Biochemical and physiological characterization of fut4 and fut6 mutants defective in arabinogalactan-protein fucosylation in Arabidopsis

Journal of Experimental Botany

Volumn 64, Issue 18, 2013, Pages 5537-5551

  Liang, Yan ^a,d   Basu, Debarati ^a   Pattathil, Sivakumar ^b   Xu, Wen Liang ^a,e   Venetos, Alexandra ^a   Martin, Stanton L ^c   Faik, Ahmed ^a   Hahn, Michael G ^b   Showalter, Allan M ^a  

^a OHIO UNIVERSITY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c SAS INSTITUTE INC   (United States)

^d JOINT BIOENERGY INSTITUTE   (United States)

^e CENTRAL CHINA NORMAL UNIVERSITY   (China)

Author keywords

Arabidopsis; arabinogalactan proteins; fucosyltransferase; glycosylation; hydroxyproline rich proteins; plant cell wall

Indexed keywords

ARABIDOPSIS PROTEIN; ARABINOGALACTAN PROTEINS; FUCOSYLTRANSFERASE; FUT4 PROTEIN, ARABIDOPSIS; FUT6 PROTEIN, ARABIDOPSIS; MUCOPROTEIN; VEGETABLE PROTEIN;

ARABIDOPSIS; ARABINOGALACTAN-PROTEINS; ARTICLE; CELL WALL; GENETICS; GLYCOSYLATION; GROWTH, DEVELOPMENT AND AGING; HYDROXYPROLINE-RICH PROTEINS; IMMUNOLOGY; METABOLISM; MUTATION; PLANT CELL WALL.; PLANT LEAF; PLANT ROOT;

ARABIDOPSIS; ARABINOGALACTAN-PROTEINS; FUCOSYLTRANSFERASE; GLYCOSYLATION; HYDROXYPROLINE-RICH PROTEINS; PLANT CELL WALL.;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL WALL; FUCOSYLTRANSFERASES; GLYCOSYLATION; MUCOPROTEINS; MUTATION; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS;

EID: 84891538392     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert321     Document Type: Article

References (66)

