Identification of a novel group of putative Arabidopsis thaliana β-(1,3)-galactosyltransferases

Plant Molecular Biology

Volumn 68, Issue 1-2, 2008, Pages 43-59

  Qu, Yongmei ^a   Egelund, Jack ^b   Gilson, Paul R ^c   Houghton, Fiona ^d   Gleeson, Paul A ^d   Schultz, Carolyn J ^e   Bacic, Antony ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Arabinogalactan protein; CAZy database; Galactosyltransferase; Glycosyltransferase; Golgi

Indexed keywords

ARABIDOPSIS PROTEIN; ARABINOGALACTAN PROTEINS; GALACTOSYLTRANSFERASE; MUCOPROTEIN; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARABIDOPSIS; ARTICLE; CELL STRAIN COS1; CERCOPITHECUS; CLASSIFICATION; DNA MICROARRAY; ENZYME SPECIFICITY; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; GOLGI COMPLEX; IMMUNOBLOTTING; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GALACTOSYLTRANSFERASES; GOLGI APPARATUS; IMMUNOBLOTTING; MOLECULAR SEQUENCE DATA; MUCOPROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYLOGENY; PLANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUBSTRATE SPECIFICITY;

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA;

EID: 48349104344     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-008-9351-3     Document Type: Article

References (81)

