Glycosyltransferases in Plant Cell Wall Synthesis

Abstract

Through their influence on plant cell wall polysaccharide structure, plant cell wall glycosyltransferases influence growth, development, cell division and environmental responses as well as plant‐derived food products, biofuels, textiles, paper and timber. Plant cell wall synthesizing enzymes can be processive (glycan synthases) or nonprocessive, and are integral membrane proteins with single or multiple transmembrane domains. Plant cell wall glycosyltransferases can be challenging to study biochemically, as they tend to be labile, present in multimeric complexes and encoded by large gene families whose members may have overlapping function. Candidate proteins may be identified by homology, but their function must be confirmed with biochemical evidence. Strategies for confirmation include expression in heterologous systems followed by assays of enzymatic activity or detection of carbohydrate products. Loss of function or gain‐of‐function techniques may be useful. Despite challenges, numerous plant cell wall glycosyltransferases have been identified; hundreds more, however, await further characterization.

Key concepts

  • Plant cell walls are critical for both biological processes and plant‐derived products, and are formed largely of polysaccharides synthesized by glycosyltransferases.

  • Plant cell wall glycosyltransferases use sugar nucleotides (NDP‐sugars) as donors, and transfer the sugar residue to acceptors to form glycosidic bonds.

  • These enzymes may transfer a single sugar molecule in nonprocessive fashion, or may transfer molecules iteratively to elongate a polymer. Processive glycosyltransferases are termed synthases whereas nonprocessive enzymes are simply termed glycosyltransferases.

  • Cellulose synthesis and callose synthesis occurs at the plasma membrane. All other plant cell wall polymers are synthesized within the Golgi and secreted to the cell wall in vesicles.

  • Nonprocessive glycosyltransferases tend to have a single transmembrane domain, whereas processive glycan synthases tend to have multiple transmembrane domains. There are exceptions to this rule, however.

  • Glycosyltransferases and glycan synthases tend to be highly specific for each donor and acceptor, and are specialized for formation of one type of carbohydrate linkage.

  • Numerous strategies exist for biochemical characterization of glycosyltransferases and glycan synthases, including heterologous expression and use of loss of function and gain‐of‐function genetic methods.

  • Plant cell wall glycosyltransferases and glycan synthases tend to be encoded by genes that are members of large multigene families.

  • Plant cell wall glycosyltransferases and glycan synthases often function in multimeric complexes.

  • Numerous enzymes involved in synthesis of plant cell wall biosynthesis have been identified. These include cellulose synthase, callose synthase, xyloglucan biosynthetic enzymes, pectin biosynthetic enzymes, mixed‐linkage glycan synthase and enzymes synthesizing mannans. However, many hundreds of enzymes remain to be identified at the biochemical level.

Keywords: glycosyltransferase; glycan synthase; plant polysaccharide

Figure 1.

Schematic representation of hypotheses regarding wall polysaccharide biosynthesis. Wall polysaccharides are made in two cellular compartments. Cellulose and callose (not shown) are made at the plasma membrane. (a) Rosettes move in the plane of the membrane, guided by cortical microtubules, producing cellulose microfibrils in the wall that have same orientation as the microtubules in the cytosol. (b) It is thought that each hexameric rosette comprises six rosette subunits, and that each rosette subunit contains six CESA proteins, providing a total of thirty‐six CESA proteins per rosette. Each CESA protein is predicted to span the membrane via eight transmembrane domains, with the N‐terminus, the C‐terminus and the active site facing the cytosol. The growing glucan chain is thought to move through a channel in the membrane to the wall, where it coalesces with other glucan chains to form a microfibril. (c) Matrix polysaccharides are synthesized in the Golgi before deposition into secretory vesicles that deliver them to the cell surface. The backbones of at least some hemicellulosic polysaccharides are synthesized by CSL proteins that show sequence similarity to the CESA proteins. (d) The topology of the CSL proteins is not known, but two possibilities are shown. If the CSL proteins use sugar nucleotides (NDP‐ϒ) present in the Golgi lumen, then the model shown in top part of (d) would apply. If the CSL proteins operate in the same way as the CESA proteins, then the model shown in the lower part of (d), and in an expanded view in (e), would be favored. The glycan synthases are thought to form complexes with glycosyltransferases that add side‐chains to the polymer (bottom part of (d)). Such organization in a complex might be especially important for the synthesis of polysaccharides such as XyG, which has a regular pattern of side‐chain substitution. TMD, transmembrane domain. Reproduced from Lerouxel et al., with permission from Elsevier.

