Dual catalytic activity of hydroxycinnamoyl-coenzyme a quinate transferase from tomato allows it to moonlight in the synthesis of both mono- and dicaffeoylquinic acids

Plant Physiology

Volumn 166, Issue 4, 2014, Pages 1777-1787

  Moglia, Andrea ^a   Lanteri, Sergio ^a   Comino, Cinzia ^a   Hill, Lionel ^b   Knevitt, Daniel ^b   Cagliero, Cecilia ^a   Rubiolo, Patrizia ^a   Bornemann, Stephen ^b   Martin, Cathie ^b  

^a UNIVERSITY OF TURIN   (Italy)

^b JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LYCOPERSICON ESCULENTUM;

ACYLTRANSFERASE; CAFFEOYLQUINIC ACID; CHLOROGENIC ACID; COENZYME A; HYDROXYCINNAMOYL-COA-QUINATE TRANSFERASE; PLANT PROTEIN; QUINIC ACID; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; STRUCTURAL MODEL; TOMATO;

ACYLTRANSFERASES; AMINO ACID SEQUENCE; CHLOROGENIC ACID; COENZYME A; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; MODELS, STRUCTURAL; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; QUINIC ACID; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

EID: 84914170872     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.251371     Document Type: Article

References (42)

1. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
2. Chanforan C, Loonis M, Mora N, Caris-Veyrat C, Dufour C (2012) The impact of industrial processing on health-beneficial tomato microconstituents. Food Chem 134: 1786-1795.
3. Choi J, Park JK, Lee KT, Park KK, Kim WB, Lee JH, Jung HJ, Park HJ (2005) In vivo antihepatotoxic effects of Ligularia fischeri var. spiciformis and the identification of the active component, 3, 4-dicaffeoylquinic acid. J Med Food 8: 348-352.
4. Clifford M (1999) Chlorogenic acids and other cinnamates: nature, occurrence and dietary burden. J Sci Food Agric 79: 362-372.
5. Comino C, Hehn A, Moglia A, Menin B, Bourgaud F, Lanteri S, Portis E (2009) The isolation and mapping of a novel hydroxycinnamoyltransferase in the globe artichoke chlorogenic acid pathway. BMC Plant Biol 9: 30.
6. Comino C, Lanteri S, Portis E, Acquadro A, Romani A, Hehn A, Larbat R, Bourgaud F (2007) Isolation and functional characterization of a cDNA coding a hydroxycinnamoyltransferase involved in phenylpropanoid biosynthesis in Cynara cardunculus L. BMC Plant Biol 7: 14.
7. D'Auria JC (2006) Acyltransferases in plants: a good time to be BAHD. Curr Opin Plant Biol 9: 331-340.
8. Gu R, Dou G, Wang J, Dong J, Meng Z (2007) Simultaneous determination of 1, 5-dicaffeoylquinic acid and its active metabolites in human plasma by liquid chromatography-tandem mass spectrometry for pharmacokinetic studies. J Chromatogr B Analyt Technol Biomed Life Sci 852: 85-91.
9. Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
10. Hoffmann L, Maury S, Martz F, Geoffroy P, Legrand M (2003) Purification, cloning, and properties of an acyltransferase controlling shikimate and quinate ester intermediates in phenylpropanoid metabolism. J Biol Chem 278: 95-103.
11. Hunter PR, Craddock CP, Di Benedetto S, Roberts LM, Frigerio L (2007) Fluorescent reporter proteins for the tonoplast and the vacuolar lumen identify a single vacuolar compartment in Arabidopsis cells. Plant Physiol 145: 1371-1382.
12. Islam S (2006) Sweetpotato (Ipomoea batatas L.) leaf: its potential effect on human health and nutrition. J Food Sci 71: R13-R21.
13. Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacteriummediated plant transformation. Trends Plant Sci 7: 193-195.
14. Kaul A, Khanduja KL (1998) Polyphenols inhibit promotional phase of tumorigenesis: relevance of superoxide radicals. Nutr Cancer 32: 81-85.
15. Lallemand LA, Zubieta C, Lee SG, Wang Y, Acajjaoui S, Timmins J, McSweeney S, Jez JM, McCarthy JG, McCarthy AA (2012) A structural basis for the biosynthesis of the major chlorogenic acids found in coffee. Plant Physiol 160: 249-260.
16. Lepelley M, Cheminade G, Tremillon N, Simkin A, Caillet V, McCarthy J (2007) Chlorogenic acid synthesis in coffee: an analysis of CGA content and real-time RT-PCR expression of HCT, HQT, C3H1, and CCoAOMT1 genes during grain development in C. canephora. Plant Sci 172: 978-996.
17. Luo J, Butelli E, Hill L, Parr A, Niggeweg R, Bailey P, Weisshaar B, Martin C (2008) AtMYB12 regulates caffeoyl quinic acid and flavonol synthesis in tomato: expression in fruit results in very high levels of both types of polyphenol. Plant J 56: 316-326.
18. Mahesh V, Million-Rousseau R, Ullmann P, Chabrillange N, Bustamante J, Mondolot L, Morant M, Noirot M, Hamon S, de Kochko A, et al (2007) Functional characterization of two p-coumaroyl ester 39-hydroxylase genes from coffee tree: evidence of a candidate for chlorogenic acid biosynthesis. Plant Mol Biol 64: 145-159.
