Genome-wide identification of bahd acyltransferases and in vivo characterization of HQT-like enzymes involved in caffeoylquinic acid synthesis in globe artichoke

Frontiers in Plant Science

Volumn 7, Issue September, 2016, Pages

  Moglia, Andrea ^a   Acquadro, Alberto ^a   Eljounaidi, Kaouthar ^a   Milani, Anna M ^a   Cagliero, Cecilia ^a   Rubiolo, Patrizia ^a   Genre, Andrea ^a   Cankar, Katarina ^b   Beekwilder, Jules ^b   Comino, Cinzia ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

BAHD acyltransferases; Caffeoylquinic acids; Cynara cardunculus; Functional characterization; VIGS

Indexed keywords

EID: 84988602948     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.01424     Document Type: Article

References (85)

1. Adzet, T., Camarassa, J., and Laguna, C. J. (1987). Hepatoprotective activity of polyphenolic compounds from Cynara scolymus against CCl4 toxicity in isolated rat hepatocytes. J. Nat. Prod. 50, 612-617. doi: 10.1021/np50052a004
2. Arakawa, T., Yamasaki, H., Ikeda, K., Ejima, D., Naito, T., and Koyama, A. (2009). Antiviral and virucidal activities of natural products. Curr. Med. Chem. 16, 2485-2497. doi: 10.2174/092986709788682065
3. Bai, S., Tuan, P., Tatsuki, M., Yaegaki, H., Ohmiya, A., Yamamizo, C., et al. (2016). Knockdown of carotenoid cleavage dioxygenase 4 (CCD4) via virus-induced gene silencing confers yellow coloration in peach fruit: evaluation of gene function related to fruit traits. Plant Mol. Biol. Rep. 34, 257-264. doi: 10.1007/s11105-015-0920-8
4. Barker, M., Kane, N., Matvienko, M., Kozik, A., Michelmore, W., Knapp, S., et al. (2008). Multiple paleopolyploidizations during the evolution of the Compositae reveal parallel patterns of duplicate gene retention after millions of years. Mol. Biol. Evol. 25, 2445-2455. doi: 10.1093/molbev/msn187
5. Baulcombe, D. (1999). Fast forward genetics based on virus-induced gene silencing. Curr. Opin. Plant Biol. 2, 109-113. doi: 10.1016/S1369-5266(99)80022-3
6. Brat, P., George, S., Bellamy, A., Du Chaffaut, L., Scalbert, A., Mennen, L., et al. (2006). Daily polyphenol intake in France from fruit and vegetables. J. Nutr. 136, 2368-2373.
7. Brown, J., and 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
8. Burch-Smith, T., Anderson, J., Martin, G., and Dinesh-Kumar, S. (2004). Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J. 39, 734-746. doi: 10.1111/j.1365-313X.2004.02158.x
9. Burhenne, K., Kristensen, B., and Rasmussen, S. (2003). A new class of N-hydroxycinnamoyltransferases - Purification, cloning, and expression of a barley agmatine coumaroyltransferase (Ec 2.3.1.64). J. Biol. Chem. 278, 13919-13927. doi: 10.1074/jbc.M213041200
10. Chen, J., Jiang, C., Gookin, T., Hunter, D., Clark, D., and Reid, M. (2004). Chalcone synthase as a reporter in virus-induced gene silencing studies of flower senescence. Plant Mol. Biol. 55, 521-530. doi: 10.1007/s11103-004-0590-7
11. Cle, C., Hill, L., Niggeweg, R., Martin, C., Guisez, Y., Prinsen, E., et al. (2008). Modulation of chlorogenic acid biosynthesis in Solanum lycopersicum; consequences for phenolic accumulation and UV-tolerance. Phytochemistry 69, 2149-2156. doi: 10.1016/j.phytochem.2008.04.024
12. Clifford, M. (2000). Chlorogenic acids and other cinnamates - nature, occurrence, dietary burden, absorption and metabolism. J. Sci. Food Agric. 80, 1033-1043. doi: 10.1002/(SICI)1097-0010(20000515)80:7<1033::AID-JSFA595>3.0.CO;2-T
13. Comino, C., Hehn, A., Moglia, A., Menin, B., Bourgaud, F., Lanteri, S., et al. (2009). The isolation and mapping of a novel hydroxycinnamoyltransferase in the globe artichoke chlorogenic acid pathway. BMC Plant Biol. 9:30. doi: 10.1186/1471-2229-9-30
14. Comino, C., Lanteri, S., Portis, E., Acquadro, A., Romani, A., Hehn, A., et al. (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
15. Coon, J., and Ernst, E. (2003). Herbs for serum cholesterol reduction: a systematic review. J. Fam. Pract. 52, 470-478.