1. M Amado R Almeida F Carneiro SB Levery EH Holmes M Nomoto MA Hollingsworth H Hassan T Schwientek PA Nielsen EP Bennett H Clausen 1998 A family of human beta 3-galactosyltransferases-characterization of four members of a UDP-galactose:beta-N-acetyl-glucosamine/beta N-acetyl-galactosamine beta-1,3-galactosyltransferase family J Biol Chem 273 21 12770 12778
2. M Amado R Almeida T Schwientek H Clausen 1999 Identification and characterization of large galactosyltransferase gene families: galactosyltransferases for all functions Biochim Biophys Acta Gen Subj 1473 1 35 53
3. K Awai E Marechal MA Block D Brun T Masuda H Shimada K Takamiya H Ohta J Joyard 2001 Two types of MGDG synthase genes, found widely in both 16:3 and 18:3 plants, differentially mediate galactolipid syntheses in photosynthetic and nonphotosynthetic tissues in Arabidopsis thaliana Proc Natl Acad Sci USA 98 19 10960 10965
4. A Bacic SC Churms AM Stephen PB Cohen GB Fincher 1987 Fine-structure of the arabinogalactan protein form Lolium multiflorum Carbohydr Res 162 1 85 93
5. XM Bai DP Zhou JR Brown BE Crawford T Hennet JD Esko 2001 Biosynthesis of the linkage region of glycosaminoglycans-cloning and activity of galactosyltransferase II, the sixth member of the beta 1,3-galactosyltransferase family (beta 3GalT6) J Biol Chem 276 51 48189 48195
6. SH Barondes V Castronovo DNW Cooper RD Cummings K Drickamer T Feizi MA Gitt J Hirabayashi C Hughes K Kasai H Leffler FT Liu R Lotan AM Mercurio M Monsigny S Pillai F Poirer A Raz PWJ Rigby JM Rini JL Wang 1994 Galectins-a family of animal beta-galactoside-binding lectins Cell 76 4 597 598
7. C Breton E Bettler DH Joziasse RA Geremia A Imberty 1998 Sequence-function relationship of prokaryotic and eukaryotic galactosyltransferases J Biochem Tokyo 123 1000 1009
8. C Breton J Mucha C Jeanneau 2001 Structural and functional features of glycosyltransferases Biochimie 83 8 713 718
9. C Breton L Snajdrova C Jeanneau J Koca A Imberty 2006 Structures and mechanisms of glycosyltransferases Glycobiology 16 2 29 37
10. SL Brown VJ Stockdale F Pettolino KF Pocock MB Lopes PJ Williams A Bacic GB Fincher PB Høj EJ Waters 2007 Reducing haziness in white wine by overexpression of Saccharomyces cerevisiae genes YOL155c and YDR055w Appl Microbiol Biotechnol 73 1363 1376
11. C Busch F Hofmann R Gerhard K Aktories 2000 Involvement of a conserved tryptophan residue in the UDP-glucose binding of large clostridial cytotoxin glycosyltransferases J Biol Chem 275 18 13228 13234
12. JA Campbell GJ Davies V Bulone B Henrissat 1997 A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities Biochem J 326 929 939
13. AE Clarke RL Anderson BA Stone 1979 Form and function of arabinogalactan-proteins Phytochemistry 18 4 521 540
14. ME Cuff KI Miller KE van Holde WA Hendrickson 1998 Crystal structure of a functional unit from Octopus hemocyanin J Mol Biol 278 4 855 870
15. RB Dodd K Drickamer 2001 Lectin-like proteins in model organisms: implications for evolution of carbohydrate-binding activity Glycobiology 11 5 71 79
16. ME Edwards CA Dickson S Chengappa C Sidebottom MJ Gidley JSG Reid 1999 Molecular characterisation of a membrane-bound galactosyltransferase of plant cell wall matrix polysaccharide biosynthesis Plant J 19 691 697
17. O Emanuelsson H Nielsen S Brunak G von Heijne 2000 Predicting subcellular localization of proteins based on their N-terminal amino acid sequence J Mol Biol 300 4 1005 1016
18. GB Fincher BA Stone AE Clarke 1983 Arabinogalactan-proteins-structure, biosynthesis, and function Annu Rev Plant Physiol 34 47 70
19. MG Gao AM Showalter 1999 Yariv reagent treatment induces programmed cell death in Arabidopsis cell cultures and implicates arabinogalactan protein involvement Plant J 19 3 321 331
20. C Garinot-Schneider AC Lellouch RA Geremia 2000 Identification of essential amino acid residues in the Sinorhizobium meliloti glucosyltransferase ExoM J Biol Chem 275 40 31407 31413
21. N Geshi B Jorgensen HV Scheller P Ulvskov 2000 In vitro biosynthesis of 1,4,-beta-galactan attached to rhamnogalacturonan I Planta 210 4 622 629
22. W Gish DJ States 1993 Identification of protein coding regions by database similarity search Nat Genet 3 266 272
23. V Gomord E Wee L Faye 1999 Protein retention and localization in the endoplasmic reticulum and the Golgi apparatus Biochimie 81 6 607 618
24. LJ Goodrum A Patel JF Leykam MJ Kieliszewski 2000 Gum arabic glycoprotein contains glycomodules of both extensin and arabinogalactan-glycoproteins Phytochemistry 54 1 99 106
25. F Goubet C Morvan 1994 Synthesis of cell-wall galactans from flax (Linum usitatissimum L) suspension-cultured cells Plant Cell Physiol 35 5 719 727
26. 2 into the cell-wall polymers of flax hypocotyl, in the course of the fiber differentiation Plant Cell Physiol 34 6 841 848
