Oxidative coupling of tyrosine and ferulic acid residues: Intra- and extra-protoplasmic occurrence, predominance of trimers and larger products, and possible role in inter-polymeric cross-linking

Phytochemistry Reviews

Volumn 3, Issue 1-2, 2004, Pages 97-111

  Fry, Stephen C ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cell walls; Cross linking; Extensin; Ferulic acid; Hydrogen peroxide; p coumaric acid; Peroxidase; Polysaccharides; Tyrosine

Indexed keywords

CINNAMIC ACID DERIVATIVE; FERULIC ACID; GLYCOPROTEIN; LACCASE; OLIGOMER; PHENOL DERIVATIVE; POLYMER; POLYSACCHARIDE; TYROSINE;

BIOASSAY; CELL WALL; CELLULAR DISTRIBUTION; CROSS COUPLING REACTION; CROSS LINKING; ENZYME ACTIVITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE; NONHUMAN; OXIDATIVE STRESS; PHYTOCHEMISTRY; PRIORITY JOURNAL; PROBABILITY; REVIEW;

ZEA MAYS;

EID: 23944490840     PISSN: 15687767     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:PHYT.0000047808.74647.43     Document Type: Review

References (82)

1. Aeschbach R, Amadò R & Neukom H (1976) Formation of dityrosine cross-links in proteins by oxidation of tyrosine residues. Biochim. Biophys. Acta 439: 292-301.
2. Andersen SO (1964) The cross-links in resilin identified as dityrosine and trityrosine. Biochim. Biophys. Acta 93: 213-215.
3. Bacon MA, Thompson DS & Davies WJ (1997) Can cell wall peroxidase activity explain the leaf growth response of Lolium temulentum L. during drought? J. Exp. Bot. 48: 2075-2085.
4. Baydoun EA-H, Pavlencheva N, Cumming CM, Waldron KW & Brett CT (2004) Control of dehydrodiferulate cross-linking in pectins from sugar-beet tissues. Phytochemistry 65: 1107-1115.
5. Biggs KJ & Fry SC (1990) Solubilization of covalently bound extensin from Capsicum cell walls Plant Physiol. 92: 197-204.
6. Bily AC, Reid LM, Taylor JH, Johnston D, Malouin C, Burt AJ, Bakan B, Regnault-Roger C, Pauls KP, Arnason JT & Philogène BJR (2003) Dehydrodimers of ferulic acid in maize grain pericarp and aleurone: resistance factors to Fusarium graminearum. Phytopathology 93: 712-719.
7. Bradley DJ, Kjellbom P & Lamb CJ (1992) Elicitor-induced and wound-induced oxidative cross-linking of a proline-rich plant-cell wall protein - a novel, rapid defence response. Cell 70: 21-30.
8. Brady JD, Sadler IH & Fry SC (1996) Di-isodityrosine, a novel tetrameric derivative of tyrosine in plant well wall proteins: a new potential cross-link. Biochem. J. 315: 323-327.
9. Brady JD, Sadler IH & Fry SC (1997) Pulcherosine, an oxidatively coupled trimer of tyrosine in plant cell walls: its role in cross-link formation. Phytochemistry 47: 349-353.
10. Brownleader MD, Hopkins J, Mobasheri A, Dey PM, Jackson P & Trevan M (2000) Role of extensin peroxidase in tomato (Lycopersicon esculentum Mill.) seedling growth. Planta 210: 668-676.
11. Bunzel M, Ralph J, Funk C & Steinhart H (2003) Isolation and identification of a ferulic acid dehydrotrimer from saponified maize bran insoluble fibre. Eur. Food Res. Technol. 217: 128-133.
12. Colquhoun IJ, Ralet MC, Thibault JF, Faulds CB & Williamson G (1994) Structure identification of feruloylated oligosaccharides from sugar-beet pulp by NMR spectroscopy. Carbohydr. Res. 263: 243-256.
13. Cooper JB & Varner JE (1983) Insolubilization of hydroxyproline-rich cell wall glycoprotein in aerated carrot root slices. Biochem. Biophys. Res. Commun. 112: 161-167.
14. Cooper JB & Varner JE (1984) Cross-linking of soluble extensin in isolated cell walls. Plant Physiol. 76: 414-417.
15. Driouich A, Levy S, Staehelin LA & Faye L (1994) Structural and functional organisation of the Golgi apparatus in plant cells. Plant Physiol. Biochem. 32: 731-749.
16. Enoki A, Yaku F, & Koshijima T (1983). Synthesis of LCC model compounds and their chemical and enzymatic stabilities. Holzforschung 37: 135-141.
