Identification and characterization of a golgi-localized UDP-xylose transporter family from arabidopsis

Plant Cell

Volumn 27, Issue 4, 2015, Pages 1218-1227

  Ebert, Berit ^a,b,c   Rautengarten, Carsten ^a,c   Guo, Xiaoyuan ^b   Xiong, Guangyan ^c,d   Stonebloom, Solomon ^a   Smith Moritz, Andreia M ^a   Herter, Thomas ^a   Chan, Leanne Jade G ^a   Adams, Paul D ^a,e   Petzold, Christopher J ^a   Pauly, Markus ^d   Willats, William G T ^b   Heazlewood, Joshua L ^a,b  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e University of California   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; GLUCOSE TRANSPORTER; URIDINE DIPHOSPHATE XYLOSE;

ARABIDOPSIS; GENETICS; GOLGI COMPLEX; METABOLISM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GOLGI APPARATUS; MONOSACCHARIDE TRANSPORT PROTEINS; URIDINE DIPHOSPHATE XYLOSE;

EID: 84928974889     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.133827     Document Type: Article

References (61)

1. Ashikov, A., Routier, F., Fuhlrott, J., Helmus, Y., Wild, M., Gerardy-Schahn, R., and Bakker, H. (2005). The human solute carrier gene SLC35B4 encodes a bifunctional nucleotide sugar transporter with specificity for UDP-xylose and UDP-N-acetylglucosamine. J. Biol. Chem. 280: 27230–27235.
2. Atmodjo, M.A., Hao, Z., and Mohnen, D. (2013). Evolving views of pectin biosynthesis. Annu. Rev. Plant Biol. 64: 747–779.
3. Bakker, H., Routier, F., Ashikov, A., Neumann, D., Bosch, D., and Gerardy-Schahn, R. (2008). A CMP-sialic acid transporter cloned from Arabidopsis thaliana. Carbohydr. Res. 343: 2148–2152.
4. Bakker, H., Routier, F., Oelmann, S., Jordi, W., Lommen, A., Gerardy-Schahn, R., and Bosch, D. (2005). Molecular cloning of two Arabi-dopsis UDP-galactose transporters by complementation of a deficient Chinese hamster ovary cell line. Glycobiology 15: 193–201.
5. Bakker, H., Oka, T., Ashikov, A., Yadav, A., Berger, M., Rana, N.A., Bai, X., Jigami, Y., Haltiwanger, R.S., Esko, J.D., and Gerardy-Schahn, R. (2009). Functional UDP-xylose transport across the endoplasmic reticulum/Golgi membrane in a Chinese hamster ovary cell mutant defective in UDP-xylose Synthase. J. Biol. Chem. 284: 2576–2583.
6. Baldwin, T.C., Handford, M.G., Yuseff, M.I., Orellana, A., and Dupree, P. (2001). Identification and characterization of GONST1, a Golgi-localized GDP-mannose transporter in Arabidopsis. Plant Cell 13: 2283–2295.
7. Bar-Peled, M., and O’Neill, M.A. (2011). Plant nucleotide sugar formation, interconversion, and salvage by sugar recycling. Annu. Rev. Plant Biol. 62: 127–155.
8. Blake, A.W., McCartney, L., Flint, J.E., Bolam, D.N., Boraston, A.B., Gilbert, H.J., and Knox, J.P. (2006). Understanding the biological rationale for the diversity of cellulose-directed carbohydrate-binding modules in prokaryotic enzymes. J. Biol. Chem. 281: 29321–29329.
9. Bromley, J.R., Busse-Wicher, M., Tryfona, T., Mortimer, J.C., Zhang, Z., Brown, D.M., and Dupree, P. (2013). GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronox-ylan with different substitution patterns. Plant J. 74: 423–434.
10. Chiniquy, D., et al. (2012). XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan. Proc. Natl. Acad. Sci. USA 109: 17117–17122.
11. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and Scheible, W.R. (2005). Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139: 5–17.
12. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K., and Pikaard, C.S. (2006). Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45: 616–629.
13. Ebringerová, A., and Heinze, T. (2000). Xylan and xylan derivatives: biopolymers with valuable properties, 1 Naturally occurring xylans structures, procedures and properties. Macromol. Rapid Commun. 21: 542–556.
14. Egelund, J., Petersen, B.L., Motawia, M.S., Damager, I., Faik, A., Olsen, C.E., Ishii, T., Clausen, H., Ulvskov, P., and Geshi, N. (2006). Arabidopsis thaliana RGXT1 and RGXT2 encode Golgi-lo-calized (1,3)-alpha-D-xylosyltransferases involved in the synthesis of pectic rhamnogalacturonan-II. Plant Cell 18: 2593–2607.
15. Fitchette-lainé, A.C., Gomord, V., Chekkafi, A., and Faye, L. (1994). Distribution of xylosylation and fucosylation in the plant Golgi-apparatus. Plant J. 5: 673–682.
16. Fry, S.C., et al. (1993). An unambiguous nomenclature for xyloglucan-derived oligosaccharides. Physiol. Plant. 89: 1–3.
17. Guillon, F., Tranquet, O., Quillien, L., Utille, J.P., Ortiz, J.J.O., and Saulnier, L. (2004). Generation of polyclonal and monoclonal antibodies against arabinoxylans and their use for immunocytochemi-cal location of arabinoxylans in cell walls of endosperm of wheat. J. Cereal Sci. 40: 167–182.
18. Handford, M., Rodríguez-Furlán, C., Marchant, L., Segura, M., Gómez, D., Alvarez-Buylla, E., Xiong, G.Y., Pauly, M., and Orellana, A. (2012). Arabidopsis thaliana AtUTr7 encodes a golgi-localized UDP-glucose/UDP-galactose transporter that affects lateral root emergence. Mol. Plant 5: 1263–1280.
19. Handford, M.G., Sicilia, F., Brandizzi, F., Chung, J.H., and Dupree, P. (2004). Arabidopsis thaliana expresses multiple Golgi-localised nucleotide-sugar transporters related to GONST1. Mol. Genet. Genomics 272: 397–410.
20. Harholt, J., Jensen, J.K., Sørensen, S.O., Orfila, C., Pauly, M., and Scheller, H.V. (2006). ARABINAN DEFICIENT 1 is a putative ara-binosyltransferase involved in biosynthesis of pectic arabinan in Arabidopsis. Plant Physiol. 140: 49–58.
21. 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.
22. Ito, J., Herter, T., Baidoo, E.E., Lao, J., Vega-Sánchez, M.E., Michelle Smith-Moritz, A., Adams, P.D., Keasling, J.D., Usadel, B., Petzold, C.J., and Heazlewood, J.L. (2014). Analysis of plant nucleotide sugars by hydrophilic interaction liquid chromatography and tandem mass spectrometry. Anal. Biochem. 448: 14–22.
23. Jensen, J.K., Johnson, N.R., and Wilkerson, C.G. (2014). Arabi-dopsis thaliana IRX10 and two related proteins from psyllium and Physcomitrella patens are xylan xylosyltransferases. Plant J. 80: 207–215.
24. Jensen, J.K., et al. (2008). Identification of a xylogalacturonan xylo-syltransferase involved in pectin biosynthesis in Arabidopsis. Plant Cell 20: 1289–1302.
25. Knappe, S., Flügge, U.I., and Fischer, K. (2003). Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site. Plant Physiol. 131: 1178–1190.
26. Koutaniemi, S., Guillon, F., Tranquet, O., Bouchet, B., Tuomainen, P., Virkki, L., Petersen, H.L., Willats, W.G., Saulnier, L., and Tenkanen, M. (2012). Substituent-specific antibody against glu-curonoxylan reveals close association of glucuronic acid and acetyl substituents and distinct labeling patterns in tree species. Planta 236: 739–751.
27. Lamesch, P., et al. (2012). The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 40: D1202–D1210.
