdom and can be identified by a signature motif in their primary sequence. Considerable progress has been made in understanding the biochemistry of glycosyltransferases and the role of these enzymes in the plant. This article outlines our current knowledge of these enzymes, drawing on information gained from recent in vitro and in planta studies.

Key concepts:

  • There is a class of glycosyltransferases (GTs) that transfers sugars to small molecule acceptors.

  • In plants, these acceptors can be natural products such as hormones and secondary metabolites, as well as nonnatural products, such as herbicides and pesticides.

  • Glycosylation changes the properties of the acceptors, increasing water solubility and leading to transport of glycosides from the cytosol.

  • Glycosylation can also affect activity of the acceptors, both in the plant, such as inactivation of hormones and in industrial applications, such as bioactivity and bioavailability.

Keywords: glycosyltransferases; homeostasis; hormones; secondary metabolites

Figure 1.

(a)–(i) The chemical structures of plant metabolites are shown in these panels, with their glycosylation sites highlighted. (j) The metabolic relatedness of the compounds is illustrated. Reproduced from Bowles et al. . With permission from Annual Reviews, Inc.
Figure 2.

(a)–(i) The chemical structures of plant metabolites are shown in these panels, with their glycosylation sites highlighted. (j) The metabolic relatedness of the compounds is illustrated. Reproduced from Bowles et al. . With permission from Annual Reviews, Inc.
Figure 3.

(a)–(i) The chemical structures of plant metabolites are shown in these panels, with their glycosylation sites highlighted. (j) The metabolic relatedness of the compounds is illustrated. Reproduced from Bowles et al. . With permission from Annual Reviews, Inc.
Figure 4.

Phylogenetic analysis of the Arabidopsis UGT superfamily shows 14 distinct groups. The tree shown was derived by neighbour‐joining distance analysis. Bootstrap values over 50% are indicated above the nodes, with the number on the left for the neighbour‐joining and right for parsimony. Hypothetical intron gains and losses are indicated by diamonds, followed by intron number. Postulated intron gains are indicated by filled diamonds, intron losses by unfilled diamonds and the questionable intron loss by striped diamonds. Reproduced from Bowles et al. . With permission from Annual Reviews, Inc.
Figure 5.

Glycosylation of esculetin by Arabidopsis GTs in phylogenetic group E. The regioselective glycosylation of esculetin falls into two subsets within group E, with the exception of UGT72B1 and UGT72B3, which suggests that a regioselectivity switching event has occurred during the gene's evolution. GTs not analysed are labelled in black.
Figure 6.

Flavonol glycosylation in Arabidopsis.
close

References

Achnine L, Huhman DV, Farag MA et al. (2005) Genomics‐based selection and functional characterization of triterpene glycosyltransferases from the model legume Medicago truncatula. Plant Journal 41: 875–887.

Bartholomew DM, Van Dyk DE, Lau SMC et al. (2002) Alternate energy‐dependent pathways for the vacuolar uptake of glucose and glutathione conjugates. Plant Physiology 130: 1562–1572.

Bouwmeester HJ (2006) Engineering the essence of plants. Nature Biotechnology 24: 1359–1361.

Bowles D, Isayenkova J, Lim EK and Poppenberger B (2005) Glycosyltransferases: managers of small molecules. Current Opinion in Plant Biology 8: 254–263.

Bowles D, Lim EK, Poppenberger B and Vaistij FE (2006) Glycosyltransferases of lipophilic small molecules. Annual Review of Plant Biology 57: 567–597.

Brazier‐Hicks M and Edwards R (2005) Functional importance of the Family 1 glucosyltransferase UGT72B1 in the metabolism of xenobiotics in Arabidopsis thaliana. Plant Journal 42: 556–566.

Brazier‐Hicks M, Offen W, Gershater MC et al. (2007) Characterisation and engineering of the bifunctional N‐ and O‐glucosyltransferase involved in xenobiotic metabolism in plants. Proceedings of the National Academy of Sciences of the USA 104: 20238–20243.

Burbulis IE and Winkel‐Shirley B (1999) Interactions among enzymes of the Arabidopsis flavonoid biosynthetic pathway. Proceedings of the National Academy of Sciences of the USA 96: 12929–12934.

Caputi L, Lim EK and Bowles DJ (2008) Discovery of new biocatalysts for the glycosylation of terpenoid scaffolds. Chemistry, a European Journal 14: 6656–6662.

Dietz KJ, Sauter A, Wichert K, Messdaghi D and Hartung W (2000) Extracellular beta‐glucosidase activity in barley involved in the hydrolysis of ABA glucose conjugate in leaves. Journal of Experimental Botany 51: 937–944.

Eudes A, Bozzo GG, Waller JC et al. (2008) Metabolism of the folate precursor p‐aminobenzoate in plants. Journal of Biological Chemistry 283: 15451–15459.

Hou B, Lim EK, Higgins GS and Bowles DJ (2004) N‐glucosylation of cytokinins by glycosyltransferases of Arabidopsis thaliana. Journal of Biological Chemistry 279: 47822–47832.

Ikan R (1999) Naturally Occurring Glycosides. Chichester, UK: Wiley.

Jackson RG, Kowalczyk M, Li Y et al. (2002) Over‐expression of an Arabidopsis gene encoding a glucosyltransferase of indole‐3‐acetic acid: phenotypic characterisation of transgenic lines. Plant Journal 32: 573–583.

Jones P, Messner B, Nakajima J, Schaffner AR and Saito K (2003) UGT73C6 and UGT78D1, glycosyltransferases involved in flavonol glycoside biosynthesis in Arabidopsis thaliana. Journal of Biological Chemistry 278: 43910–43918.

Jones P and Vogt T (2001) Glycosyltransferases in secondary plant metabolism: tranquilizers and stimulant controllers. Planta 213: 164–174.

