Structural characterization of Arabidopsis leaf arabinogalactan polysaccharides

Plant Physiology

Volumn 160, Issue 2, 2012, Pages 653-666

  Tryfona, Theodora ^a   Liang, Hui Chung ^a   Kotake, Toshihisa ^b   Tsumuraya, Yoichi ^b   Stephens, Elaine ^a   Dupree, Paul ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b SAITAMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84867129575     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.202309     Document Type: Article

References (52)

1. 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 GDP-L-fucose. Proc Natl Acad Sci USA 94: 2085-2090.
2. Borner GHH, Lilley KS, Stevens TJ, Dupree P (2003) Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis: a proteomic and genomic analysis. Plant Physiol 132: 568-577.
3. Chai W, Piskarev V, Lawson AM (2001) Negative-ion electrospray mass spectrometry of neutral underivatized oligosaccharides. Anal Chem 73: 651-657.
4. Cheung AY, Wang H, Wu HM (1995) A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 82: 383-393.
5. Chun H, Shin DH, Hong BS, Cho HY, Yang HC (2001) Purification and biological activity of acidic polysaccharide from leaves of Thymus vulgaris L. Biol Pharm Bull 24: 941-946.
6. Ciucanu I, Kerek F (1984) A simple and rapid method for the permethylation of carbohydrates. Carbohydr Res 131: 209-217.
7. Clarke AE, Anderson RL, Stone BA (1979) Form and function of arabinogalactans and arabinogalactan-proteins. Phytochemistry 18: 521-540.
8. Currie HA, Perry CC (2006) Resolution of complex monosaccharide mixtures from plant cell wall isolates by high pH anion exchange chromatography. J Chromatogr A 1128: 90-96.
9. Domon B, Costello CE (1988) A systematic nomenclature for carbohydrate fragmentations in FAβ-MS/MS spectra of glycoconjugates. Glycoconj J 5: 397-409.
10. Estévez JM, Kieliszewski MJ, Khitrov N, Somerville C (2006) Characterization of synthetic hydroxyproline-rich proteoglycans with arabinogalactan protein and extensin motifs in Arabidopsis. Plant Physiol 142: 458-470.
11. Fincher GB, Stone BA, Clarke AE (1983) Arabinogalactan-proteins: structure, biosynthesis, and function. Annu Rev Plant Physiol 34: 47-70.
12. Gane AM, Craik D, Munro SLA, Howlett GJ, Clarke AE, Bacic A (1995) Structural analysis of the carbohydrate moiety of arabinogalactanproteins from stigmas and styles of Nicotiana alata. Carbohydr Res 277: 67-85.
13. Gaspar Y, Johnson KL, McKenna JA, Bacic A, Schultz CJ (2001) The complex structures of arabinogalactan-proteins and the journey towards understanding function. Plant Mol Biol 47: 161-176.
14. Goubet F, Barton CJ, Mortimer JC, Yu X, Zhang Z, Miles GP, Richens J, Liepman AH, Seffen K, Dupree P (2009) Cell wall glucomannan in Arabidopsis is synthesised by CSLA glycosyltransferases, and influences the progression of embryogenesis. Plant J 60: 527-538.
15. Goubet F, Jackson P, Deery MJ, Dupree P (2002) Polysaccharide analysis using carbohydrate gel electrophoresis: a method to study plant cell wall polysaccharides and polysaccharide hydrolases. Anal Biochem 300: 53-68.
16. Haque MA, Kotake T, Tsumuraya Y (2005) Mode of action of β-glucuronidase from Aspergillus niger on the sugar chains of arabinogalactan-protein. Biosci Biotechnol Biochem 69: 2170-2177.