1. Baldwin TC, McCann MC, Roberts K. 1993. A novel hydroxyproline-deficient arabinogalactan protein secreted by suspension-cultured cells of Daucus carota (purification and partial characterization). Plant Physiology 103, 115-123
2. Basu D, Liang Y, Liu X, Himmeldirk K, Faik A, Kieliszewski M, Held M, Showalter AM. 2013. Functional identification of a hydroxyproline-O- galactosyltransferase specific for arabinogalactanprotein biosynthesis in Arabidopsis. Journal of Biological Chemistry 288, 10132-10143
3. Bonin CP, Potter I, Vanzin GF, Reiter W-D. 1997. The MUR1 gene of Arabidopsis thaliana encodes an isoform of GDP-D-mannose-4,6-dehydratase, catalyzing the first step in the de novo synthesis of GDPL-fucose. Proceedings of the National Academy of Sciences USA 94, 2085-2090
4. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Gorlach J. 2001. Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants. The Plant Cell 13, 1499-1510
5. Cannon MC, Terneus K, Hall Q, Tan L, Wang Y, Wegenhart BL, Chen L, Lamport DT, Chen Y, Kieliszewski MJ. 2008. Selfassembly of the plant cell wall requires an extensin scaffold. Proceedings of the National Academy of Sciences USA 105, 2226-2231
6. Carpita N, McCann M. 2000. The cell wall. In BB Buchanan, W Gruissem, R Jones, eds, Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, MD, pp 52-109
7. Carpita NC. 1989. Pectic polysaccharides of maize coleoptiles and proso millet cells in liquid culture. Phytochemistry 28, 121-125
8. Carpita NC, Gibeaut DM. 1993. Structural models of primary-cell walls in flowering plants-consistency of molecular-structure with the physical-properties of the walls during growth. The Plant Journal 3, 1-30
9. Ding L, Zhu JK. 1997. A role for arabinogalactan-proteins in root epidermal cell expansion. Planta 203, 289-294
10. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350-356
11. Ellis M, Egelund J, Schultz CJ, Bacic A. 2010. Arabinogalactanproteins: Key regulators at the cell surface? Plant Physiology 153, 403-419
12. Faik A, Bar-Peled M, DeRocher AE, Zeng WQ, Perrin RM, Wilkerson C, Raikhel NV, Keegstra K. 2000. Biochemical characterization and molecular cloning of an alpha-1,2-fucosyltransferase that catalyzes the last step of cell wall xyloglucan biosynthesis in pea. Journal of Biological Chemistry 275, 15082-15089
13. Fry SC. 1988. The Growing Plant Cell Wall: Chemical and Metabolic Analysis. Longman Scientific & Technical, Essex
14. Gaspar YM, Nam J, Schultz CJ, Lee L-Y, Gilson PR, Gelvin SB, Bacic A. 2004. Characterization of the Arabidopsis lysine-rich arabinogalactan-protein ATAGP17 mutant (rat1) that results in a decreased efficiency of Agrobacterium transformation. Plant Physiology 135, 2162-2171
15. Geshi N, Johansen JN, Dilokpimol A et al. 2013. A galactosyltransferase acting on arabinogalactan protein glycans is essential for embryo development in Arabidopsis. The Plant Journal, doi: 10.1111/tpj.12281
16. Gibeaut DM, Hulett J, Cramer GR, Seemann Jr. 1997. Maximal biomass of Arabidopsis thaliana using a simple, low-maintenance hydroponic method and favorable environmental conditions. Plant Physiology 115, 317-319
17. Gille S, Sharma V, Baidoo EEK, Keasling JD, Scheller HV, Pauly M. 2013. Arabinosylation of a Yariv-precipitable cell wall polymer impacts plant growth as exemplified by the Arabidopsis glycosyltransferase mutant ray1. Molecular Plant 6, 1369-1372
18. Gorshkova TA, Wyatt SE, Salnikov VV, Gibeaut DM, Ibragimov MR, Lozovaya VV, Carpita NC. 1996. Cell-wall polysaccharides of developing flax plants. Plant Physiology 110, 721-729
19. Günter EA, Popéko OV, OvodovIu S. 2004. Isolation of polysaccharides from callus culture of Lemna minor L. Applied Biochemistry and Microbiology 40, 80-83
20. Hashimoto Y. 2000. Structure and biosynthesis of L-fucosylated arabinogalactan-proteins in cruciferous plants. In EA Nothnagel, A Bacic, AE Clarke, eds, Cell and Developmental Biology of Arabinogalactan-Proteins. Kluwer Academic/Plenum Publishers, New York, pp 51-60
21. Hayashi T, Maclachlan G. 1984. Glycolipids and glycoproteins formed from UDP-galactose by pea membranes. Phytochemistry 23, 487-492