17. Epstein L & Lamport DTA (1984) An intramolecular linkage involving isodityrosine in extensin. Phytochemistry 23, 1241-1246.
18. Everdeen DS, Kiefer S, Willard JJ, Muldoon EP, Dey PM, Li X-B, & Lamport DTA (1988) Enzymic cross-linkage of monomeric extensin precursors in vitro. Plant Physiol. 87: 616-621.
19. Frahry G & Schopfer P (1998) Hydrogen peroxide production by roots and its stimulation by exogenous NADH. Physiol. Plant. 103: 395-404.
20. Fry SC (1979) Phenolic components of the primary cell wall and their possible rôle in the hormonal regulation of growth. Planta 146: 343-351.
21. Fry SC (1980) Gibberellin-controlled pectinic acid and protein secretion in growing cells. Phytochemistry 19: 735-740.
22. Fry SC (1982a) Phenolic components of the primary cell wall: feruloylated disaccharides of D-galactose and L-arabinose from spinach polysaccharide. Biochem. J. 203: 493-504.
23. Fry SC (1982b) Isodityrosine, a new cross-linking amino acid from plant cell-wall glycoprotein. Biochem. J. 204: 449-455.
24. 14C]cinnamate into hydrolase-resistant components of the primary cell wall. Phytochemistry 23: 59-64.
25. Fry SC (1986) Cross-linking of matrix polymers in the growing cell walls of angiosperms. Annu. Rev. Plant Physiol. 37: 165-186.
26. Fry SC (1987) Intracellular feruloylation of pectic polysaccharides. Planta 171: 205-211.
27. Fry SC (2000) The Growing Plant Cell Wall: Chemical and Metabolic Analysis Reprint Edition, Blackburn Press
28. Fry SC & Northcote DH (1983) Sugar-nucleotide precursors of the arabinofuranosyl, arabinopyranosyl and xylopyranosyl residues of spinach polysaccharides. Plant Physiol. 73: 1055-1061.
29. Fry SC, Willis SC & Paterson AEJ (2000) Intraprotoplasmic and wall-localised formation of arabinoxylan-bound diferulates and larger ferulate coupling-products in maize cell-suspension cultures Planta 211: 679-692.
30. Geissmann T & Neukom H (1971) Vernetzung von Phenolcarbonsä ureestern von Polysacchariden durch oxydative phenolische Kupplung. Helv. Chim. Acta 54: 1108-1112.
31. Grabber JH, Hatfield RD, Ralph J, Zon'J & Amrhein N (1995) Ferulate cross-linking in cell walls isolated from maize cell suspensions Phytochemistry 40: 1077-1082.
32. Gross AJ & Sizer IW (1959). The oxidation of tyramine, tyrosine and related compound by peroxidase. J. Biol. Chem. 234: 1611-1614.
33. Harris PJ & Hartley RD (1980) Phenolic constituents of the cell walls of Monocotyledons. Biochem. Syst. Ecol. 8: 153-160.
34. Hartley RD & Harris PJ (1981) Phenolic constituents of the cell walls of Dicotyledons. Biochem. Syst. Ecol. 9: 189-203.
35. Hartley RD & Jones EC (1976). Diferulic acid as a component of cell walls of Lolium multiflorum. Phytochemistry 15: 1157-1160.
36. Hartley RD, Morrison WH, Himmelsbach DS & Borneman WS (1990) Cross-linking of cell wall phenolic arabinoxylans in graminaceous plants. Phytochemistry 29: 3705-3709.
37. Hatfield RD, Ralph J & Grabber JH (1999) Cell wall cross-linking by ferulates and diferulates in grasses. J. Sci. Food Agric. 79: 403-407.
38. Iiyama K., Lam TBT & Stone BA (1994) Covalent cross-links in the cell wall. Plant Physiol. 104: 315-320.
39. Ishii T (1991) Isolation and characterization of a diferuloyl arabinoxylan hexasaccharide from bamboo shoot cell-walls. Carbohydr Res 219: 15-22.
40. Ishii T (1997) Structure and functions of feruloylated polysaccharides Plant Science, 127, 111-127.
41. Jackson P, Paulo S, Brownleader M, Freire PO & Ricardo CPP (1999) An extensin peroxidase is associated with white-light inhibition of lupin (Lupinus albus) hypocotyl growth. Aust. J. Plant Physiol. 26: 29-36.
