Abstract
Globe artichoke represents a natural source of phenolic compounds with dicaffeoylquinic acids along with their biosynthetic precursor chlorogenic acid (5-caffeoylquinic acid) as the predominant molecules. We report the isolation and characterization of a full-length cDNA and promoter of a globe artichoke p-coumaroyl ester 3′-hydroxylase (CYP98A49), which is involved in both chlorogenic acid and lignin biosynthesis. Phylogenetic analyses demonstrated that this gene belongs to the CYP98 family. CYP98A49 was also heterologously expressed in yeast, in order to perform an enzymatic assay with p-coumaroylshikimate and p-coumaroylquinate as substrates. Real Time quantitative PCR analysis revealed that CYP98A49 expression is induced upon exposure to UV-C radiation. A single nucleotide polymorphism in the CYP98A49 gene sequence of two globe artichoke varieties used for genetic mapping allowed the localization of this gene to linkage group 10 within the previously developed maps.
Similar content being viewed by others
References
Abdulrazzak N, Pollet B, Ehlting J, Larsen K, Asnaghi C, Ronseau S, Proux C, Erhardt M, Seltzer V, Renou J, Ullman P, Pauly M, Lapierre C, Werck-Reichhart D (2006) A coumaroyl-ester-3-hydroxylase insertion mutant reveals the existence of non redundant meta-hydroxylation pathways and essential roles for phenolic precursors in cell expansion and plant growth. Plant Physiol 140:30–48. doi:10.1104/pp.105.069690
Adzet T, Camarassa J, Laguna CJ (1987) Hepatoprotective activity of polyphenolic compounds from Cynara scolymus against CCl4 toxicity in isolated rat hepatocytes. J Nat Prod 50:612–617
Basson A, Dubery I (2007) Identification of a cytochrome P450 cDNA (CYP98A5) from Phaseolus vulgaris, inducible by 3, 5-dichlorosalicylic acid and 2, 6-dichloro isonicotinic acid. J Plant Physiol 164:421–428. doi:10.1016/j.jplph.2006.02.006
Boudet A (2007) Evolution and current status of research in phenolic compounds. Phytochemistry 68:2722–2735. doi:10.1016/j.phytochem.2007.06.012
Brown J, Rice-Evans C (1998) Luteolin-rich artichoke extract protects low density lipoprotein from oxidation in vitro. Free Radic Res 29:247–255. doi:10.1080/10715769800300281
Cantos E, Espin J, Tomas-Barberan F (2001) Effect of wounding on phenolic enzymes in six minimally processed lettuce cultivars upon storage. J Agric Food Chem 49:322–330. doi:10.1021/jf000644
Chen F, Dixon R (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25:759–761. doi:10.1038/nbt1316
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. doi:10.1186/1471-2229-7-14
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 artichoke chlorogenic acid pathway. BMC Plant Biol 9
Paolis De, Pignone D, Morgese A, Sonnante G (2008) Characterization and differential expression analysis of artichoke phenylalanine ammonia-lyase-coding sequences. Physiol Plant 132:33–43. doi:10.1111/j.1399-3054.2007.00996.x
Dixon R, Paiva N (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097
Douglas C (1996) Phenylpropanoid metabolism and lignin biosynthesis: from weeds to trees. Trends Plant Sci 1:171–178. doi:10.1016/1360-1385(96)10019-4
Franke R, Humphreys J, Hemm M, Denault J, Ruegger M, Cusumano J, Chapple C (2002) The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism. Plant J 30:33–45. doi:10.1046/j.1365-313X.2002.01266.x
Gebhardt R (1997) Antioxidative and protective properties of extracts from leaves of the artichoke (Cynara scolymus L) against hydroperoxide-induced oxidative stress in cultured rat hepatocytes. Toxicol Appl Pharmacol 144:279–286. doi:10.1006/taap.1997.8130
Gebhardt R (1998) Inhibition of cholesterol biosynthesis in primary cultured rat hepatocytes by artichoke (Cynara scolymus L.) extracts. J Pharmacol Exp Ther 286:1122–1128
Gietz R, Woods R (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350:87–96
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. doi:10.1074/jbc.M209362200
Izaguirre M, Mazza C, Svatos A, Baldwin I, Ballare C (2007) Solar ultraviolet-B radiation and insect herbivory trigger partially overlapping phenolic responses in Nicotiana attenuata and Nicotiana longiflora. Ann Bot 99:103–109. doi:10.1093/aob/mcl226
Keurentjes J, Fu J, de Vos C, Lommen A, Hall R, Bino R, van der Plas L, Jansen R, Vreugdenhil D, Koornneef M (2006) The genetics of plant metabolism. Nat genet 38:842–849. doi:10.1038/ng0706-737
Kosambi D (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
Kühnl T, Koch U, Heller W, Wellmann E (1987) Chlorogenic acid biosynthesis: characterization of a light-induced microsomal 5-O-(4-coumaroyl)-d-quinate/shikimate 3′-hydroxylase from carrot (Daucus carota L.) cell suspension cultures. Arch Biochem Biophys 258:226–232. doi:10.1016/0003-9861(87)90339-0
Lanteri S, di Leo I, Ledda L, Mameli M, Portis E (2001) RAPD variation within and among populations of globe artichoke cultivar “Spinoso sardo”. Plant Breed 120:243–246. doi:10.1111/j.1439-0523.2001.tb01994.x
