Characterization of a multifunctional caffeoyl-CoA O-methyltransferase activated in grape berries upon drought stress

Plant Physiology and Biochemistry

Volumn 101, Issue , 2016, Pages 23-32

  Giordano, Debora ^a   Provenzano, Sofia ^a   Ferrandino, Alessandra ^a   Vitali, Marco ^a   Pagliarani, Chiara ^a   Roman, Federica ^a   Cardinale, Francesca ^a   Castellarin, Simone D ^b   Schubert, Andrea ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Anthocyanins; Berry ripening; Botrytis cinerea; Drought stress; Grapevine; O methyltransferases

Indexed keywords

ANTHOCYANIN; CAFFEOYL-COA O-METHYLTRANSFERASE; METHYLTRANSFERASE; PLANT PROTEIN;

BIOSYNTHESIS; ENZYMOLOGY; FRUIT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHYLATION; PHYSIOLOGICAL STRESS; VITIS;

ANTHOCYANINS; FRUIT; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; METHYLATION; METHYLTRANSFERASES; PLANT PROTEINS; STRESS, PHYSIOLOGICAL; VITIS;

EID: 84956681091     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2016.01.015     Document Type: Article

References (60)

1. Adams D.O. Phenolics and ripening in grape berries. Am. J. Enol. Vitic. 2006, 57:249-256.
2. Ageorges A., Fernandez L., Vialet S., Merdinoglu D., Terrier N., Romieu C. Four specific isogenes of the anthocyanin metabolic pathway are systematically co-expressed with the red colour of grape berries. Plant Sci. 2006, 170:372-383.
3. Bezier A., Lambert B., Baillieul F. Study of defense-related gene expression in grapevine leaves and berries infected with Botrytis cinerea. Eur. J. Plant Pathol. 2002, 108:111-120.
4. Bhuiyan N., Selvaraj G., Wei Y., King J. Gene expression profiling and silencing reveal that monolignol biosynthesis plays a critical role in penetration defence in wheat against powdery mildew invasion. J. Exp. Bot. 2009, 60:509-521.
5. Boss P.K., Davies C., Robinson S.P. Analysis of the expression of anthocyanin pathway genes in developing Vitis vinifera L. cv Shiraz grape berries and the implications for pathway regulation. Plant Physiol. 1996, 111:1059-1066.
6. Busam G., Junghanns K.T., Kneusel R.E., Kassemeyer H.H., Matern U. Characterization and expression of caffeoyl-coenzyme A 3-O-methyltransferase proposed for the induced resistance response of Vitis vinifera L. Plant Physiol. 1997, 115:1039-1048.
7. Carra A., Gambino G., Schubert A. A cetyltrimethylammonium bromide-based method to extract low-molecular-weight RNA from polysaccharide-rich plant tissues. Anal. Biochem. 2007, 360:318-320.
8. Castellarin S.D., Pfeiffer A., Sivilotti P., Degan M., Peterlunger E., Di Gaspero G. Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ. 2007, 30:1381-1399.
9. Castellarin S.D., Matthews M.A., Di Gaspero G., Gambetta G.A. Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta 2007, 227:101-112.
10. Chalker-Scott L. Environmental significance of anthocyanins in plant stress responses. Photochem. Photobiol. 1999, 70:1-9.
11. Chaves M.M., Zarrouk O., Francisco R., Costa J.M., Santos T., Regalado A.P., Rodrigues M.L., Lopes C.M. Grapevine under deficit irrigation: hints from physiological and molecular data. Ann. Bot. 2010, 105:661-676.
12. Chitarra W., Balestrini R., Vitali M., Pagliarani C., Perrone I., Schubert A., Lovisolo C. Gene expression in vessel-associated cells upon xylem embolism repair in Vitis vinifera L. petioles. Planta 2014, 239:887-899.