27. E Grabenhorst P Schlenke S Pohl M Nimtz HS Conradt 1999 Genetic engineering of recombinant glycoproteins and the glycosylation pathway in mammalian host cells Glycoconj J 16 2 81 97
28. JS Griffitts JL Whitacre DE Stevens RV Aroian 2001 Bt toxin resistance from loss of a putative carbohydrate-modifying enzyme Science 293 5531 860 864
29. FA Hanisch 2001 O-glycosylation of the mucin type J Biol Chem 382 2 143 149
30. A Hellberg J Poole ML Olsson 2002 Molecular basis of the globoside-deficient P-k blood group phenotype-identification of four inactivating mutations in the UDP-N-acetylgalactosamine: globotriaosylceramide 3-beta-N-acetylgalactosaminyltransferase gene J Biol Chem 277 33 29455 29459
31. T Hennet 2002 The galactosyltransferase family Cell Mol Life Sci 59 7 1081 1095
32. T Hiruma A Togayachi K Okamura T Sato N Kikuchi YD Kwon A Nakamura K Fujimura M Gotoh K Tachibana Y Ishizuka T Noce H Nakanishi H Narimatsu 2004 A novel human beta 1,3-N-acetylgalactosaminyltransferase that synthesizes a unique carbohydrate structure, GalNAc beta 1-3GlcNAc J Biol Chem 279 14 14087 14095
33. T Iwai N Inaba A Naundorf Y Zhang M Gotoh H Iwasaki T Kudo A Togayachi Y Ishizuka H Nakanishi H Narimatsu 2002 Molecular cloning and characterization of a novel UDP-GlcNAc: GalNAc-peptide,beta 1,3-N-acetylglucosaminyltransferase (beta 3Gn-T6), an enzyme synthesizing the core 3 structure of O-glycans J Biol Chem 277 15 12802 12809
34. KL Johnson BJ Jones A Bacic CJ Schultz 2003 The fasciclin-like arabinogalactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules Plant Physiol 133 1911 1925
35. TZ Ju RD Cummings WM Canfield 2002 Purification, characterization, and subunit structure of rat core 1 beta 1,3-galactosyltransferase J Biol Chem 277 1 169 177
36. GY Juah EM Lord 1996 Localization of pectins and arabinogalactan-proteins in lily (Lilium longiflorum L) pollen tube and style, and their possible roles in pollination Planta 199 2 251 261
37. D Kapitonov RK Yu 1999 Conserved domains of glycosyltransferases Glycobiology 10 961 978
38. WJ Keenleyside AJ Clarke C Whitfield 2001 Identification of residues involved in catalytic activity of the inverting glycosyl transferase WbbE from Salmonella enterica serovar borreze J Bacteriol 183 1 77 85
39. MJ Kieliszewski 2001 The latest hype on Hyp-O-glycosylation codes Phytochemistry 57 3 319 323
40. L Kjer-Nielsen C van Vliet R Erlich BH Toh PA Gleeson 1999 The Golgi-targeting sequence of the peripheral membrane protein p230 J Cell Sci 112 11 1645 1654
41. A Krogh B Larsson G von Heijne ELL Sonnhammer 2001 Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes J Mol Biol 305 3 567 580
42. KJD Lee Y Sakata SL Mau F Pettolino A Bacic RS Quatrano CD Knight JP Knox 2005 Arabinogalactan proteins are required for apical cell extension in the moss Physcomitrella patens Plant Cell 17 11 3051 3065
43. AX Li FZ Kong 2004 Syntheses of arabinogalactans consisting of beta-(1-6)-linked D-galactopyranosyl backbone and alpha-(1-3)-linked L-arabinofuranosyl side chains Carbohydr Res 339 11 1847 1856
44. J Llopis JM McCaffrey A Miyawaki MG Farquhar RY Tsien 1998 Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins Proc Natl Acad Sci USA 95 6803 6808
45. NW Lo JH Shaper J Pevsner NL Shaper 1998 The expanding beta 4-galactosyltransferase gene family: messages from the databanks Glycobiology 8 5 517 526
46. MR Luke L Kjer-Nielsen DL Brown JL Stow PA Gleeson 2003 GRIP domain-mediated targeting of two new coiled-coil proteins, GCC88 and GCC185, to subcompartments of the trans-Golgi network J Biol Chem 278 4216 4226
47. M Malissard A Dinter EG Berger T Hennet 2002 Functional assignment of motifs conserved in beta 1,3-glycosyltransferases-a mutagenesis study of murine UDP-galactose:beta-N-acetylglucosamine beta 1,3-galactosyltransferase-I Eur J Biochem 269 1 233 239
48. T Mascara GB Fincher 1982 Biosynthesis of arabinogalactan-protein in Lolium multiflorum (Ryegrass) endosperm cells-in vitro incorporation of galactosyl residues from UDP-galactose into polymeric products Aust J Plant Physiol 9 1 31 45
49. JM McNab CL Villemez P Albersheim 1968 Biosynthesis of galactan by a particulate enzyme preparation from Phaseolus aureus seedlings Biochem J 106 2 355 360
50. H Motose M Sugiyama H Fukuda 2004 A proteoglycan mediates inductive interaction during plant vascular development Nature 429 873 878
51. N Nakamura M Lowe TP Levine C Rabouille G Warren 1997 The vesicle docking protein p115 binds GM130 a cis-Golgi matrix protein, in a mitotically regulated manner Cell 89 445 455
52. M Negishi J Dong TA Darden LG Pedersen LC Pedersen 2003 Glucosaminylglycan biosynthesis: what we can learn from the X-ray crystal structures of glycosyltransferases GlcAT1 and EXTL2 Biochem Biophys Res Commun 303 2 393 398
53. H Nielsen S Brunak G von Heijen 1999 Machine learning approaches for the prediction of signal peptides and other protein sorting signals Protein Eng 12 3 9