22. Immerzeel P, Eppink MM, De Vries SC, Schols HA, Voragen AGJ. 2006. Carrot arabinogalactan proteins are interlinked with pectins. Physiologia Plantarum 128, 18-28
23. Iraki NM, Singh N, Bressan RA, Carpita NC. 1989. Cell-walls of tobacco cells and changes in composition associated with reduced growth upon adaptation to water and saline stress. Plant Physiology 91, 48-53
24. Lamport DT, Kieliszewski MJ, Showalter AM. 2006. Salt stress upregulates periplasmic arabinogalactan proteins: Using salt stress to analyse AGP function. New Phytologist 169, 479-492
25. Lamport DTA, Kieliszewski MJ, Chen Y, Cannon MC. 2011. Role of the extensin superfamily in primary cell wall architecture. Plant Physiology 156, 11-19
26. Liang Y, Faik A, Kieliszewski M, Tan L, Xu WL, Showalter AM. 2010. Identification and characterization of in vitro galactosyltransferase activities involved in arabinogalactan-protein glycosylation in tobacco and Arabidopsis. Plant Physiology 154, 632-642
27. Mascara T, Fincher GB. 1982. Biosynthesis of arabinogalactanprotein in Lolium multiflorum (ryegrass) endosperm cells. 2. In vitro incorporation of galactosyl residues from UDP-galactose into polymeric products. Australian Journal of Plant Physiology 9, 31-45
28. Masuko T, Minami A, Iwasaki N, Majima T, Nishimura S-I, Lee YC. 2005. Carbohydrate analysis by a phenol-sulfuric acid method in microplate format. Analytical Biochemistry 339, 69-72
29. Memelink J, Swords KMM, Dekam RJ, Schilperoort RA, Hoge JHC, Staehelin LA. 1993. Structure and regulation of tobacco extensin. The Plant Journal 4, 1011-1022
30. Misawa H, Tsumuraya Y, Kaneko Y, Hashimoto Y. 1996. Alpha- Lfucosyltransferases from radish primary roots. Plant Physiology 110, 665-673
31. Nam J, Mysore KS, Zheng C, Knue MK, Matthysse AG, Gelvin SB. 1999. Identification of T-DNA tagged Arabidopsis mutants that are resistant to transformation by Agrobacterium. Molecular and General Genetics 261, 429-438
32. Nothnagel EA. 1997. Proteoglycans and related components in plant cells. International Review of Cytology. A Survey of Cell Biology. 174, 195-291
33. Oka T, Saito F, Shimma YI, Yoko-O T, Nomura Y, Matsuoka K, Jigami Y. 2010. Characterization of endoplasmic reticulum-localized UDP-D-galactose: Hydroxyproline O-galactosyltransferase using synthetic peptide substrates in Arabidopsis. Plant Physiology 152, 332-340
34. Pattathil S, Avci U, Baldwin D et al. 2010. A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiology 153, 514-525
35. Pattathil S, Avci U, Miller JS, Hahn MG. 2012. Immunological approaches to plant cell wall and biomass characterization: Glycome profiling. In M Himmel, ed, Biomass Conversion: Methods and Protocols, Methods in Molecular Biology, Vol 908. Springer Science & Business Media, New York, pp 61-72
36. Perrin RM, DeRocher AE, Bar-Peled M, Zeng WQ, Norambuena L, Orellana A, Raikhel NV, Keegstra K. 1999. Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis. Science 284, 1976-1979
37. Ponce MR, Quesada V, Micol JL. 1998. Rapid discrimination of sequences flanking and within T-DNA insertions in the Arabidopsis genome. The Plant Journal 14, 497-501
38. Puhlmann J, Bucheli E, Swain MJ, Dunning N, Albersheim P, Darvill AG, Hahn MG. 1994. Generation of monoclonal-Antibodies against plant cell-wall polysaccharides. I. Characterization of a monoclonal-Antibody to a terminal alpha-(1→2)-linked fucosylcontaining epitope. Plant Physiology 104, 699-710
39. Reiter WD, Chapple C, Somerville CR. 1997. Mutants of Arabidopsis thaliana with altered cell wall polysaccharide composition. The Plant Journal 12, 335-345
40. Roy S, Jauh GY, Hepler PK, Lord EM. 1998. Effects of Yariv phenylglycoside on cell wall assembly in the lily pollen tube. Planta 204, 450-458
41. Sarria R, Wagner TA, O'Neill MA, Faik A, Wilkerson CG, Keegstra K, Raikhel NV. 2001. Characterization of a family of Arabidopsis genes related to xyloglucan fucosyltransferase1. Plant Physiology 127, 1595-1606
42. Schibeci A, Pnjak A, Fincher GB. 1984. Biosynthesis of arabinogalactan-protein in Lolium multiflorum (Italian ryegrass) endosperm cells-subcellular-distribution of galactosyltransferases. Biochemical Journal 218, 633-636