16. D’Auria, J. (2006). Acyltransferases in plants: a good time to be BAHD. Curr. Opin. Plant Biol. 9, 331-340. doi: 10.1016/j.pbi.2006.03.016
17. Deng, X., Elomaa, P., Nguyen, C., Hytonen, T., Valkonen, J., and Teeri, T. (2012). Virus-induced gene silencing for Asteraceae-a reverse genetics approach for functional genomics in Gerbera hybrida. Plant Biotechnol. J. 10, 970-978. doi: 10.1111/j.1467-7652.2012.00726.x
18. Eljounaidi, K., Comino, C., Moglia, A., Cankar, K., Genre, A., Hehn, A., et al. (2015). Accumulation of cynaropicrin in globe artichoke and localization of enzymes involved in its biosynthesis. Plant Sci. 239, 128-136. doi: 10.1016/j.plantsci.2015.07.020
19. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. (2007). Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953-971. doi: 10.1038/nprot.2007.131
20. Eudes, A., Pereira, J., Yogiswara, S., Wang, G., Benites, V., Baidoo, E., et al. (2016). Exploiting the substrate promiscuity of hydroxycinnamoyl-Coa:shikimate hydroxycinnamoyl transferase to reduce lignin. Plant Cell Physiol. 57, 568-579. doi: 10.1093/pcp/pcw016
21. Fujiwara, H., Tanaka, Y., Yonekura-Sakakibara, K., Fukuchi-Mizutani, M., Nakao, M., Fukui, Y., et al. (1998). cDNA cloning, gene expression and subcellular localization of anthocyanin 5-aromatic acyltransferase from Gentiana triflora. Plant J. 16, 421-431. doi: 10.1046/j.1365-313x.1998.00312.x
22. Gaquerel, E., Kotkar, H., Onkokesung, N., Galis, I., and Baldwin, I. (2013). Silencing an N-acyltransferase-like involved in lignin biosynthesis in Nicotiana attenuata dramatically alters herbivory-induced phenolamide metabolism. PLoS ONE 8:e62336. doi: 10.1371/journal.pone.0062336
23. 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
24. Gebhardt, R. (2001). Anticholestatic activity of flavonoids from artichoke (Cynara scolymus L.) and of their metabolites. Med. Sci. Monit. 7, 316-320.
25. Gould, B., and Kramer, E. (2007). Virus-induced gene silencing as a tool for functional analyses in the emerging model plant Aquilegia (columbine, Ranunculaceae). Plant Methods 3:6. doi: 10.1186/1746-4811-3-6
26. Grienenberger, E., Besseau, S., Geoffroy, P., Debayle, D., Heintz, D., Lapierre, C., et al. (2009). A BAHD acyltransferase is expressed in the tapetum of Arabidopsis anthers and is involved in the synthesis of hydroxycinnamoyl spermidines. Plant J. 58, 246-259. doi: 10.1111/j.1365-313X.2008.03773.x
27. Halvorsen, B., Carlsen, M., Phillips, K., Bohn, S., Holte, K., Jacobs, D., et al. (2006). Content of redox-active compounds (i.e., antioxidants) in foods consumed in the United States. Am. J. Clin. Nutr. 84, 95-135.
