Arabidopsis GUX proteins are glucuronyltransferases responsible for the addition of glucuronic acid side chains onto xylan

Plant and Cell Physiology

Volumn 53, Issue 7, 2012, Pages 1204-1216

  Lee, Chanhui ^a   Teng, Quincy ^b   Zhong, Ruiqin ^a   Ye, Zheng Hua ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Arabidopsis; GlcA; Glucuronyltransferase; Secondary wall; Xylan; Xylan biosynthesis

Indexed keywords

ARABIDOPSIS PROTEIN; CELLULOSE; GLUCURONIC ACID; GLYCOSYLTRANSFERASE; GUX1 PROTEIN, ARABIDOPSIS; GUX2 PROTEIN, ARABIDOPSIS; XYLAN;

ARABIDOPSIS; ARTICLE; CELL LINE; CELL WALL; CHEMISTRY; ENZYME ACTIVATION; ENZYME ASSAY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; MASS SPECTROMETRY; METHODOLOGY; MUTATION; PLANT GENE; REPORTER GENE; TOBACCO; XYLEM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL LINE; CELL WALL; CELLULOSE; ENZYME ACTIVATION; ENZYME ASSAYS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENES, REPORTER; GLUCURONIC ACID; GLYCOSYLTRANSFERASES; MUTATION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TOBACCO; XYLANS; XYLEM;

ARABIDOPSIS; NICOTIANA TABACUM;

EID: 84863909822     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcs064     Document Type: Article

References (41)