42. Jackson PAP, Galinha CIR, Pereira CS, Fortunato A, Soares NC, Amancio SBQ & Ricardo CPP (2001) Rapid deposition of extensin during the elicitation of grapevine callus cultures is specifically catalysed by a 40-kilodalton peroxidase. Plant Physiol. 127: 1065-1076
43. Jupe SC & Scott IM (1992) Gibberellin and the pro gene suppress peroxidase activity in elongating tomato (Lycopersicon esculentum Mill.) stem tissues. Ann. Bot. 69: 33-37.
44. Kamisaka S, Takeda S, Takahashi K & Shibata K (1990) Diferulic and ferulic acids in the cell wall of oat coleoptiles - their relationships to mechanical properties of the cell wall Physiol. Plant. 78, 1-7.
45. Kerr EM & Fry SC (2003) Pre-formed xyloglucans and xylans increase in molecular weight in three distinct compartments of a maize cell-suspension culture. Planta 217: 327-339.
46. Kerr EM & Fry SC (2004). Extracellular cross-linking of xylan and xyloglucan in maize cell-suspension cultures: the role of oxidative phenolic coupling. Planta, 219: 73-83.
47. 2+-mediated binding of the glycoprotein peroxidase to membranes of Pharbitis cotyledons Plant Sci. 39: 37-43.
48. Lopez Llorca LV & Fry SC (1989) Dityrosine, trityrosine and tetratyrosine, potential cross-links in structural proteins of plant-parasitic nematodes. Nematologica 35: 165-179.
49. Macadam JW, Nelson CJ & Sharp RE (1992) Peroxidase activity in the elongation zone of tall fescue. II. Spatial distribution of apoplastic peroxidase activity in genotypes differing in length of elongation zone. Plant Physiol. 99: 879-885.
50. Markwalder H-U & Neukom H (1976) Diferulic acid as a possible crosslink in hemicelluloses from wheat germ. Phytochemistry 15: 836-837.
51. Marshall JG, Dumbroff EB, Thatcher BJ, Martin B, Rutledge RG & Blumwald E (1999) Synthesis and oxidative insolubilization of cell-wall proteins during osmotic stress. Planta 208: 401-408.
52. Miyamoto K, Ueda J, Takeda S, Ida K, Hoson T, Masuda Y & Kamisaka S (1994) Light-induced increase in the contents of ferulic and diferulic acids in cell walls of Avena coleoptiles: its relationship to growth inhibition by light. Physiol. Plant. 92: 350-355.
53. Moore JP, Taylor JE, Paul ND & Whittaker JB (2003) Reduced leaf expansion as a cost of systemic induced resistance to herbivory. Functional Ecology 17: 75-81.
54. Myton KE & Fry SC (1994) Intraprotoplasmic feruloylation of arabinoxylans in Festuca arundinacea cell cultures. Planta 193: 326-330.
55. Myton KE & Fry SC (1995) Dithiothreitol and cobalt effects on membrane-associated peroxidases oxidizing feruloyl-CoA. Phytochemistry 38: 573-577.
56. Nomura K, Suzuki N & Matsumoto S (1990) Pulcherosine, a novel tyrosine-derived, trivalent cross-linking amino-acid from the fertilization envelope of sea-urchin embryo. Biochemistry 29: 4525-4534.
57. Northcote DH & Pickett-Heaps JD (1966) A function of the Golgi apparatus in polysaccharide synthesis and transport in the root-cap cells of wheat. Biochem. J. 98: 159-167.
58. Obel N, Porchia AC & Scheller HV (2002) Dynamic changes in cell wall polysaccharides during wheat seedling development. Phytochemistry 60: 603-610.
59. Otte O & Barz W (2000) Characterization and oxidative in vitro cross-linking of an extensin-like protein and a proline-rich protein purified from chickpea cell walls. Phytochemistry 53: 1-5.
60. Parr AJ, Waldron KW, Ng A & Parker ML (1996) The wall-bound phenolics of Chinese water chestnut (Eleocharis dulcis). J. Sci. Food Agric. 71: 501-507.
61. Parvez MM, Wakabayashi K, Hoson T & Kamisaka S (1997) White light promotes the formation of diferulic acid in maize coleoptile cell walls by enhancing PAL activity. Physiol. Plant. 99: 39-48.
62. Ralph J, Quideau S, Grabber JH & Hatfield RD (1994) Identification and synthesis of new ferulic acid dehydrodimers present in grass cell walls. J. Chem. Soc. Perkin Trans. (I) 1994: 3485-3498.