13. Cramer G.R., Ergul A., Grimplet J., Tillett R.L., Tattersall E.A.R., Bohlman M.C., Vincent D., Sonderegger J., Evans J., Osborne C., et al. Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct. Integr. Genom. 2007, 7:111-134.
14. Davies C., Boss P.K., Robinson S.P. Treatment of grape berries, a nonclimacteric fruit with a synthetic auxin, retards ripening and alters the expression of developmentally regulated genes. Plant Physiol. 1997, 115:1155-1161.
15. Day A., Neutelings G., Nolin F., Grec S., Habrant A., Cronier D., Maher B., Rolando C., David H., Chabbert B., et al. Caffeoyl coenzyme A O-methyltransferase down-regulation is associated with modifications in lignin and cell-wall architecture in flax secondary xylem. Plant Physiol. Biochem. 2009, 47:9-19.
16. Deluc L.G., Quilici D.R., Decendit A., Grimplet J., Wheatley M.D., Schlauch K.A., Mérillon J.M., Cushman J.C., Cramer G.R. Water deficit alters differentially metabolic pathways affecting important flavor and quality traits in grape berries of Cabernet Sauvignon and Chardonnay. BMC Genomics 2009, 10:212.
17. Do C.T., Pollet B., Thévenin J., Sibout R., Denoue D., Barrière Y., Lapierre C., Jouanin L. Both caffeoyl Coenzyme A 3-O-methyltransferase 1 and caffeic acid O-methyltransferase 1 are involved in redundant functions for lignin, flavonoids and sinapoyl malate biosynthesis in Arabidopsis. Planta 2007, 226:1117-1129.
18. Downey M.O., Harvey J.S., Robinson S.P. Synthesis of flavonols and expression of flavonol synthase genes in the developing grape berries of Shiraz and Chardonnay. Aust. J. Grape Wine Res. 2003, 9:110-121.
19. Ferrandino A., Carra A., Rolle L., Schneider A., Schubert A. Profiling of hydroxycinnamoyl tartrates and acylated anthocyanins in the skin of 34 Vitis vinifera genotypes. J. Agric. Food Chem. 2012, 60:4931-4945.
20. Ferrandino A., Lovisolo C. Abiotic stress effects on grapevine (Vitis vinifera L.): focus on abscisic acid-mediated consequences on secondary metabolism and berry quality. Environ. Exp. Bot. 2014, 103:138-147.
21. Ferrer J., Zubieta H., Dixon R., Noel J. Crystal structures of alfalfa caffeoyl coenzyme A 3-O-methyltransferase. Plant Physiol. 2005, 137:1009-1017.
22. Ford C.M., Boss P.K., Hoj P.B. Cloning and characterization of Vitis vinifera UDP-glucose:flavonoid 3-O-glucosyltransferase, a homologue of the enzyme encoded by the maize Bronze-1 locus that may primarily serve to glucosylate anthocyanidins in vivo. J. Biol. Chem. 1998, 273:9224-9233.
23. Fournier-Level A., Hugueney P., Verries C., This P., Ageorges A. Genetic mechanisms underlying the methylation level of anthocyanins in grape (Vitis vinifera L.). BMC Plant Biol. 2011, 11:179.
24. Frick S., Kutchan T.M. Molecular cloning and functional expression of O-methyltransferases common to isoquinoline alkaloid and phenylpropanoid biosynthesis. Plant J. Cell Mol. Biol. 1999, 17:329-339.
25. Gambetta G., Matthews M., Shaghasi T., McElrone A., Castellarin S. Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape. Planta 2010, 232:219-234.
26. Gambino G., Perrone I., Gribaudo I. A rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochem. Anal. 2008, 19:520-525.
27. Grimplet J., Deluc L.G., Tillett R.L., Wheatley M.D., Schlauch K.A., Cramer G.R., Cushman J.C. Tissue-specific mRNA expression profiling in grape berry tissues. BMC Genom. 2007, 8:187.