1. An, G. (1985) High efficiency transformation of tobacco cells. Plant Physiol. 79: 568-570.
2. Andersson, S.-I., Samuelson, O., Ishihara, M. and Shimizu, K. (1983) Structure of the reducing end-groups in spruce xylan. Carbohydr. Res. 111: 283-288.
3. Bechtold, N. and Bouchez, D. (1994) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. In Gene Transfer to Plants. Edited by Potrykus, I. and Spangenberg, G. pp. 19-23. Springer-Verlag, Berlin.
4. Brown, D.M., Goubet, F., Wong, V.W., Goodacre, R., Stephens, E., Dupree, P. et al. (2007) Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis. Plant J. 52: 1154-1168.
5. Brown, D.M., Wightman, R., Zhang, Z., Gomez, L.D., Atanassov, I., Bukowski, J.P. et al. (2011) Arabidopsis genes IRREGULAR XYLEM (IRX15) and IRX15L encode DUF579-containing proteins that are essential for normal xylan deposition in the secondary cell wall. Plant J. 66: 401-413.
6. Brown, D.M., Zhang, Z., Stephens, E., Dupree, P. and Turner, S.R. (2009) Characterization of IRX10 and IRX10-like reveals an essential role in glucuronoxylan biosynthesis in Arabidopsis. Plant J. 57: 732-746.
7. Burk, D.H., Zhong, R., Morrison, W.H. III and Ye, Z.-H. (2006) Disruption of cortical microtubules by overexpression of green fluorescent protein-tagged a-tubulin 6 causes a marked reduction in cell wall synthesis. J. Integr. Plant Biol. 48: 85-98.
8. Chen, F. and Dixon, R.A. (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat. Biotechnol. 25: 759-761.
9. Doco, T., O'Neill, M.A. and Pellerin, P. (2001) Determination of the neutral and acidic glycosyl-residue compositions of plant polysaccharides by GC-EI-MS analysis of the trimethylsilyl methyl glycoside derivatives. Carbohydr. Polymers 46: 249-259.
10. Harper, A.D. and Bar-Peled, M. (2002) Biosynthesis of UDP-xylose. Cloning and characterization of a novel Arabidopsis gene family, UXS, encoding soluble and putative membrane-bound UDP-glucuronic acid decarboxylase isoforms. Plant Physiol. 130: 2188-2198.
11. Helle, S., Cameron, D., Lam, J., White, B. and Duff, S. (2003) Effect of inhibitory compounds found in biomass hydrolysates on growth and xylose fermentation by a genetically engineered strain of S. cerevisiae. Enzyme Microb. Technol. 33: 786-792.
12. Himmel, M.E., Ding, S.Y., Johnson, D.K., Adney, W.S., Nimlos, M.R., Brady, J.W. et al. (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315: 804-807.
13. Hoebler, C., Barry, J.L., David, A. and Delort-Laval, J. (1989) Rapid acid-hydrolysis of plant cell wall polysaccharides and simplified quantitative determination of their neutral monosaccharides by gas-liquid chromatography. J. Agric. Food Chem. 37: 360-367.
14. Ishii, T. (1997) Structure and functions of feruloylated polysaccharides. Plant Sci. 127: 111-127.
15. Ishikawa, M., Kuroyama, H., Takeuchi, Y. and Tsumuraya, Y. (2000) Characterization of pectin methyltransferase from soybean hypocotyls. Planta 210: 782-791.
16. Johansson, M.H. and Samuelson, O. (1977) Reducing end groups in birch xylan and their alkaline degradation. Wood Sci. Technol. 11: 251-263.
17. Jensen, J.K., Kim, H., Cocuron, J.C., Orler, R., Ralph, J. and Wilkerson, C.G. (2011) The DUF579 domain containing proteins IRX15 and IRX15-L affect xylan synthesis in Arabidopsis. Plant J. 66: 387-400.
18. Kabel, M.A., van den Borne, H., Vincken, J.-P., Voragen, A.G.J. and Schols, H.A. (2007) Structural differences of xylans affect their interaction with cellulose. Carbohydr. Polym. 69: 94-105.
19. Kuroyama, H. and Tsumuraya, Y. (2001) A xylosyltransferase that synthesizes b-(1!4)-xylans in wheat (Triticum aestivum L.) seedlings. Planta 213: 231-240.
20. Lee, C., O'Neill, M.A., Tsumuraya, Y., Darvill, A.G. and Ye, Z.-H. (2007a) The irregular xylem9 mutant is deficient in xylan xylosyltransferase activity. Plant Cell Physiol. 48: 1624-1634.
21. Lee, C., Teng, Q., Huang, W., Zhong, R. and Ye, Z.-H. (2009a) Down-regulation of PoGT47C expression in poplar results in a reduced glucuronoxylan content and an increased wood digestibility by cellulase. Plant Cell Physiol. 50: 1075-1089.
22. Lee, C., Teng, Q., Huang, W., Zhong, R. and Ye, Z.-H. (2009b) The F8H glycosyltransferase is a functional paralog of FRA8 involved in glucuronoxylan biosynthesis in Arabidopsis. Plant Cell Physiol. 50: 812-827.
23. Lee, C., Teng, Q., Huang, W., Zhong, R. and Ye, Z.-H. (2010) The Arabidopsis family GT43 glycosyltransferases form two functionally nonredundant groups essential for the elongation of glucuronoxylan backbone. Plant Physiol. 153: 526-541.
24. Lee, C., Teng, Q., Zhong, R. and Ye, Z.-H. (2011) The four Arabidopsis REDUCED WALL ACETYLATION genes are expressed in secondary wall-containing cells and required for the acetylation of xylan. Plant Cell Physiol. 52: 1289-1301.
25. Lee, C., Zhong, R., Richardson, E.A., Himmelsbach, D.S., McPhail, B.T. and Ye, Z.-H. (2007b) The PARVUS gene is expressed in cells undergoing secondary wall thickening and is essential for glucuronoxylan biosynthesis. Plant Cell Physiol. 48: 1659-1672.
26. Lee, C., Zhong, R. and Ye, Z.-H. (2012a) Arabidopsis family GT43 members are xylan xylosyltransferases required for the elongation of the xylan backbone. Plant Cell Physiol. 53: 135-143.
27. Lee, C., Zhong, R. and Ye, Z.-H. (2012b) Biochemical characterization of xylan xylosyltransferases involved in wood formation in poplar. Plant Signal. Behav. 7: 332-337.
28. Mortimer, J.C., Miles, G.P., Brown, D.M., Zhang, Z., Segura, M.P., Weimar, T. et al. (2010) Absence of branches from xylan in Arabidopsis gux mutants reveals potential for simplification of lignocellulosic biomass. Proc. Natl Acad. Sci. USA 107: 17409-17414.
29. Page, R.D.M. (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12: 357-358.
30. Peña, M.J., Zhong, R., Zhou, G.-K., Richardson, E.A., O'Neill, M.A., Darvill, A.G. et al. (2007) Arabidopsis irregular xylem8 and irregular xylem9: implications for the complexity of glucuronoxylan biosynthesis. Plant Cell 19: 549-563.
31. Persson, S., Caffall, K.H., Freshour, G., Hilley, M.T., Bauer, S., Poindexter, P. et al. (2007) The Arabidopsis irregular xylem8 mutant is deficient in glucuronoxylan and homogalacturonan, which are essential for secondary cell wall integrity. Plant Cell 19: 237-255.
32. Shimizu, K., Ishihara, M. and Ishihara, T. (1976) Hemicellulases of brown rotting fungus, Tyromyces palustris. II. The oligosaccharides from the hydrolysate of a hardwood xylan by the intracellular xylanase. Mokuzai Gaikkashi 22: 618-625.
33. Timell, T.E. (1967) Recent progress in the chemistry of wood hemicelluloses. Wood Sci. Technol. 1: 45-70.
34. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
35. Wu, A.M., Hörnblad, E., Voxeur, A., Gerber, L., Rihouey, C., Lerouge, P. et al. (2010) Analysis of the Arabidopsis IRX9/IRX9-L and IRX14/IRX14-L pairs of glycosyltransferase genes reveals critical contributions to biosynthesis of the hemicellulose glucuronoxylan. Plant Physiol. 153: 542-554.
36. Wu, A.M., Rihouey, C., Seveno, M., Hörnblad, E., Singh, S.K., Matsunaga, T. et al. (2009) The Arabidopsis IRX10 and IRX10-LIKE glycosyltransferases are critical for glucuronoxylan biosynthesis during secondary cell wall formation. Plant J. 57: 718-731.
37. Zhong, R., Demura, T. and Ye, Z.-H. (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18: 3158-3170.
38. Zhong, R., Lee, C. and Ye, Z.-H. (2010) Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Mol. Plant 3: 1087-1103.
39. Zhong, R., Peña, M.J., Zhou, G.-K., Nairn, C.J., Wood-Jones, A., Richardson, E.A. et al. (2005) Arabidopsis Fragile Fiber8, which encodes a putative glucuronyltransferase, is essential for normal secondary wall synthesis. Plant Cell 17: 3390-3408.
40. Zhong, R., Richardson, E.A. and Ye, Z.-H. (2007) Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 225: 1603-1611.
41. Zhong, R., Taylor, J.J. and Ye, Z.-H. (1997) Disruption of interfascicular fiber differentiation in an Arabidopsis mutant. Plant Cell 9: 2159-2170.