17. Hata K, Tanaka M, Tsumuraya Y, Hashimoto Y (1992) α-L- Arabinofuranosidase from radish (Raphanus sativus L.) seeds. Plant Physiol 100: 388-396.
18. Ichinose H, Kuno A, Kotake T, Yoshida M, Sakka K, Hirabayashi J, Tsumuraya Y, Kaneko S (2006) Characterization of an exo-β-1,3-galactanase from Clostridium thermocellum. Appl Environ Microbiol 72: 3515-3523.
19. Jensen MH, Otten H, Christensen U, Borchert TV, Christensen LLH, Larsen S, Leggio LL (2010) Structural and biochemical studies elucidate the mechanism of rhamnogalacturonan lyase from Aspergillus aculeatus. J Mol Biol 404: 100-111.
20. Kieliszewski MJ, Lamport DTA (1994) Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J 5: 157-172.
21. Konishi T, Kotake T, Soraya D, Matsuoka K, Koyama T, Kaneko S, Igarashi K, Samejima M, Tsumuraya Y (2008) Properties of family 79 β-glucuronidases that hydrolyze β-glucuronosyl and 4-O-methyl-β-glucuronosyl residues of arabinogalactan-protein. Carbohydr Res 343: 1191-1201.
22. Kotake T, Kaneko S, Kubomoto A, Haque MA, Kobayashi H, Tsumuraya Y (2004) Molecular cloning and expression in Escherichia coli of a Trichoderma viride endo-β-(1→6)-galactanase gene. Biochem J 377: 749-755.
23. Lin LY, Ker YB, Chang CH, Chen KC, Peng RY (2011) Arabinogalactan present in the mountain celery seed extract potentiated hypolipidemic bioactivity of coexisting polyphenols in hamsters. Pharm Biol 49: 319-326.
24. Maslen SL, Goubet F, Adam A, Dupree P, Stephens E (2007) Structure elucidation of arabinoxylan isomers by normal phase HPLC-MALDI-TOF/TOF-MS/MS. Carbohydr Res 342: 724-735.
25. Misawa H, Tsumuraya Y, Kaneko Y, Hashimoto Y (1996) α-L-Fucosyltransferases from radish primary roots. Plant Physiol 110: 665-673.
26. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473-497.
27. Nakamura K., Tsumuraya Y, Hashimoto Y, Yamamoto S (1984) Arabinogalactan-proteins reacting with Eel anti-H agglutinin from leaves of cruciferous plants. Agric Biol Chem 48: 753-760.
28. Neukom H, Markwalder H (1975) Isolation and characterization of an arabinogalactan from wheat flour. Carbohydr Res 39: 387-389.
29. O'Neill MA, Eberhard S, Albersheim P, Darvill AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294: 846-849.
30. Qu Y, Egelund J, Gilson PR, Houghton F, Gleeson PA, Schultz CJ, Bacic A (2008) Identification of a novel group of putative Arabidopsis thaliana β-(1,3)-galactosyltransferases. Plant Mol Biol 68: 43-59.
31. Redgwell RJ, Curti D, Fischer M, Nicolas P, Fay LB (2002) Coffee bean arabinogalactans: acidic polymers covalently linked to protein. Carbohydr Res 337: 239-253.
32. Reiter W-D, Chapple C, Somerville CR (1997) Mutants of Arabidopsis thaliana with altered cell wall polysaccharide composition. Plant J 12: 335-345.
33. Reiter W-D, Chapple CCS, Somerville CR (1993) Altered growth and cell walls in a fucose-deficient mutant of Arabidopsis. Science 261: 1032-1035.
34. Renard CMGC, Voragen AGJ, Thibault JF, Pilnik W (1991) Studies on apple protopectin. V. Structural studies on enzymatically extracted pectins. Carbohydr Polym 16: 137-154.
35. Ridlova G, Mortimer JC, Maslen SL, Dupree P, Stephens E (2008) Oligosaccharide relative quantitation using isotope tagging and normalphase liquid chromatography/mass spectrometry. Rapid Commun Mass Spectrom 22: 2723-2730.
36. Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58: 137-161.
37. Spina E, Sturiale L, Romeo D, Impallomeni G, Garozzo D, Waidelich D, Glueckmann M (2004) New fragmentation mechanisms in matrix-assisted laser desorption/ionization time-of-flight/time-of-flight tandem mass spectrometry of carbohydrates. Rapid Commun Mass Spectrom 18: 392-398.
38. Takata R, Tokita K, Mori S, Shimoda R, Harada N, Ichinose H, Kaneko S, Igarashi K, Samejima M, Tsumuraya Y, et al (2010) Degradation of carbohydrate moieties of arabinogalactan-proteins by glycoside hydrolases from Neurospora crassa. Carbohydr Res 345: 2516-2522.
39. Tan L, Qiu F, Lamport DTA, Kieliszewski MJ (2004) Structure of a hydroxyproline (Hyp)-arabinogalactan polysaccharide from repetitive Alα-Hyp expressed in transgenic Nicotiana tabacum. J Biol Chem 279: 13156-13165.
40. Tan L, Varnai P, Lamport DTA, Yuan C, Xu J, Qiu F, Kieliszewski MJ (2010) Plant O-hydroxyproline arabinogalactans are composed of repeating trigalactosyl subunits with short bifurcated side chains. J Biol Chem 285: 24575-24583.
41. Tryfona T, Liang H-C, Kotake T, Kaneko S, Marsh J, Ichinose H, Lovegrove A, Tsumuraya Y, Shewry PR, Stephens E, et al (2010) Carbohydrate structural analysis of wheat flour arabinogalactan protein. Carbohydr Res 345: 2648-2656.
42. Tryfona T, Stephens E (2010) Analysis of carbohydrates on proteins by offline normal-phase liquid chromatography MALDI-TOF/TOF-MS/ MS. Methods Mol Biol 658: 137-151.
43. Tsumuraya Y, Hashimoto Y, Yamamoto S, Shibuya N (1984a) Structure of l-arabino-D-galactan-containing glycoproteins from radish leaves. Carbohydr Res 134: 215-228.
44. Tsumuraya Y, Mochizuki N, Hashimoto Y, Kovác P (1990) Purification of an exo-betα-(1→3)-D-galactanase of Irpex lacteus (Polyporus tulipiferae) and its action on arabinogalactan-proteins. J Biol Chem 265: 7207-7215.
45. Tsumuraya Y, Nakamura K, Hashimoto Y, Yamamoto S (1984b) Immunological properties of arabinogalactan proteins from leaves of cruciferous plants. Agric Biol Chem 48: 2915-2917.
46. Tsumuraya Y, Ogura K, Hashimoto Y, Mukoyama H, Yamamoto S (1988) Arabinogalactan-proteins from primary and mature roots of radish (Raphanus sativus L.). Plant Physiol 86: 155-160.
47. van Hengel AJ, Roberts K (2002) Fucosylated arabinogalactan-proteins are required for full root cell elongation in Arabidopsis. Plant J 32: 105-113.
48. van Hengel AJ, Van Kammen A, De Vries SC (2002) A relationship between seed development, arabinogalactan-proteins (AGPs) and the AGP mediated promotion of somatic embryogenesis. Physiol Plant 114: 637-644.
49. van Holst G-J, Clarke AE (1985) Quantification of arabinogalactan-protein in plant extracts by single radial gel diffusion. Anal Biochem 148: 446-450.
50. Wu Y, Williams M, Bernard S, Driouich A, Showalter AM, Faik A (2010) Functional identification of two nonredundant Arabidopsis alpha(1,2) fucosyltransferases specific to arabinogalactan proteins. J Biol Chem 285: 13638-13645.
51. Xu J, 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.
52. Yariv J, Lis H, Katchalski E (1967) Precipitation of arabic acid and some seed polysaccharides by glycosylphenylazo dyes. Biochem J 105: 1C-2C.