28. Hileman, L., Drea, S., de Martino, G., Litt, A., and Irish, V. (2005). Virus-induced gene silencing is an effective tool for assaying gene function in the basal eudicot species Papaver somniferum (opium poppy). Plant J. 44, 334-341. doi: 10.1111/j.1365-313X.2005.02520.x
29. Hofberger, J., Lyons, E., Edger, P., Pires, J., and Schranz, M. (2013). Whole genome and tandem duplicate retention facilitated glucosinolate pathway diversification in the mustard family. Genome Biol. Evol. 5, 2155-2173. doi: 10.1093/gbe/evt162
30. Hoffmann, L., Besseau, S., Geoffroy, P., Ritzenthaler, C., Meyer, D., Lapierre, C., et al. (2004). Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. Plant Cell 16, 1446-1465. doi: 10.1105/tpc.020297
31. Hoffmann, L., Maury, S., Martz, F., Geoffroy, P., and 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
32. Jiang, Y., Ye, S., Wang, L., Duan, Y., Lu, W., Liu, H., et al. (2014). Heterologous gene silencing induced by tobacco rattle virus (TRV) is efficient for pursuing functional genomics studies in woody plants. Plant Cell Tissue Organ Cult. 116, 163-174. doi: 10.1007/s11240-013-0393-0
33. Karimi, M., Inze, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195. doi: 10.1016/S1360-1385(02)02251-3
34. Kim, S., Park, M., Yeom, S. I., Kim, Y. M., Min, L. J., Lee, H. A., et al. (2014). Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat. Genet. 46, 270-278. doi: 10.1038/ng.2877
35. Kumagai, M., Donson, J., Dellacioppa, G., Harvey, D., Hanley, K., and Grill, L. (1995). Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. Proc. Natl. Acad. Sci. U.S.A. 92, 1679-1683. doi: 10.1073/pnas.92.5.1679
36. Lallemand, L., Zubieta, C., Lee, S., Wang, Y., Acajjaoui, S., Timmins, J., et al. (2012). A structural basis for the biosynthesis of the major chlorogenic acids found in coffee. Plant Physiol. 160, 249-260. doi: 10.1104/pp.112.202051
37. Lattanzio, V., Cardinali, A., Di Venere, D., Linsalata, V., and Palmieri, S. (1994). Browning phenomena in stored artichoke (Cynara scolymus L.) heads: enzymic or chemical reactions?. Food Chem. 50, 1-7. doi: 10.1016/0308-8146(94)90083-3
38. Lattanzio, V., Kroon, P., Linsalata, V., and Cardinali, A. (2009). Globe artichoke: a functional food and source of nutraceutical ingredients. J. Funct. Foods 1, 131-144. doi: 10.1016/j.jff.2009.01.002
39. Legrand, G., Delporte, M., Khelifi, C., Harant, A., Vuylsteker, C., Morchen, M., et al. (2016). Identification and characterization of five BAHD acyltransferases involved in hydroxycinnamoyl ester metabolism in chicory. Front. Plant Sci. 7:741. doi: 10.3389/fpls.2016.00741
40. Lei, L., Zhou, S., Ma, H., and Zhang, L. (2012). Expansion and diversification of the SET domain gene family following whole-genome duplications in Populus trichocarpa. BMC Evol. Biol. 12:51. doi: 10.1186/1471-2148-12-51
41. Leiss, K., Maltese, F., Choi, Y., Verpoorte, R., and Klinkhamer, P. (2009). Identification of chlorogenic acid as a resistance factor for thrips in Chrysanthemum. Plant Physiol. 150, 1567-1575. doi: 10.1104/pp.109.138131
42. Li, X., Zhang, J., Wu, Z., Lai, B., Huang, X., Qin, Y., et al. (2016). Functional characterization of a glucosyltransferase gene, LcUFGT1, involved in the formation of cyanidin glucoside in the pericarp of Litchi chinensis. Physiol. Plant 156, 139-149. doi: 10.1111/ppl.12391
43. Liu, Y., Schiff, M., and Dinesh-Kumar, S. P. (2002). Virus-induced gene silencing in tomato. Plant J. 31, 777-786. doi: 10.1046/j.1365-313X.2002.01394.x
44. Lotfy, S., Javelle, F., and Negrel, J. (1995). Distribution of hydroxycinnamoyl-CoA: ω-hydroxypalmitic acid O-hydroxycinnamoyltransferase in higher plants. Phytochemistry 40, 389-391. doi: 10.1016/0031-9422(95)00284-e
45. Lotfy, S., Javelle, F., and Negrel, J. (1996). Purification and characterization of hydroxycinnamoyl-coenzyme A: ω-hydroxypalmitic acid from tobacco (Nicotiana tabacum L.) cell-suspension cultures. Planta 199, 475-480. doi: 10.1007/bf00195742
46. Mahesh, V., Million-Rousseau, R., Ullmann, P., Chabrillange, N., Bustamante, J., Mondolot, L., et al. (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
47. Markovic, S., and Tošovic, J. (2016). Comparative study of the antioxidative activities of caffeoylquinic and caffeic acids. Food Chem. 210, 585-592. doi: 10.1016/j.foodchem.2016.05.019
