The arabidopsis DUF231 domain-containing protein ESK1 mediates 2-o- and 3-o-acetylation of xylosyl residues in xylan

Plant and Cell Physiology

Volumn 54, Issue 7, 2013, Pages 1186-1199

  Yuan, Youxi ^a   Teng, Quincy ^a   Zhong, Ruiqin ^a   Ye, Zheng Hua ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

Acetylation; Acetyltransferase; Arabidopsis; Secondary wall; Xylan

Indexed keywords

ACYLTRANSFERASE; ARABIDOPSIS PROTEIN; ENDO 1,4 BETA XYLANASE; ESK1 PROTEIN, ARABIDOPSIS; GLYCOSYLTRANSFERASE; OLIGOSACCHARIDE; PHOTOPROTEIN; SND1 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR; UDP XYLOSE PROTEIN XYLOSYLTRANSFERASE; UDP XYLOSE-PROTEIN XYLOSYLTRANSFERASE; XYLAN;

ACETYLATION; ARABIDOPSIS; ARTICLE; BINDING SITE; CELL WALL; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GOLGI COMPLEX; MASS SPECTROMETRY; METABOLISM; MUTATION; PROTOPLAST; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECONDARY WALL; TRANSGENIC PLANT;

ACETYLATION; ACETYLTRANSFERASE; ARABIDOPSIS; SECONDARY WALL; XYLAN;

ACETYLATION; ACETYLTRANSFERASES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; CELL WALL; ENDO-1,4-BETA XYLANASES; GENE EXPRESSION REGULATION, PLANT; GOLGI APPARATUS; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MUTATION; OLIGOSACCHARIDES; PENTOSYLTRANSFERASES; PLANTS, GENETICALLY MODIFIED; PROTOPLASTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRANSCRIPTION FACTORS; XYLANS;

EID: 84880211805     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pct070     Document Type: Article

References (62)