28. Lerouxel, O., Choo, T.S., Séveno, M., Usadel, B., Faye, L., Lerouge, P., and Pauly, M. (2002). Rapid structural phenotyping of plant cell wall mutants by enzymatic oligosaccharide fingerprinting. Plant Physiol. 130: 1754–1763.
29. Liepman, A.H., Wightman, R., Geshi, N., Turner, S.R., and Scheller, H.V. (2010). Arabidopsis - a powerful model system for plant cell wall research. Plant J. 61: 1107–1121.
30. Liwanag, A.J., Ebert, B., Verhertbruggen, Y., Rennie, E.A., Rautengarten, C., Oikawa, A., Andersen, M.C., Clausen, M.H., and Scheller, H.V. (2012). Pectin biosynthesis: GALS1 in Arabi-dopsis thaliana is a b-1,4-galactan b-1,4-galactosyltransferase. Plant Cell 24: 5024–5036.
31. MacLean, B., Tomazela, D.M., Shulman, N., Chambers, M., Finney, G.L., Frewen, B., Kern, R., Tabb, D.L., Liebler, D.C., and MacCoss, M.J. (2010). Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bio-informatics 26: 966–968.
32. Major, L.L., Wolucka, B.A., and Naismith, J.H. (2005). Structure and function of GDP-mannose-39,59-epimerase: an enzyme which performs three chemical reactions at the same active site. J. Am. Chem. Soc. 127: 18309–18320.
33. McCartney, L., Marcus, S.E., and Knox, J.P. (2005). Monoclonal antibodies to plant cell wall xylans and arabinoxylans. J. Histochem. Cytochem. 53: 543–546.
34. Mølhøj, M., Verma, R., and Reiter, W.D. (2003). The biosynthesis of the branched-chain sugar d-apiose in plants: functional cloning and characterization of a UDP-d-apiose/UDP-d-xylose synthase from Arabidopsis. Plant J. 35: 693–703.
35. Moller, I., Sørensen, I., Bernal, A.J., Blaukopf, C., Lee, K., Øbro, J., Pettolino, F., Roberts, A., Mikkelsen, J.D., Knox, J.P., Bacic, A., and Willats, W.G. (2007). High-throughput mapping of cell-wall polymers within and between plants using novel microarrays. Plant J. 50: 1118–1128.
36. Mortimer, J.C., et al. (2013). Abnormal glycosphingolipid man-nosylation triggers salicylic acid-mediated responses in Arabi-dopsis. Plant Cell 25: 1881–1894.
37. Nelson, B.K., Cai, X., and Nebenführ, A. (2007). A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51: 1126–1136.
38. Norambuena, L., Marchant, L., Berninsone, P., Hirschberg, C.B., Silva, H., and Orellana, A. (2002). Transport of UDP-galactose in plants. Identification and functional characterization of AtUTr1, an Arabidopsis thaliana UDP-galactos/UDP-glucose transporter. J. Biol. Chem. 277: 32923–32929.
39. Norambuena, L., Nilo, R., Handford, M., Reyes, F., Marchant, L., Meisel, L., and Orellana, A. (2005). AtUTr2 is an Arabidopsis thaliana nucleotide sugar transporter located in the Golgi apparatus capable of transporting UDP-galactose. Planta 222: 521–529.
40. ØBro, J., Harholt, J., Scheller, H.V., and Orfila, C. (2004). Rham-nogalacturonan I in Solanum tuberosum tubers contains complex arabinogalactan structures. Phytochemistry 65: 1429–1438.
41. Oikawa, A., Joshi, H.J., Rennie, E.A., Ebert, B., Manisseri, C., Heazlewood, J.L., and Scheller, H.V. (2010). An integrative approach to the identification of Arabidopsis and rice genes involved in xylan and secondary wall development. PLoS ONE 5: e15481.
42. Pattathil, S., Harper, A.D., and Bar-Peled, M. (2005). Biosynthesis of UDP-xylose: characterization of membrane-bound AtUxs2. Planta 221: 538–548.