43. Schultz CJ, Johnson KL, Currie G, Bacic A. 2000. The classical arabinogalactan protein gene gamily of Arabidopsis. The Plant Cell 12, 1751-1768
44. Seifert GJ, Roberts K. 2007. The biology of arabinogalactan proteins. Annual Review of Plant Biology 58, 137-161
45. Shi HZ, Kim Y, Guo Y, Stevenson B, Zhu JK. 2003. The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. The Plant Cell 15, 19-32
46. Showalter AM. 1993. Structure and function of plant cell wall proteins. The Plant Cell 5, 9-23
47. Showalter AM. 2001. Arabinogalactan-proteins: Structure, expression and function. Cellular and Molecular Life Sciences 58, 1399-1417
48. Showalter AM, Keppler B, Lichtenberg J, Gu DZ, Welch LR. 2010. A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiology 153, 485-513
49. Shpak E, Barbar E, Leykam JF, Kieliszewski MJ. 2001. Contiguous hydroxyproline residues direct hydroxyproline arabinosylation in Nicotiana tabacum. Journal of Biological Chemistry 276, 11272-11278
50. Springer GF, Desai PR. 1971. Monosaccharides as specific precipitinogens of eel antihuman blood-group H(O) antibody. Biochemistry 10, 3749-3761
51. Tan L, Eberhard S, Pattathil S et al. 2013. An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein. The Plant Cell 25, 270-287
52. Tan L, Qiu F, Lamport DT, Kieliszewski MJ. 2004. Structure of a hydroxyproline (Hyp)-Arabinogalactan polysaccharide from repetitive Ala-Hyp expressed in transgenic Nicotiana tabacum. Journal of Biological Chemistry 279, 13156-13165
53. Tryfona T, Liang H-C, Kotake T, Tsumuraya Y, Stephens E, Dupree P. 2012. Structural characterisation of Arabidopsis leaf arabinogalactan polysaccharides. Plant Physiology 160, 653-666
54. Tsumuraya Y, Hashimoto Y, Yamamoto S. 1987. An L-Arabino-D-galactan and an L-Arabino-D-galactan-containing proteoglycan from radish (Raphanus sativus) seeds. Carbohydrate Research 161, 113-126
55. Tsumuraya Y, Hashimoto Y, Yamamoto S, Shibuya N. 1984. Structure of L-Arabino-D-galactan-containing glycoproteins from radish leaves. Carbohydrate Research 134, 215-228
56. Tsumuraya Y, Ogura K, Hashimoto Y, Mukoyama H, Yamamoto S. 1988. Arabinogalactan-proteins from primary and mature roots of radish (Raphanus sativus L). Plant Physiology 86, 155-160
57. van Hengel AJ, Roberts K. 2002. Fucosylated arabinogalactanproteins are required for full root cell elongation in Arabidopsis. The Plant Journal 32, 105-113
58. Vanzin GF, Madson M, Carpita NC, Raikhel NV, Keegstra K, Reiter WD. 2002. The mur2 mutant of Arabidopsis thaliana lacks fucosylated xyloglucan because of a lesion in fucosyltransferase AtFUT1. Proceedings of the National Academy of Sciences USA 99, 3340-3345
59. Watkins WM, Morgan WT. 1952. Neutralization of the anti-H agglutinin in eel serum by simple sugars. Nature. 169, 825-826
60. Wei G, Shirsat AH. 2006. Extensin over-expression in Arabidopsis limits pathogen invasiveness. Molecular Plant Pathology 7, 579-592
61. Willats WGT, Knox JP. 1996. A role for arabinogalactan-proteins in plant cell expansion: Evidence from studies on the interaction of beta-glucosyl Yariv reagent with seedlings of Arabidopsis thaliana. The Plant Journal 9, 919-925
62. Wu YY, Williams M, Bernard S, Driouich A, Showalter AM, Faik A. 2010. Functional identification of two nonredundant Arabidopsis α(1,2) fucosyltransferases specific to arabinogalactan proteins. Journal of Biological Chemistry 285, 13638-13645
63. Xu JF, Tan L, Lamport DTA, Showalter AM, Kieliszewski MJ. 2008. The O-Hyp glycosylation code in tobacco and Arabidopsis and a proposed role of Hyp-glycans in secretion. Phytochemistry 69, 1631-1640
64. Yong WD, Link B, O'Malley R et al. 2005. Genomics of plant cell wall biogenesis. Planta 221, 747-751
65. Zhan X, Wang B, Li H, Liu R, Kalia RK, Zhu J-K, Chinnusamy V. 2012. Arabidopsis proline-rich protein important for development and abiotic stress tolerance is involved in microRNA biogenesis. Proceedings of the National Academy of Sciences USA 109, 18198-18203
66. Zhu S-Y, Yu X-C, Wang X-J et al. 2007. Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. The Plant Cell 19, 3019-3036