1. Anders, N., Wilkinson, M.D., Lovegrove, A., Freeman, J., Tryfona, T., Pellny, T.K. et al. (2012) Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses. Proc. Natl Acad. Sci. USA 109: 989-993.
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. Bischoff, V., Nita, S., Neumetzler, L., Schindelasch, D., Urbain, A., Eshed, R. et al. (2010) TRICHOME BIREFRINGENCE and its homolog AT5G01360 encode plant-specific DUF231 proteins required for cellulose biosynthesis in Arabidopsis. Plant Physiol. 153: 590-602.
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. Bouchabke-Coussa, O., Quashie, M.L., Seoane-Redondo, J., Fortabat, M.N., Gery, C., Yu, A. et al. (2008) ESKIMO1 is a key gene involved in water economy as well as cold acclimation and salt tolerance. BMC Plant Biol. 8: 125.
8. 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.
9. Carroll, A. and Somerville, C. (2009) Cellulosic biofuels. Annu. Rev. Plant Biol. 60: 165-182.
10. Chen, Z., Hong, X., Zhang, H., Wang, Y., Li, X., Zhu, J.K. et al. (2005) Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. Plant J. 43: 273-283.
11. Curri, A.L. and Timell, T.E. (1959) The constitution of a methyl glucuronoxylan from kapok (Ceiba pentandra). Can. J. Chem. 37: 922-929.
12. Evtuguin, D.V., Tomás, J.L., Silva, A.M. and Neto, C.P. (2003) Characterization of an acetylated heteroxylan from Eucalyptus globulus Labill. Carbohydr. Res. 338: 597-604.
13. Gille, S., de Souza, A., Xiong, G., Benz, M., Cheng, K., Schultink, A. et al. (2011) O-acetylation of Arabidopsis hemicellulose xyloglucan requires AXY4 or AXY4L, proteins with a TBL and DUF231 domain. Plant Cell 23: 4041-4053.
14. Gonçalves, V.M., Evtuguin, D.V. and Domingues, M.R. (2008) Structural characterization of the acetylated heteroxylan from the natural hybrid Paulownia elongata/Paulownia fortunei. Carbohydr. Res. 343: 256-266.
15. 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.
16. 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.
17. 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.
18. Ishikawa, M., Kuroyama, H., Takeuchi, Y. and Tsumuraya, Y. (2000) Characterization of pectin methyltransferase from soybean hypocotyls. Planta 210: 782-791.
19. Janbon, G., Himmelreich, U., Moyrand, F., Improvisi, L. and Dromer, F. (2001) Cas1p is a membrane protein necessary for the O-acetylation of the Cryptococcus neoformans capsular polysaccharide. Mol. Microbiol. 42: 453-467.
20. Johansson, M.H. and Samuelson, O.(1977) Reducing end groupsinbirch xylan and their alkaline degradation. Wood Sci. Technol. 11: 251-263.
21. 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.
22. Keppler, B.D. and Showalter, A.M. (2010) IRX14 and IRX14-LIKE, two glycosyl transferases involved in glucuronoxylan biosynthesis and drought tolerance in Arabidopsis. Mol. Plant 3: 834-841.
23. Kuroyama, H. and Tsumuraya, Y. (2001) A xylosyltransferase that synthesizes b-(1!4)-xylans in wheat (Triticum aestivum L.) seedlings. Planta 213: 231-240.
24. 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.
25. 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.
26. 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.
27. 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 glucuronox-ylan backbone. Plant Physiol. 153: 526-541.
28. Lee, C., Teng, Q., Zhong, R. and Ye, Z.-H. (2011a) Molecular dissection of xylan biosynthesis during wood formation in poplar. Mol. Plant 4: 730-747.
29. Lee, C., Teng, Q., Zhong, R. and Ye, Z.-H. (2011b) 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.
30. Lee, C., Teng, Q., Zhong, R. and Ye, Z.-H. (2012a) Arabidopsis GUX proteins are glucuronyltransferases responsible for the addition of glucuronic acid side chains onto xylan. Plant Cell Physiol. 53: 1204-1216.
31. Lee, C., Teng, Q., Zhong, R., Yuan, Y., Haghighat, M. and Ye, Z.-H. (2012d) Three Arabidopsis DUF579 domain-containing GXM proteins are methyltransferases catalyzing 4-O-methylation of glucur-onic acid on xylan. Plant Cell Physiol. 53: 1934-1949.
32. 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 glucuro-noxylan biosynthesis. Plant Cell Physiol. 48: 1659-1672.
33. Lee, C., Zhong, R. and Ye, Z.-H. (2012b) Arabidopsis family GT43 members are xylan xylosyltransferases required for the elongation of the xylan backbone. Plant Cell Physiol. 53: 135-143.
34. Lee, C., Zhong, R. and Ye, Z.-H. (2012c) Biochemical characterization of xylan xylosyltransferases involved in wood formation in poplar. Plant Signal. Behav. 7: 332-337.
35. Lee, H., Biely, P., Latta, R.K., Barbosa, M.F. and Schneider, H. (1986) Utilization of xylan by yeasts and its conversion to ethanol by Pichia stipitis strains. Appl. Environ. Microbiol. 52: 320-324.
36. Lefebvre, V., Fortabat, M.N., Ducamp, A., North, H.M., Maia-Grondard, A., Trouverie, J. et al. (2011) ESKIMO1 disruption in Arabidopsis alters vascular tissue and impairs water transport. PLoS One 6: e16645.
37. Lugan, R., Niogret, M.F., Kervazo, L., Larher, F.R., Kopka, J. and Bouchereau, A. (2009) Metabolome and water status phenotyping of Arabidopsis under abiotic stress cues reveals new insight into ESK1 function. Plant Cell Environ. 32: 95-108.
38. Marques, G., Gutierrez, A., del Rio, J.C. and Evtuguin, D.V. (2010) Acetylated heteroxylan from Agave sisalana and its behavior in alkaline pulping and TCF/ECF bleaching. Carbohydr. Polymers 81: 517-523.
39. 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.
40. Naran, R., Black, S., Decker, S.R. and Azadi, P. (2009) Extraction and characterization of native heteroxylans from delignified corn stover and aspen. Cellulose 16: 661-675.
41. 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.
42. 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.
43. Potikha, T. and Delmer, D.P. (1995) A mutant of Arabidopsis thaliana displaying altered patterns of cellulose deposition. Plant J. 7: 453-460.
44. Prozil, S.O., Costa, E.V., Evtuguin, D.V., Lopes, L.P. and Domingues, M.R. (2012) Structural characterization of polysaccharides isolated from grape stalks of Vitis vinifera L. Carbohydr. Res. 356: 252-259.
45. Rennie, E.A., Hansen, S.F., Baidoo, E.E., Hadi, M.Z., Keasling, J.D. and Scheller, H.V. (2012) Three members of the Arabidopsis glycosyl-transferase family 8 are xylan glucuronosyltransferases. Plant Physiol. 159: 1408-1417.
46. Scheller, H.V. and Ulvskov, P. (2010) Hemicelluloses. Annu. Rev. Plant Biol. 61: 263-289.
47. Selig, M.J., Adney, W.S., Himmel, M.E. and Decker, S.R. (2009) The impact of cell wall acetylation on corn stover hydrolysis by cellu-lolytic and xylanolytic enzymes. Cellulose 16: 711-722.
48. Sheen, J. (2001) Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiol. 127: 1466-1475.
49. 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 xyla-nase. Mokuzai Gaikkashi 22: 618-625.
50. 13C NMR spectroscopy. Carbohydr. Res. 329: 807-815.
51. Teleman, A., Tenkanen, M., Jacobs, A. and Dahlman, O. (2002) Characterization of O-acetyl-(4-O-methylglucurono)xylan isolated from birch and beech. Carbohydr. Res. 337: 373-377.
52. Teng, Q., Ekman, D.R., Huang, W. and Collette, T.W. (2012) Push-through direct injection NMR: an optimized automation method applied to metabolomics. Analyst 137: 2226-2232.
53. Timell, T.E. (1967) Recent progress in the chemistry of wood hemicel-luloses. Wood Sci. Technol. 1: 45-70.
54. Urbanowicz, B.R., Peña, M.J., Ratnaparkhe, S., Avci, U., Backe, J., Steet, H.F. et al. (2012) 4-O-Methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein. Proc. Natl Acad. Sci. USA 109: 14253-14258.
55. 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.
56. 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.
57. Xin, Z. and Browse, J. (1998) eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc. Natl Acad. Sci. USA 95: 7799-7804.
58. Xin, Z., Mandaokar, A., Chen, J., Last, R.L. and Browse, J. (2007) Arabidopsis ESK1 encodes a novel regulator of freezing tolerance. Plant J. 49: 786-799.
59. 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.
60. 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.
61. 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.
62. Zhong, R., Taylor, J.J. and Ye, Z.-H. (1997) Disruption of interfascicular fiber differentiation in an Arabidopsis mutant. Plant Cell 9: 2159-2170. Biosciences, Office of Basic Energy Sciences of the US Department of Energy