63. Ranocha P, McDougall G, Hawkins S, Sterjiades R, Borderies G, Stewart D, Cabanes-Macheteau M, Boudet AM & Goffner D (1999) Biochemical characterization, molecular cloning and expression of laccases - a divergent gene family - in poplar. Eur. J. Biochem. 259: 485-495.
64. Rodriguez-Arcos RC, Smith AC & Waldron KW (2002) Effect of storage on wall-bound phenolics in green asparagus. J. Agric. Food Chem. 50: 3197-3203.
65. Ros Barceló AR, Muñoz F, Sabater F (1988) Lupin peroxidases. III. Subcellular location of membrane-bound acidic peroxidases. Plant. Physiol. Biochem. 26: 575-583.
66. Rouau X, Cheynier V, Surget A, Gloux D, Barron C, Meudec E, Louis-Montero J & Criton M (2003) A dehydrotrimer of ferulic acid from maize bran. Phytochemistry 63: 899-903.
67. Takabe K, Takeuchi M, Sato T, Ito M & Fujita M (2001) Immunocytochemical localization of enzymes involved in lignification of the cell wall. J. Plant Res. 114: 509-515.
68. Takahama U & Oniki T (1992). Regulation of peroxidase-dependent oxidation of phenolics in the apoplast of spinach leaves by ascorbate. Plant Cell Physiol. 33: 379-387.
69. Takeda T & Fry SC (2004) Control of xyloglucan endotransglucosylase activity by salts and anionic polymers. Planta, in press.
70. Tan K-S, Hoson T, Masuda Y & Kamisaka S (1991) Correlation between cell wall extensibility and the content of diferulic and ferulic acids in cell walls of Oryza sativa coleoptiles grown under water and in air. Physiol. Plant. 83: 397-403.
71. Tan K-S, Hoson T, Masuda Y & Kamisaka S (1992) Involvement of cell wall-bound diferulic acid in light-induced decrease in growth rate and cell wall extensibility of Oryza coleoptiles. Plant Cell Physiol. 33: 103-108.
72. Wakabayashi K, Hoson T & Kamisaka S (1997) Suppression of cell wall stiffening along coleoptiles of wheat (Triticum aestivum L.) seedlings grown under osmotic stress conditions. J. Plant Res. 110: 311-316.
73. Waldron KW, Parr AJ, Ng A & Ralph J (1996) Cell wall esterified phenolic dimers: identification and quantitation by reverse phase high performance liquid chromatography and diode array detection. Phytochem. Anal. 7: 305-312.
74. Waldron KW, Ng A, Parker ML & Parr AJ (1997) Ferulic acid dehydrodimers in the cell walls of Beta vulgaris and their possible role in texture. J. Sci. Food Agric. 74: 221-228.
75. Wallace G & Fry SC (1995) In-vitro peroxidase-catalysed oxidation of ferulic acid esters. Phytochemistry 39: 1293-1299.
76. Wallace G & Fry SC (1999) Action of diverse peroxidases and laccases on six cell wall-related phenolic compounds. Phytochemistry 52: 769-773.
77. Wang LH & Lin CH (1992) The effect of paclobutrazol on physiological and biochemical changes in the primary roots of pea. J. Exp. Bot. 43: 1367-1372.
78. Warneck HM, Haug T & Seitz HU (1996) Activation of cell wall-associated peroxidase isoenzymes in pea epicotyls by a xyloglucan-derived nonasaccharide. J. Exp. Bot. 47: 1897-1904.
79. Wende G & Fry SC (1997) O-Feruloylated, O-acetylated oligosaccharides as side-chains of grass xylans. Phytochemistry 44: 1011-1018.
80. Wende G, Waldron KW, Smith AC & Brett CT (1999) Developmental changes in cell-wall ferulate and dehydrodiferulates in sugar beet. Phytochemistry 52, 819-827.
81. Wojtaszek P, Trethowan J & Bolwell GP (1995) Specificity in the immobilization of cell wall proteins in response to different elicitor molecules in suspension-cultured cells of French bean (Phaseolus vulgaris L.). Plant Molec. Biol. 28: 1075-1087.
82. Yoshida-Shimokawa T, Yoshida S, Kakegawa K & Ishii T (2001) Enzymic feruloylation of arabinoxylan-trisaccharide by feruloyl-CoA : arabinoxylan-trisaccharide O-hydroxycinnamoyltransferase from Oryza sativa. Planta 212: 470-474.