Xyloglucan xylosyltransferases XXT1, XXT2, and XXT5 and the glucan synthase CSLC4 form Golgi-localized multiprotein complexes

Plant Physiology

Volumn 159, Issue 4, 2012, Pages 1355-1366

  Chou, Yi Hsiang ^a   Pogorelko, Gennady ^a   Zabotina, Olga A ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84864665675     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.199356     Document Type: Article

References (46)

1. Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A (2010) Plant Cell Walls. Garland Science, New York
2. Atmodjo MA, Sakuragi Y, Zhu X, Burrell AJ, Mohanty SS, Atwood JA III, Orlando R, Scheller HV, Mohnen D (2011) Galacturonosyl-transferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan:galacturonosyltransferase complex. Proc Natl Acad Sci USA 108: 20225-20230
3. Carpita NC (2011) Update on mechanisms of plant cell wall biosynthesis: how plants make cellulose and other (1→4)-b-D-glycans. Plant Physiol 155: 171-184
4. Cavalier DM, Keegstra K (2006) Two xyloglucan xylosyltransferases catalyze the addition of multiple xylosyl residues to cellohexaose. J Biol Chem 281: 34197-34207
5. Cavalier DM, Keegstra K (2010) Members of Arabidopsis cellulose synthase-like C (CSLC) family are involved in xyloglucan biosynthesis. In S Coimbra, LG Per-eira, eds, Abstract Book: XII Cell Wall Meeting, Porto-Portugal, July 25-30. In-vulgar, Penafiel, Portugal, p 84
6. Cavalier DM, Lerouxel O, Neumetzler L, Yamauchi K, Reinecke A, Freshour G, Zabotina OA, Hahn MG, Burgert I, Pauly M, et al (2008) Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xy-loglucan, a major primary cell wall component. Plant Cell 20: 1519-1537
7. Charnock SJ, Henrissat B, Davies GJ (2001) Three-dimensional structures of UDP-sugar glycosyltransferases illuminate the biosynthesis of plant polysaccharides. Plant Physiol 125: 527-531
8. Citovsky V, Gafni Y, Tzfira T (2008) Localizing protein-protein interactions by bimolecular fluorescence complementation in planta. Methods 45: 196-206
9. Cocuron J-C, Lerouxel O, Drakakaki G, Alonso AP, Liepman AH, Keegstra K, Raikhel NV, Wilkerson CG (2007) A gene from the cellulose synthase-like C family encodes a b-1,4 glucan synthase. Proc Natl Acad Sci USA 104: 8550-8555
10. Davis J, Brandizzi F, Liepman AH, Keegstra K (2010) Arabidopsis mannan synthase CSLA9 and glucan synthase CSLC4 have opposite orientations in the Golgi membrane. Plant J 64: 1028-1037
11. Desprez T, Juraniec M, Crowell EF, Jouy H, Pochylova Z, Parcy F, Höfte H, Gonneau M, Vernhettes S (2007) Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 104: 15572-15577
12. Doblin MS, Kurek I, Jacob-Wilk D, Delmer DP (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol 43: 1407-1420
13. Fry SC, York WS, Albersheim P, Darvill A, Hayashi T, Joseleau J-P, Kato Y, Lorences EP, Maclachlan GA, McNeil M, et al (1993) An unambiguous nomenclature for xyloglucan derived oligosaccharides. Physiol Plant 89: 1-3
14. Harholt J, Jensen JK, Verhertbruggen Y, Søgaard C, Bernard S, Nafisi M, Poulsen CP, Geshi N, Sakuragi Y, Driouich A, et al (2012) ARAD proteins associated with pectic arabinan biosynthesis form complexes when transiently overexpressed in planta. Planta 236: 115-128
15. Hassinen A, Rivinoja A, Kauppila A, Kellokumpu S (2010) Golgi N-glycosyltransferases form both homo- and heterodimeric enzyme complexes in live cells. J Biol Chem 285: 17771-17777
16. Hu C-D, Chinenov Y, Kerppola TK (2002) Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol Cell 9: 789-798
17. Jensen JK, Schultink A, Keegstra K, Wilkerson CG, Pauly M (April 2 2012) RNA-Seq analysis of developing nasturtium seeds (Tropaeolum majus): identification and characterization of an additional galactosyltransferase involved in xylo-glucan biosynthesis. Mol Plant http://dx.doi.org/10.1093/mp/sss032
18. Jin JB, Kim YA, Kim SJ, Lee SH, Kim DH, Cheong G-W, Hwang I (2001) New dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis. Plant Cell 13: 1511-1526
19. Keegstra K (2010) Plant cell walls. Plant Physiol 154: 483-486
20. Keegstra K, Raikhel NV (2001) Plant glycosyltransferases. Curr Opin Plant Biol 4: 219-224
21. Kurek I, Kawagoe Y, Jacob-Wilk D, Doblin M, Delmer D (2002) Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc-binding domains. Proc Natl Acad Sci USA 99: 11109-11114
22. Li M, Doll J, Weckermann K, Oecking C, Berendzen KW, Schöffl F (2010) Detection of in vivo interactions between Arabidopsis class A-HSFs, using a novel BiFC fragment, and identification of novel class B-HSF interacting proteins. Eur J Cell Biol 89: 126-132