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References

Arioli T, Peng L, Betzner A et al. (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279: 717–720.

Brownfield L, Ford K, Doblin MS et al. (2007) Proteomic and biochemical evidence links the callose synthase in Nicotiana alata pollen tubes to the product of the NaGSL1 gene. Plant Journal 52: 147–156.

Burton RA, Wilson SM, Hrmova M et al. (2006) Cellulose synthase‐like CslF genes mediate the synthesis of cell wall (1,3;1,4)‐beta‐d‐glucans. Science 311: 1940–1942.

Campbell JA, Davies GJ, Bulone V and Henrissat B (1997) A classification of nucleotide‐diphospho‐sugar glycosyltransferases based on amino acid sequence similarities. The Biochemical Journal 326: 929–942.

Carpita NC and Gibeaut D (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of walls during growth. Plant Journal 3: 1–30.

Chapman RL and Staehelin LA (1985) Plasma membrane “rosettes” in carrot and sycamore suspension culture cells. Journal of Ultrastructural Research 93: 87–91.

Cocuron JC, Lerouxel O, Drakakaki G et al. (2007) A gene from the cellulose synthase‐like C family encodes a beta‐1,4 glucan synthase. Proceedings of the National Academy of Sciences of the USA 104: 8550–8555.

Coutinho PM, Deleury E, Davies GJ and Henrissat B (2003) An Evolving Hierarchical Family Classification for Glycosyltransferases. Journal of Molecular Biology 328: 307–317.

Cui X, Shin H, Song C et al. (2001) A putative plant homolog of the yeast beta‐1,3‐glucan synthase subunit FKS1 from cotton (Gossypium hirsutum L.) fibers. Planta 213: 223–230.

Dhugga KS, Barreiro R, Whitten B et al. (2004) Guar seed beta‐mannan synthase is a member of the cellulose synthase super gene family. Science 303: 363–366.

Doblin MS, Kurek I, Jacob‐Wilk D and Delmer DP (2002) Cellulose biosynthesis in higher plants: from genes to rosettes. Plant Cell Physiology 43: 1407–1420.

Edwards M, Choo T, Dickson C et al. (1999) Molecularl characterization of a membrane‐bound galactosyltransferase of plant cell wall matrix polysaccharide biosynthesis. The Plant Journal 19: 691–697.

Egelund J, Petersen BL, Motawia MS et al. (2006) Arabidopsis thaliana RGXT1 and RGXT2 encode Golgi‐localized (1,3)‐alpha‐D‐xylosyltransferases involved in the synthesis of pectic rhamnogalacturonan II. Plant Cell 18: 2593–2607.

Faik A, Price NJ, Raikhel NV and Keegstra K (2002) An Arabidopsis gene encoding an alpha‐xylosyltransferase involved in xyloglucan biosynthesis. Proceedings of the National Academy of Sciences of the USA 99: 7797–7802.

Farrokhi N, Burton RA, Brownfield LN et al. (2006) Plant cell wall biosynthesis: genetic, biochemical, and functional genomics approaches to the identification of key genes. Plant Biotechnology Journal 4: 145–167.

Fry SC, York W, Albersheim P et al. (1993) An unambiguous nomenclature for xyloglucan‐derived oligosaccharides. Physiologia Plantarum 89: 1–3.

Hong Z, Zhang Z, Olson JM and Verma DP (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: 769–779.

Jensen JK, Sørensen SO, Harholt J et al. (2008) Identification of a xylogalacturonan xylosyltransferase involved in pectin biosynthesis in Arabidopsis. Plant Cell 20(5): 1289–1302.

Keegstra K and Walton J (2006) Beta‐glucans – brewer's bane, dietician's delight. Science 311: 1872–1873.

Kurek I, Kawagoe Y, Jacob‐Willk D, Doblin M and Delmer D (2002) Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc‐binding domains. Proceedings of the National Academy of Sciences of the USA 99: 111009–111114.