19. Martin C, Butelli E, Petroni K, Tonelli C (2011) How can research on plants contribute to promoting human health? Plant Cell 23: 1685-1699.
20. Martin C, Zhang Y, Tonelli C, Petroni K (2013) Plants, diet, and health. Annu Rev Plant Biol 64: 19-46.
21. McDougall B, King PJ, Wu BW, Hostomsky Z, Reinecke MG, Robinson WE Jr (1998) Dicaffeoylquinic and dicaffeoyltartaric acids are selective inhibitors of human immunodeficiency virus type 1 integrase. Antimicrob Agents Chemother 42: 140-146.
22. Menin B, Comino C, Moglia A, Dolzhenko Y, Portis E, Lanteri S (2010) Identification and mapping of genes related to caffeoylquinic acid synthesis in Cynara cardunculus L. Plant Sci 179: 338-347.
23. Meyer A, Donovan J, Pearson D, Waterhouse A, Frankel E (1998) Fruit hydroxycinnamic acids inhibit human low-density lipoprotein oxidation in vitro. J Agric Food Chem 46: 1783-1787.
24. Moco S, Bino RJ, Vorst O, Verhoeven HA, de Groot J, van Beek TA, Vervoort J, de Vos CH (2006) A liquid chromatography-mass spectrometrybased metabolome database for tomato. Plant Physiol 141: 1205-1218.
25. Moco S, Capanoglu E, Tikunov Y, Bino RJ, Boyacioglu D, Hall RD, Vervoort J, De Vos RC (2007) Tissue specialization at the metabolite level is perceived during the development of tomato fruit. J Exp Bot 58: 4131-4146.
26. Moglia A, Comino C, Portis E, Acquadro A, De Vos RC, Beekwilder J, Lanteri S (2009) Isolation and mapping of a C39H gene (CYP98A49) from globe artichoke, and its expression upon UV-C stress. Plant Cell Rep 28: 963-974.
27. Moglia A, Lanteri S, Comino C, Acquadro A, de Vos R, Beekwilder J (2008) Stress-induced biosynthesis of dicaffeoylquinic acids in globe artichoke. J Agric Food Chem 56: 8641-8649.
28. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15: 473-478.
29. Niggeweg R, Michael AJ, Martin C (2004) Engineering plants with increased levels of the antioxidant chlorogenic acid. Nat Biotechnol 22: 746-754.
30. Peluso G, De Feo V, De Simone F, Bresciano E, Vuotto ML (1995) Studies on the inhibitory effects of caffeoylquinic acids on monocyte migration and superoxide ion production. J Nat Prod 58: 639-646.
31. Rice-Evans C, Miller NJ, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2: 152-159.
32. Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichhart D (2001) CYP98A3 from Arabidopsis thaliana is a 39-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J Biol Chem 276: 36566-36574.
33. Slanina J, Taborska E, Bochorakova H, Slaninova I, Humpa O, Robinson W, Schram K (2001) New and facile method of preparation of the anti-HIV-1 agent, 1, 3-dicaffeoylquinic acid. Tetrahedron Lett 42: 3383-3385.
34. Slimestad R, Verheul M (2009) Review of flavonoids and other phenolics from fruits of different tomato (Lycopersicon esculentum Mill.) cultivars. J Sci Food Agric 89: 1255-1270.
35. Sonnante G, D'Amore R, Blanco E, Pierri CL, De Palma M, Luo J, Tucci M, Martin C (2010) Novel hydroxycinnamoyl-coenzyme A quinate transferase genes from artichoke are involved in the synthesis of chlorogenic acid. Plant Physiol 153: 1224-1238.
36. Strack D, Gross W (1990) Properties and activity changes of chlorogenic acid: glucaric acid caffeoyltransferase from tomato (Lycopersicon esculentum). Plant Physiol 92: 41-47.
37. Teutschbein J, GrossW, Nimtz M, Milkowski C, Hause B, Strack D (2010) Identification and localization of a lipase-like acyltransferase in phenylpropanoid metabolism of tomato (Solanum lycopersicum). J Biol Chem 285: 38374-38381.
38. Vain P, Keen N, Murillo J, Rathus C, Nemes C, Finer J (1993) Development of the particle inflow gun. Plant Cell Tissue Organ Cult 33: 237-246.
39. Vallverdú-Queralt A, Odriozola-Serrano I, Oms-Oliu G, Lamuela-Raventós RM, Elez-Martínez P, Martín-Belloso O (2012) Changes in the polyphenol profile of tomato juices processed by pulsed electric fields. J Agric Food Chem 60: 9667-9672.
40. D-glucose. Quinate hydroxycinnamoyl transferase in the root of sweet potato, Ipomoea batatas Lam. J Biol Chem 261: 8729-8733.
41. Walker AM, Hayes RP, Youn B, Vermerris W, Sattler SE, Kang C (2013) Elucidation of the structure and reaction mechanism of sorghum hydroxycinnamoyltransferase and its structural relationship to other Coenzyme A-dependent transferases and synthases. Plant Physiol 162: 640-651.
42. Wang M, Simon JE, Aviles IF, He K, Zheng QY, Tadmor Y (2003) Analysis of antioxidative phenolic compounds in artichoke (Cynara scolymus L.). J Agric Food Chem 51: 601-608.