48. Menin, B., Comino, C., Moglia, A., Dolzhenko, Y., Portis, E., and Lanteri, S. (2010). Identification and mapping of genes related to caffeoylquinic acid synthesis in Cynara cardunculus L. Plant Sci. 179, 338-347. doi: 10.1016/j.plantsci.2010.06.010
49. Menin, B., Comino, C., Portis, E., Moglia, A., Cankar, K., Bouwmeester, H. J., et al. (2012). Genetic mapping and characterization of the globe artichoke (+)-germacrene A synthase gene, encoding the first dedicated enzyme for biosynthesis of the bitter sesquiterpene lactone cynaropicrin. Plant Sci. 190, 1-8. doi: 10.1016/j.plantsci.2012.03.006
50. Menin, B., Moglia, A., Comino, C., Hakkert, J., Lanteri, S., and Beekwilder, J. (2013). In vitro callus-induction in globe artichoke (Cynara cardunculus L. var. scolymus) as a system for the production of caffeoylquinic acids. J. Hortic. Sci. Biotechnol. 88, 537-542. doi: 10.1080/14620316.2013.11513003
51. Moglia, A., Comino, C., Lanteri, S., de Vos, R., de Waard, P., van Beek, T., et al. (2010). Production of novel antioxidative phenolic amides through heterologous expression of the plant’s chlorogenic acid biosynthesis genes in yeast. Metab. Eng. 12, 223-232. doi: 10.1016/j.ymben.2009.11.003
52. Moglia, A., Comino, C., Portis, E., Acquadro, A., De Vos, R., Beekwilder, J., et al. (2009). 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. doi: 10.1007/s00299-009-0695-1
53. Moglia, A., Lanteri, S., Comino, C., Hill, L., Knevitt, D., Cagliero, C., et al. (2014). 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 Physiol. 166, 1777-1787. doi: 10.1104/pp.114.251371
54. Molina, I., and Kosma, D. (2015). Role of HXXXD-motif/BAHD acyltransferases in the biosynthesis of extracellular lipids. Plant Cell Rep. 34, 587-601. doi: 10.1007/s00299-014-1721-5
55. Mullen, W., Nemzer, B., Ou, B., Stalmach, A., Hunter, J., Clifford, M., et al. (2011). The antioxidant and chlorogenic acid profiles of whole coffee fruits are influenced by the extraction procedures. J. Agric. Food Chem. 59, 3754-3762. doi: 10.1021/jf200122m
56. Negruk, V., Yang, P., Subramanian, M., McNevin, J., and Lemieux, B. (1996). Molecular cloning and characterization of the CER2 gene of Arabidopsis thaliana. Plant J. 9, 137-145. doi: 10.1046/j.1365-313X.1996.09020137.x
57. Niggeweg, R., Michael, A., and Martin, C. (2004). Engineering plants with increased levels of the antioxidant chlorogenic acid. Nat. Biotechnol. 22, 746-754. doi: 10.1038/nbt966
58. Ohno, S., Wolf, U., and Atkin, N. B. (1968). Evolution from fish to mammals by gene duplication. Hereditas 59, 169-187. doi: 10.1111/j.1601-5223.1968.tb02169.x
59. Payyavula, R., Shakya, R., Sengoda, V., Munyaneza, J., Swamy, P., and Navarre, D. (2015). Synthesis and regulation of chlorogenic acid in potato: rerouting phenylpropanoid flux in HQT-silenced lines. Plant Biotechnol. J. 13, 551-564. doi: 10.1111/pbi.12280
60. Puangpraphant, S., Berhow, M. A., Vermillion, K., Potts, G., and Gonzalez de Mejia, E. (2011). Dicaffeoylquinic acids in Yerba mate (Ilex paraguariensis St. Hilaire) inhibit NF-B κ nucleus translocation in macrophages and induce apoptosis by activating caspases-8 and -3 in human colon cancer cells. Mol. Nutr. Food Res. 55, 1509-1522. doi: 10.1002/mnfr.201100128
61. Ruiz, M., Voinnet, O., and Baulcombe, D. (1998). Initiation and maintenance of virus-induced gene silencing. Plant Cell 10, 937-946. doi: 10.1105/tpc.10.6.937
62. Sainsbury, F., Thuenemann, E. C., and Lomonossoff, G. P. (2009). pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol. J. 7, 682-693. doi: 10.1111/j.1467-7652.2009.00434.x
63. Sato, S., Tabata, S., Hirakawa, H., Asamizu, E., Shirasawa, K., Isobe, S., et al. (2012). The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635-641. doi: 10.1038/nature11119
64. Scaglione, D., Lanteri, S., Acquadro, A., Lai, Z., Knapp, S. J., Rieseberg, L., et al. (2012). Large-scale transcriptome characterization and mass discovery of SNPs in globe artichoke and its related taxa. Plant Biotechnol. J. 10, 956-969. doi: 10.1111/j.1467-7652.2012.00725.x
65. Scaglione, D., Reyes Chin Wo, S., Lanteri, S., Acquadro, A., Portis, E., Tirone, M., et al. (2014). "De novo genome assembly and ultra-dense mapping of artichoke, chicory and endive, and syntenic comparisons across the Compositae," in W205 Proceedings of the Plant and Animal Genome XXIInd Conference, San Diego, CA.