Leboeuf E, Immerzeel P, Gibon Y, Steup M and Pauly M (2008) High‐throughput functional assessment of polysaccharide‐active enzymes using matrix‐assisted laser desorption/ionization–time‐of‐flight mass spectrometry as exemplified on plant cell wall polysaccharides. Analytical Biochemistry 373: 9–17.

Lerouxel O, Cavalier DM, Liepman AH and Keegstra K (2006) Biosynthesis of plant cell wall polysaccharides – a complex process. Current Opinion in Plant Biology 9: 621–630.

Li J, Burton RA, Harvey AJ et al. (2003) Biochemical evidence linking a putative callose synthase gene with (1,3)‐beta‐d‐glucan biosynthesis in barley. Plant Molecular Biology 53: 213–225.

Liepman A, Wilkerson C and Keegstra K (2005) Expression of cellulose synthase‐like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases. Proceedings of the National Academy of Sciences of the USA 102: 2221–2226.

Madson M, Dunand C, Li X et al. (2003) The MUR3 gene of Arabidopsis encodes a xyloglucan galactosyltransferase that is evolutionarily related to animal exostosins. Plant Cell 15: 1662–1670.

Mohnen D (2008) Pectin structure and biosynthesis. Current Opinion in Plant Biology 11: 266–277.

Pear J, Kawagoe Y, Schreckengost W, Delmer D and Stalker D (1996) Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proceedings of the National Academy of Sciences of the USA 93: 12637–12642.

Perrin RM, Derocher AE, Bar‐Peled M et al. (1999) Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis. Science 284: 1976–1979.

Reiter WD and Vanzin GF (2001) Molecular genetics of nucleotide sugar interconversion pathways in plants. Plant Molecular Biology 47: 95–113.

Richmond TA and Somerville CR (2000) The cellulose synthase superfamily. Plant Physiology 124: 495–498.

Robert S, Bichet A, Grandjean O et al. (2005) An Arabidopsis endo‐1,4‐beta‐d‐glucanase involved in cellulose synthesis undergoes regulated intracellular cycling. Plant Cell 17: 3378–3389.

Robert S, Mouille G and Höfte H (2004) The mechanism and regulation of cellulose synthesis in primary walls: lessons from cellulose‐deficient Arabidopsis mutants. Cellulose 11: 351–364.

Ryden P, Sugimoto‐Shirasu K, Smith AC et al. (2003) Tensile properties of Arabidopsis cell walls depend on both a xyloglucan cross‐linked microfibrillar network and rhamnogalacturonan II‐borate complexes. Plant Physiology 132: 1033–1040.

Saxina IM and Brown RM Jr (2005) Cellulose biosynthesis: current views and evolving concepts. Annals of Botany 96: 9–21.

Seifert GJ (2004) Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside. Current Opinions in Plant Biology 7: 277–284.

Shipp M, Nadella R, Gao H et al. (2008) Glyco‐array technology for efficient monitoring of plant cell wall glycosyltransferase activities. Glycoconjugate Journal 25: 49–58.

Somerville CR (2006) Cellulose synthesis in higher plants. Annual Review of Cell and Developmental Biology 22: 53–78.

Sterling JD, Atmodjo MA, Inwood SE et al. (2006) Functional identification of an Arabidopsis pectin biosynthetic homogalacturonan galacturonosyltransferase. Proceedings of the National Academy of Sciences of the USA 103: 5236–5241.

Taylor NG, Gardiner JC, Whiteman R and Turner SR (2004) Cellulose synthesis in the Arabidopsis secondary cell wall. Cellulose 11: 329–338.

Further Reading

Carpita NC and McCann M (2002) The cell wall. In: Buchanan RB, Gruissem W and Jones RL (eds) Biochemistry and Molecular Biology of Plants. Rockville, MD: American Society of Plant Biologists.

Gabeau DM and Carpita NC (1994) Biosynthesis of plant cell wall polysaccharides. FASEB Journal 8: 904–915.

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 Molecular Biology 47: 115–130.

Somerville C, Bauer S, Brininstool G et al. (2004) Toward a systems approach to understanding plant cell walls. Science 306: 2206–2211.

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How to Cite close
Perrin, Robyn M(Dec 2008) Glycosyltransferases in Plant Cell Wall Synthesis. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020102]