28. Gutha L.R., Casassa L.F., Harbertson J.F., Naidu R.A. Modulation of flavonoid biosynthetic pathway genes and anthocyanins due to virus infection in grapevine (Vitis vinifera L.) leaves. BMC Plant Biol. 2010, 10:187.
29. Harborne J.B., Williams C.A. Advances in flavonoid research since 1992. Phytochemistry 2000, 55:481-504.
30. Hochberg U., Degu A., Fait A., Rachmilevitch S. Near isohydric grapevine cultivar displays higher photosynthetic efficiency and photorespiration rates under drought stress as compared with near anisohydric grapevine cultivar. Physiol. Plant. 2013, 147:443-452.
31. Hugueney P., Provenzano S., Verries C., Ferrandino A., Meudec E., Batelli G., Merdinoglu D., Cheynier V., Schubert A., Ageorges A. A novel cation-dependent O-methyltransferase involved in anthocyanin methylation in grapevine. Plant Physiol. 2009, 150:2057-2070.
32. Ibdah M., Zhang X.H., Schmidt J., Vogt T. A novel Mg(2+)-dependent O-methyltransferase in the phenylpropanoid metabolism of Mesembryanthemum crystallinum. J. Biol. Chem. 2003, 278:43961-43972.
33. Ibrahim R.K., Bruneau A., Bantignies B. Plant O-methyltransferases: molecular analysis, common signature and classification. Plant Mol. Biol. 1998, 36:1-10.
34. Inoue K., Sewalt V.J., Murray G.B., Ni W., Stürzer C., Dixon R.A. Developmental expression and substrate specificities of alfalfa caffeic acid 3-O-methyltransferase and caffeoyl coenzyme A 3-O-methyltransferase in relation to lignification. Plant Physiol. 1998, 117:761-770.
35. Jeong S., Goto-Yamamoto N., Kobayashi S., Esaka A. Effects of plant hormones and shading on the accumulation of anthocyanins and the expression of anthocyanin biosynthetic genes in grape berry skins. Plant Sci. 2004, 167:247-252.
36. Joshi C.P., Chiang V.L. Conserved sequence motifs in plant S-adenosyl-L-methionine-dependent methyltransferases. Plant Mol. Biol. 1998, 37:663-674.
37. Kai K., Mizutani M., Kawamura N., Yamamoto R., Tamai M., Yamaguchi H., Sakata K., Shimizu B. Scopoletin is biosynthesized via ortho-hydroxylation of feruloyl CoA by a 2-oxoglutarate-dependent dioxygenase in Arabidopsis thaliana. Plant J. Cell Mol. Biol. 2008, 55:989-999.
38. Lam K.C., Ibrahim R.K., Behdad B., Dayanandan S. Structure, function, and evolution of plant O-methyltransferases. Genome 2007, 50:1001-1013.
39. Lee Y., Kim B., Chong Y., Lim Y., Ahn J. Cation dependent O-methyltransferases from rice. Planta 2008, 227:641-647.
40. Li L., Osakabe Y., Joshi C.P., Chiang V.L. Secondary xylem-specific expression of caffeoyl-coenzyme A 3-O-methyltransferase plays an important role in the methylation pathway associated with lignin biosynthesis in loblolly pine. Plant Mol. Biol. 1999, 40:555-565.
41. Loreti E., Povero G., Novi G., Solfanelli C., Alpi A., Perata P. Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol. 2008, 179:1004-1016.
42. Lücker J., Martens S., Lund S.T. Characterization of a Vitis vinifera cv. Cabernet Sauvignon 3',5'-O-methyltransferase showing strong preference for anthocyanins and glycosylated flavonols. Phytochemistry 2010, 71:1474-1484.
43. Margaria P., Ferrandino A., Caciagli P., Kedrina O., Schubert A., Palmano S. Metabolic and transcript analysis of the flavonoid pathway in diseased and recovered Nebbiolo and Barbera grapevines (Vitis vinifera L.) following infection by Flavescence doree phytoplasma. Plant Cell Environ. 2014, 37:2183-2200.