Lanteri S, Acquadro A, Comino C, Mauro R, Mauromicale G, Portis E (2006) A first linkage map of globe artichoke (Cynara cardunculus var. scolymus L.) based on AFLP, S-SAP, M-AFLP and microsatellite markers. Theor Appl Genet 112:1532–1542. doi:10.1007/s00122-006-0256-8
Lattanzio V, Cardinali A, Di Venere D, Linsalata V, Palmieri S (1994) Browning phenomena in stored artichoke (Cynara scolymus L.) heads: enzymic or chemical reactions? Food Chem 50:1–7
Mahesh V, Million-Rousseau R, Ullmann P, Chabrillange N, Bustamante J, Mondolot L, Morant M, Noirot M, Hamon S, de Kochko A, Werck-Reichhart D, Campa C (2007) Functional characterization of two p-coumaroyl ester 3′-hydroxylase genes from coffee tree: evidence of a candidate for chlorogenic acid biosynthesis. Plant Mol Biol 64:145–159. doi:10.1007/s11103-007-9141-3
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. doi:10.1021/jf801653w
Morant M, Hehn A, Werck-Reichhart D (2002) Conservation and diversity of gene families explored using the CODEHOP strategy in higher plants. BMC Plant Biol 2:7. doi:10.1186/1471-2229-2-7
Morant M, Schoch GA, Ullmann P, Ertunç T, Little D, Olsen CE, Petersen M, Negrel J, Werck-Reichhart D (2007) Catalytic activity, duplication and evolution of the CYP98 cytochrome P450 family in wheat. Plant Mol Biol 63:1–19. doi:10.1007/s11103-006-9028-8
Narusaka M, Narusaka Y, Seki M, Umezawa T, Ishida J, Nakajima M, Enju A, Shinozaki K (2004) Crosstalk in the responses to biotic and abiotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol 55:327–342. doi:10.1007/s11103-004-0685-1
Niggeweg R, Michael A, Martin C (2004) Engineering plants with increased levels of the antioxidant chlorogenic acid. Nat Biotechnol 22:746–754. doi:10.1038/nbt966
Pompon D, Louerat B, Bronine A, Urban P (1996) Yeast expression of animal and plant P450s in optimized redox environments. Methods Enzymol 272:51–64
Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichhart D (2001) CYP98A3 from Arabidopsis thaliana is a 3′-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J Biol Chem 276:36566–36574. doi:10.1074/jbc.M104047200
Schoch G, Morant M, Abdulrazzak N, Asnaghi C, Goepfert S, Petersen M, Ullmann P, Werck-Reichhart D (2006) The meta-hydroxylation step in the phenylpropanoid pathway: a new level of complexity in the pathway and its regulation. Environ Chem Lett 4:127–136. doi:10.1007/s10311-006-0062-1
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. doi:10.1016/S0040-4039(01)00448-8
Stam P, Van Ooijen J (1995) JoinMap version 2.0: software for the calculation of genetic linkage maps. CPRO-DLO, Wageningen
Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol 7:581–591. doi:10.1055/s-2005-873009
Urban P, Mignotte C, Kazmaier M, Delorme F, Pompon D (1997) Cloning, yeast expression, and characterization of the coupling of two distantly related Arabidopsis thaliana NADPH-cytochrome P450 reductases with P450 CYP73A5. J Biol Chem 272:19176–19186
Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wang M, Simon J, Aviles I, He K, Zheng Q, Tadmor Y (2003) Analysis of antioxidative phenolic compounds in artichoke (Cynara scolymus L.). J Agric Food Chem 51:601–608. doi:10.1021/jf020792bS0021-8561(02)00792-6
Weeden N (1994) Approaches to mapping in horticultural crops. In: Gresshoff PM (ed) Plant genome analysis. CRC, Boca Raton, pp 51–60
Ye S, Dhillon S, Ke X, Collins A, Day I (2001) An efficient procedure for genotyping single nucleotide polymorphisms. Nucleic Acid Res 29:E88-8
Acknowledgments
The authors kindly thank Harry Jonker (PRI) for his excellent technical assistance. The authors kindly thank Dr. Ullmann (Université Louis Pasteur, Strasbourg) for providing the substrates of the reaction, p-coumaroylquinate and p-coumaroylshikimate and for critical reading of the paper. The authors kindly thank Dr Nelson for providing CYP number to the new gene. The authors kindly thank Prof G. Mauromicale and Dr R. Mauro for providing plant material. Andrea Moglia acknowledges MIUR, for its financial support. Jules Beekwilder was financially supported by the EU 6th Frame FLORA project (2005-FOOD-CT-01730). Ric C. H. De Vos acknowledges initial support from the Centre for BioSystems Genomics, an initiative under the auspices of the Netherlands Genomics Initiative (NGI/NWO).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by H. Judelson.
Nucleotide sequence data reported are available in the GenBank database under accession number: FJ225121
Rights and permissions
About this article
Cite this article
Moglia, A., Comino, C., Portis, E. et al. Isolation and mapping of a C3′H gene (CYP98A49) from globe artichoke, and its expression upon UV-C stress. Plant Cell Rep 28, 963–974 (2009). https://doi.org/10.1007/s00299-009-0695-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-009-0695-1