23. Liebminger E, Hüttner S, Vavra U, Fischl R, Schoberer J, Grass J, Blaukopf C, Seifert GJ, Altmann F, Mach L, et al (2009) Class I a-mannosidases are required for N-glycan processing and root development in Arabidopsis thaliana. Plant Cell 21: 3850-3867
24. Madson M, Dunand C, Li X, Verma R, Vanzin GF, Caplan J, Shoue DA, Carpita NC, Reiter W-D (2003) The MUR3 gene of Arabidopsis encodes a xyloglucan galactosyltransferase that is evolutionarily related to animal exostosins. Plant Cell 15: 1662-1670
25. McCormick C, Duncan G, Goutsos KT, Tufaro F (2000) The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes the synthesis of heparan sulfate. Proc Natl Acad Sci USA 97: 668-673
26. Morell M, Espargaro A, Aviles FX, Ventura S (2008) Study and selection of in vivo protein interactions by coupling bimolecular fluorescence complementation and flow cytometry. Nat Protoc 3: 22-33
27. Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo or-ganelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51: 1126-1136
28. Perrin RM, DeRocher AE, Bar-Peled M, Zeng W, Norambuena L, Orellana A, Raikhel NV, Keegstra K (1999) Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis. Science 284: 1976-1979
29. Perrin RM, Wilkerson C, Keegstra K (2001) Golgi enzymes that synthesize plant cell wall polysaccharides: finding and evaluating candidates in the genomicera. Plant Mol Biol 47: 115-130
30. Reyes F, Orellana A (2008) Golgi transporters: opening the gate to cell wall polysaccharide biosynthesis. Curr Opin Plant Biol 11: 244-251
31. Sakuragi Y, Norholm MHH, Scheller HV (2011) Visual mapping of cell wall biosynthesis. In ZA Popper, ed, The Plant Cell Wall: Methods and Protocols. Springer Science-Business Media, Humana Press, New York pp 153-167
32. Sandhu APS, Randhawa GS, Dhugga KS (2009) Plant cell wall matrix polysaccharide biosynthesis. Mol Plant 2: 840-850
33. Saxena IM, Brown RM Jr, Fevre M, Geremia RA, Henrissat B (1995) Multidomain architecture of b-glycosyl transferases: implications for mechanism of action. J Bacteriol 177: 1419-1424
34. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61: 263-289
35. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37: 501-506
36. Søgaard C, Stenbæk A, Bernard S, Hadi M, Driouich A, Scheller HV, Sakuragi Y (2012) GO-PROMTO illuminates protein membrane topologies of glycan biosynthetic enzymes in the Golgi apparatus of living tissues. PLoS ONE 7: e31324
37. Stolz J, Munro S (2002) The components of the Saccharomyces cerevisiae mannosyltransferase complex M-Pol I have distinct functions in mannan synthesis. J Biol Chem 277: 44801-44808
38. Taylor NG, Howells RM, Huttly AK, Vickers K, Turner SR (2003) Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc Natl Acad Sci USA 100: 1450-1455
39. van Meer G (2001) What sugar next? Dimerization of sphingolipid glyco-syltransferases. Proc Natl Acad Sci USA 98: 1321-1323
40. Vanzin GF, Madson M, Carpita NC, Raikhel NV, Keegstra K, Reiter W-D (2002) The mur2 mutant of Arabidopsis thaliana lacks fucosylated xylo-glucan because of a lesion in fucosyltransferase AtFUT1. Proc Natl Acad Sci USA 99: 3340-3345
41. Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C, et al (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40: 428-438
42. Zabotina OA, Avci U, Cavalier D, Pattathil S, Chou YH, Eberhard S, Danhof L, Keegstra K, Hahn MG (2012) Mutations in multiple XXT genes of Arabidopsis reveal the complexity of xyloglucan biosynthesis. Plant Physiol 159: 1367-1384
43. Zabotina OA, van de Ven WTG, Freshour G, Drakakaki G, Cavalier D, Mouille G, Hahn MG, Keegstra K, Raikhel NV (2008) Arabidopsis XXT5 gene encodes a putative a-1,6-xylosyltransferase that is involved in xyloglucan biosynthesis. Plant J 56: 101-115
44. Zeng W, Jiang N, Nadella R, Killen TL, Nadella V, Faik A (2010) A glucurono (arabino)xylan synthase complex from wheat contains members of the GT43, GT47, and GT75 families and functions cooperatively. Plant Physiol 154: 78-97
45. Zhang B, Liu X, Qian Q, Liu L, Dong G, Xiong G, Zeng D, Zhou Y (2011) Golgi nucleotide sugar transporter modulates cell wall biosynthesis and plant growth in rice. Proc Natl Acad Sci USA 108: 5110-5115
46. Zhang GF, Staehelin LA (1992) Functional compartmentation of the Golgi apparatus of plant cells: immunocytochemical analysis of high-pressure frozen- and freeze-substituted sycamore maple suspension culture cells. Plant Physiol 99: 1070-1083