44. Martz F., Maury S., Pinçon G., Legrand M. cDNA cloning, substrate specificity and expression study of tobacco caffeoyl-CoA 3-O-methyltransferase, a lignin biosynthetic enzyme. Plant Mol. Biol. 1998, 36:427-437.
45. Mattivi F., Guzzon R., Vrhovsek U., Stefanini M., Velasco R. Metabolite profiling of grape: flavonols and anthocyanins. J. Agric. Food Chem. 2006, 54:7692-7702.
46. Meyermans H., Morreel K., Lapierre C., Pollet B., De Bruyn A., Busson R., Herdewijn P., Devreese B., Van Beeumen J., Marita J.M., et al. Modifications in lignin and accumulation of phenolic glucosides in poplar xylem upon down-regulation of caffeoyl-coenzyme A O-methyltransferase, an enzyme involved in lignin biosynthesis. J. Biol. Chem. 2000, 275:36899-36909.
47. Nakabayashi R., Mori T., Saito K. Alternation of flavonoid accumulation under drought stress in Arabidopsis thaliana. Plant Signal. Behav. 2014, 9:e29518.
48. NDong C., Anzellotti D., Ibrahim R.K., Huner N.P., Sarhan F. Daphnetin methylation by a novel O-methyltransferase is associated with cold acclimation and photosystem II excitation pressure in rye. J. Biol. Chem. 2003, 278:6854-6861.
49. Noel J., Dixon R., Pichersky E., Zubieta C., Ferrer J. Structural, functional and evolutionary bases for methylation of plant small molecules. Archives of Biochemistry and Biophysics 2003, 37-58. Elsevier Science, Oxford UK. J. Romeo (Ed.).
50. Perrone I., Pagliarani C., Lovisolo C., Chitarra W., Roman F., Schubert A. Recovery from water stress affects grape leaf petiole transcriptome. Planta 2012, 235:1383-1396.
51. Pirie A., Mullins M.G. Changes in anthocyanin and phenolics content of grapevine leaf and fruit tissues treated with sucrose, nitrate, and abscisic acid. Plant Physiol. 1976, 58:468-472.
52. Prozil S., Evtuguin D., Silva A., Lopes L. Structural characterization of lignin from grape stalks (Vitis vinifera L.). J. Agric. Food Chem. 2014, 62:5420-5428.
53. Rautengarten C., Baidoo E., Keasling J.D., Vibe Scheller H. A simple method for enzymatic synthesis of unlabeled and radiolabeled hydroxycinnamate-CoA. BioEnergy Res. 2010, 3:115-122.
54. Rotter A., Camps C., Lohse M., Kappel C., Pilati S., Hren M., Stitt M., Coutos-Thévenot P., Moser C., Usadel B., et al. Gene expression profiling in susceptible interaction of grapevine with its fungal pathogen Eutypa lata: extending MapMan ontology for grapevine. BMC Plant Biol. 2009, 9:104.
55. Sarni P., Fulcrand H., Souillol V., Souquet J., Cheynier V. Mechanisms of anthocyanin degradation in grape must-like model solutions. J. Sci. Food Agric. 1995, 69:385-391.
56. Sperdouli I., Moustakas M. Interaction of proline, sugars, and anthocyanins during photosynthetic acclimation of Arabidopsis thaliana to drought stress. J. Plant Physiol. 2012, 169:577-585.
57. Tolia N., Joshua-Tor L. Strategies for protein coexpression in Escherichia coli. Nat. Methods 2006, 3:55-64.
58. Vannozzi A., Dry I., Fasoli M., Zenoni S., Lucchin M. Genome-wide analysis of the grapevine stilbene synthase multigenic family: genomic organization and expression profiles upon biotic and abiotic stresses. BMC Plant Biol. 2012, 12:130.
59. Yamaguchi-Shinozaki K., Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 2006, 57:781-803.
60. Yang Y., He M., Zhu Z., Li S., Xu Y., Zhang C., Singer S., Wang Y. Identification of the dehydrin gene family from grapevine species and analysis of their responsiveness to various forms of abiotic and biotic stress. BMC Plant Biol. 2012, 12:140.