54. EA Nothnagel 1997 Proteoglycans and related components in plant cells Int Rev Cytol 174 195 291
55. KJ Nunan HV Scheller 2003 Solubilization of an arabinan arabinosyltransfgerase activity from mung bean hypocotyls Plant Physiol 132 1 12
56. AS Opat C van Vliet PA Gleeson 2001 Trafficking and localisation of resident Golgi glycosylation enzymes Biochemie 83 763 773
57. RDM Page 1996 TreeView: an application to display phylogenetic trees on personal computers Comput Appl Biosci 12 4 357 358
58. N Panayotatos CL Villemez 1973 Formation of a beta-(1-)4)-D-galactan chain catalyzed by a Phaseolus aureus enzyme Biochem J 133 2 263 271
59. JC Paulson KJ Colley 1989 Glycosylatansferaese-structure, localization, and control of cell type-specific glycosylation J Biol Chem 264 30 17615 17618
60. RM Perrin AE DeRocher M Bar-Peled W Zeng L Norambuena A Orellana NV Raikhel K Keegstra 1999 Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis Science 284 1976 1979
61. R Perrin C Wilkerson K Keegstra 2001 Golgi enzymes that synthesize plant cell wall polysaccharides: finding and evaluating candidates in the genomic era Plant Mol Biol 47 1-2 115 130
62. I Peugnet F Goubet MP Bruyant-Vannier B Thoiron C Morvan HA Schols AGJ Voragen 2001 Solubilization of rhamnogalacturonan I galactosyltransferases from membranes of a flax cell suspension Planta 213 3 435 445
63. W Qi C Fong DTA Lamport 1991 Gum-arabic glycoprotein is a twisted hairy rope-a new model based on O-galactosylhydroxyproline as the polysaccharide attachment site Plant Physiol 96 3 848 855
64. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, NY
65. A Schibeci A Pnjak GB Fincher 1984 Biosynthesis of arabinogalactan- protein in Lolium multiflorum (Italian ryegrass) endosperm cells-subcellular- distribution of galactosyltransferases Biochem J 218 2 633 636
66. C Schultz P Gilson D Oxley J Youl A Bacic 1998 GPI-anchors on arabinogalactan-proteins: implications for signalling in plants TIPS 3 11 426 431
67. R Schwacke A Schneider E van der Graaff K Fischer E Catoni M Desimone WB Frommer UI Flugge R Kunze 2003 ARAMEMNON, a novel database for Arabidopsis integral membrane proteins Plant Physiol 131 1 16 26
68. K Shibayama S Ohsuka T Tanaka Y Arakawa M Ohta 1998 Conserved structural regions involved in the catalytic mechanism of Escherichia coli K-12 WaaO (RfaI) J Bacteriol 180 20 5313 5318
69. AM Showalter 1993 Structure and function of plant-cell wall proteins Plant Cell 5 1 9 23
70. R Strasser JS Bondili U Vavra J Schoberer B Svoboda J Glossl R Leonard J Stadlmann F Altmann H Steinkellner L Mach 2007 A unique 1,3- Galactosyltransferase is indispensable for the biosynthesis of N-glycans containing Lewis a structures in Arabidopsis thaliana Plant Cell 19 2278 2292
71. GE Stenvik MA Butenko BR Urbanowicz JKC Rose RB Aalen 2006 Overexpression of inflorescence deficient in abscission activates cell separation in vestigial abscission zones in Arabidopsis Plant Cell 18 6 1467 1476
72. L Tan J Xu D Lamport F Qiu C Cottrel J Qian M Kieliszewski 2007 The AGP Hyp-arabinogalactan backbone is a folded polysaccharide of reverse-turn hairpins generated by β-(1-6)-linked repeats of β-(1-3) trigalactosyl units. Copenhagen 2007 XIth cell wall meeting. Abstract Physiol Plant 130 68
73. M Tenno S Toba FJ Kezdy AP Elhammer A Kurosaka 2002 Identification of two cysteine residues involved in the binding of UDP-GalNAc to UDP-GalNAc: polypeptide N-acetylgalactosaminyltransferase 1(GalNAc-T1) Eur J Biochem 269 17 4308 4316
74. HJM Thompson JP Knox 1998 Stage-specific responses of embryogenic carrot cell suspension cultures to arabinogalactan protein-binding beta-glucosyl Yariv reagent Planta 205 1 32 38
75. JD Thompson DG Higgins TJ Gibson 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 22 4673 4680
76. JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins 1997 The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res 25 4876 4882
77. M Watanabe K Miyake K Yanae Y Kataoka S Koizumi T Endo A Ozaki S Iijima 2002 Molecular characterization of a novel beta 1,3-galactosyltransferase for capsular polysaccharide synthesis by Streptococcus agalactiae type Ib J Biochem 131 2 183 191
78. CAR Wiggins S Munro 1998 Activity of the yeast MNN1 alpha-1,3- mannosyltransferase requires a motif conserved in many other families of glycosyltransferases Proc Natl Acad Sci USA 95 14 7945 7950
79. MM Wu J Llopis S Adams JM McCaffrey MS Kuloma TE Machen HP Moore RY Tsien 2000 Organelle pH studies using targeted avidin and fluorescein-biotin Chem Biol 7 197 209
80. Z Yuan RD Teasdale 2002 Prediction of Golgi Type II membrane proteins based on their transmembrane domains Bioinformatics 18 8 1109 1115
81. P Zimmermann M Hirsch-Hoffmann L Hennig W Gruissem 2004 GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox Plant Physiol 136 1 2621 2632