43. Pauly, M., Andersen, L.N., Kauppinen, S., Kofod, L.V., York, W.S., Albersheim, P., and Darvill, A. (1999). A xyloglucan-specific endo-b-1,4-glucanase from Aspergillus aculeatus: expression cloning in yeast, purification and characterization of the recombinant enzyme. Glycobiology 9: 93–100.
44. Pedersen, H.L., et al. (2012). Versatile high resolution oligosaccha-ride microarrays for plant glycobiology and cell wall research. J. Biol. Chem. 287: 39429–39438.
45. Rautengarten, C., Ebert, B., Herter, T., Petzold, C.J., Ishii, T., Mukhopadhyay, A., Usadel, B., and Scheller, H.V. (2011). The interconversion of UDP-arabinopyranose and UDP-arabinofuranose is indispensable for plant development in Arabidopsis. Plant Cell 23: 1373–1390.
46. Rautengarten, C., Ebert, B., Ouellet, M., Nafisi, M., Baidoo, E.E., Benke, P., Stranne, M., Mukhopadhyay, A., Keasling, J.D., Sakuragi, Y., and Scheller, H.V. (2012). Arabidopsis Deficient in Cutin Ferulate encodes a transferase required for feruloylation of v-hydroxy fatty acids in cutin polyester. Plant Physiol. 158: 654–665.
47. Rautengarten, C., et al. (2014). The Golgi localized bifunctional UDP-rhamnose/UDP-galactose transporter family of Arabidopsis. Proc. Natl. Acad. Sci. USA 111: 11563–11568.
48. Rennie, E.A., and Scheller, H.V. (2014). Xylan biosynthesis. Curr. Opin. Biotechnol. 26: 100–107.
49. Rollwitz, I., Santaella, M., Hille, D., Flügge, U.I., and Fischer, K. (2006). Characterization of AtNST-KT1, a novel UDP-galactose transporter from Arabidopsis thaliana. FEBS Lett. 580: 4246–4251.
50. Scheible, W.R., and Pauly, M. (2004). Glycosyltransferases and cell wall biosynthesis: novel players and insights. Curr. Opin. Plant Biol. 7: 285–295.
51. Scheller, H.V., and Ulvskov, P. (2010). Hemicelluloses. Annu. Rev. Plant Biol. 61: 263–289.
52. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Schölkopf, B., Weigel, D., and Lohmann, J.U. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37: 501–506.
53. Schmittgen, T.D., and Livak, K.J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3: 1101–1108.
54. Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J.D., and Higgins, D.G. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7: 539.
55. St John, F.J., Rice, J.D., and Preston, J.F. (2006). Characterization of XynC from Bacillus subtilis subsp. subtilis strain 168 and analysis of its role in depolymerization of glucuronoxylan. J. Bacteriol. 188: 8617–8626.
56. Strasser, R., Mucha, J., Mach, L., Altmann, F., Wilson, I.B., Glössl, J., and Steinkellner, H. (2000). Molecular cloning and functional expression of b1, 2-xylosyltransferase cDNA from Arabidopsis thaliana. FEBS Lett. 472: 105–108.
57. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30: 2725–2729.
58. Tan, L., et al. (2013). An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein. Plant Cell 25: 270–287.
59. Urbanowicz, B.R., Peña, M.J., Moniz, H.A., Moremen, K.W., and York, W.S. (2014). Two Arabidopsis proteins synthesize acetylated xylan in vitro. Plant J. 80: 197–206.
60. York, W.S., and O’Neill, M.A. (2008). Biochemical control of xylan biosynthesis - which end is up? Curr. Opin. Plant Biol. 11: 258–265.
61. Zhang, B., Liu, X., Qian, Q., Liu, L., Dong, G., Xiong, G., Zeng, D., and Zhou, Y. (2011). Golgi nucleotide sugar transporter modulates cell wall biosynthesis and plant growth in rice. Proc. Natl. Acad. Sci. USA 108: 5110–5115.