Kim JH, Shin KH, Ko JH and Ahn JH (2006) Glucosylation of flavonols by Escherichia coli expressing glucosyltransferase from rice (Oryza sativa). Journal of Bioscience and Bioengineering 102: 135–137.

Lanot A, Hodge D, Jackson RG et al. (2006) The glucosyltransferase UGT72E2 is responsible for monolignol 4‐O‐glucoside production in Arabidopsis thaliana. Plant Journal 48: 286–295.

Li L, Modolo LV, Escamilla‐Trevino LL et al. (2007) Crystal structure of Medicago truncatula UGT85H2 – insights into the structural basis of a multifunctional (iso)flavonoid glycosyltransferase. Journal of Molecular Biology 370: 951–963.

Li Y, Baldauf S, Lim EK and Bowles DJ (2001) Phylogenetic analysis of the UDP‐glycosyltransferase multigene family of Arabidopsis thaliana. Journal of Biological Chemistry 276: 4338–4343.

Lim EK, Ashford DA, Hou B, Jackson RG and Bowles DJ (2004) Arabidopsis glycosyltransferases as biocatalysts in fermentation for regioselective synthesis of diverse quercetin glucosides. Biotechnology and Bioengineering 87: 623–631.

Lim EK, Baldauf S, Li Y et al. (2003) Evolution of substrate recognition across a multigene family of glycosyltransferases in Arabidopsis. Glycobiology 13: 139–145.

Lim EK and Bowles DJ (2004) A class of plant glycosyltransferases involved in cellular homeostasis. EMBO Journal 23: 2915–2922.

Lim EK, Doucet CJ, Hou B et al. (2005a) Resolution of (+)‐abscisic acid using an Arabidopsis glycosyltransferase. Tetrahedron Asymmetry 16: 143–147.

Lim EK, Doucet CJ, Li Y et al. (2002) The activity of Arabidopsis glycosyltransferases toward salicylic acid, 4‐hydroxybenzoic acid, and other benzoates. Journal of Biological Chemistry 277: 586–592.

Lim EK, Jackson RG and Bowles DJ (2005b) Identification and characterisation of Arabidopsis glycosyltransferases capable of glucosylating coniferyl aldehyde and sinapyl aldehyde. FEBS Letters 579: 2802–2806.

Lim EK, Li Y, Parr A et al. (2001) Identification of glucosyltransferase genes involved in sinapate metabolism and lignin synthesis in Arabidopsis. Journal of Biological Chemistry 276: 4344–4349.

Mackenzie PI, Owens IS, Burchell B et al. (1997) The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics 7: 255–269.

Martinoia E, Klein M, Gesser M, Sanchez‐Hernandez R and Rea PA (2001) Vacuolar transport of secondary metabolites and xenobiotics. In: Robinson D and Rogers J (eds) Vacuolar Compartments, pp. 221–253. Sheffield, UK: Sheffield Academy.

Morrissey JP and Osbourn AE (1999) Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiology and Molecular Biology Reviews 63: 708–724.

Offen W, Martinez‐Fleites C, Yang M et al. (2006) Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification. EMBO Journal 25: 1396–1405.

Paquette S, Moller BL and Bak S (2003) On the origin of Family 1 plant glycosyltransferases. Phytochemistry 62: 399–413.

Pflugmacher S and Sandermann H (1998) Taxonomic distribution of plant glucosyltransferases acting on xenobiotics. Phytochemistry 49: 507–511.

Poppenberger B, Fujioka S, Soeno K et al. (2005) The UGT73C5 of Arabidopsis thaliana glucosylates brassinosteroids. Proceedings of the National Academy of Sciences of the USA 102: 15253–15258.

Priest DM, Ambrose SJ, Vaistij FE et al. (2006) Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana. Plant Journal 46: 492–502.

Rask L, Andr′easson E, Ekbom B et al. (2000) Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Molecular Biology 42: 93–113.

Rea PA (1999) MRP subfamily ABC transporters from plants and yeast. Journal of Experimental Botany 50: 895–913.

Ross J, Li Y, Lim E and Bowles DJ (2001) Higher plant glycosyltransferases. Genome Biology 2: 30041–30046.

Samuels AL, Rensing KH, Douglas CJ et al. (2002) Cellular machinery of wood production: differentiation of secondary xylem in Pinus contorta var latifolia. Planta 216: 72–82.

Shao H, He X, Achinine L et al. (2005) Crystal structures of a multifunctional triterpene/flavonoid glycosyltransferase from Medicago truncatula. Plant Cell 17: 3141–3154.

Tohge T, Nishiyama Y, Hirai MY et al. (2005) Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over‐expressing an MYB transcription factor. Plant Journal 42: 218–235.

Vogt T and Jones P (2000) Glycosyltransferases in plant natural product synthesis: characterization of a supergene family. Trends in Plant Science 5: 380–386.

Yonekura‐Sakakibara K, Tohge T, Niida R and Saito K (2007) Identification of a flavonol 7‐O‐rhamnosyltransferase gene determining flavonoid pattern in Arabidopsis by transcriptome coexpression analysis and reverse genetics. Journal of Biological Chemistry 282: 14932–14941.

Further Reading

Dewick PM (1997) Medicinal Natural Products. Chichester, UK: Wiley.

Related Sub-Topics:

Enzymes: Structure and Action Mechanism | Postsynaptic Signalling Mechanisms | Plant Genetics and Molecular Biology
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Glycosyltransferases of Small Molecules: Their Roles in Plant Biology
 
How to Cite close
Bowles, Dianna, and Lim, Eng‐Kiat(Apr 2010) Glycosyltransferases of Small Molecules: Their Roles in Plant Biology. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021537]