66. Scaglione, D., Reyes-Chin-Wo, S., Acquadro, A., Froenicke, L., Portis, E., Beitel, C., et al. (2016). The genome sequence of the outbreeding globe artichoke constructed de novo incorporating a phase-aware low-pass sequencing strategy of F-1 progeny. Sci. Rep. 6:19427. doi: 10.1038/srep19427
67. Schutz, K., Kammerer, D., Carle, R., and Schieber, A. (2004). Identification and quantification of caffeoylquinic acids and flavonolds from artichoke (Cynara scolymus L.) heads, juice, and pomace by HPLC-DAD-ESI/MSn. J. Agric. Food Chem. 52, 4090-4096. doi: 10.1021/jf049625x
68. Senthil-Kumar, M., and Mysore, K. (2014). Tobacco rattle virus-based virus- induced gene silencing in Nicotiana benthamiana. Nat. Protoc. 9, 1549-1562. doi: 10.1038/nprot.2014.092
69. Singh, A., Dwivedi, V., Rai, A., Pal, S., Reddy, S., Rao, D., et al. (2015). Virus-induced gene silencing of Withania somnifera squalene synthase negatively regulates sterol and defence-related genes resulting in reduced withanolides and biotic stress tolerance. Plant Biotechnol. J. 13, 1287-1299. doi: 10.1111/pbi.12347
70. Small, I., Peeters, N., Legeai, F., and Lurin, C. (2004). Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4, 1581-1590. doi: 10.1002/pmic.200300776
71. Sonnante, G., D’Amore, R., Blanco, E., Pierri, C. L., De Palma, M., Luo, J., et al. (2010). Novel hydroxycinnamoyl-coenzyme A quinate transferase genes from artichoke are involved in the synthesis of chlorogenic acid. Plant Physiol. 153, 1224-1238. doi: 10.1104/pp.109.150144
72. St-Pierre, B., and De Luca, V. (2000). "Evolution of acyltransferase genes: origin and diversification of the BAHD superfamily of acyltransferases involved in secondary metabolism," in Recent Advances in Phytochemistry, eds J. T. Romeo, R. Ibrahim, L. Varin, and V. De Luca (Amsterdam: Elsevier), 285-315. doi: 10.1016/S0079-9920(00)80010-6
73. Suzuki, H., Nakayama, T., Yonekura-Sakakibara, K., Fukui, Y., Nakamura, N., Yamaguchi, M., et al. (2002). cDNA cloning, heterologous expressions, and functional characterization of malonyl-coenzyme a:anthocyanidin 3-o- glucoside-6"-o-malonyltransferase from dahlia flowers. Plant Physiol. 130, 2142-2151. doi: 10.1104/pp.010447
74. Tacke, E., Korfhage, C., Michel, D., Maddaloni, M., Motto, M., Lanzini, S., et al. (1995). Transposon tagging of the maize Glossy2 locus with the transposable element En/Spm. Plant J. 8, 907-917. doi: 10.1046/j.1365-313X.1995.8060907.x
75. Tuominen, L., Johnson, V., and Tsai, C. (2011). Differential phylogenetic expansions in BAHD acyltransferases across five angiosperm taxa and evidence of divergent expression among Populus paralogues. BMC Genomics 12:236. doi: 10.1186/1471-2164-12-236
76. Ulbrich, B., and Zenk, M. (1979). Partial purification and properties of p-hydroxycinnamoyl-CoA:quinate hydroxycinnamoyl transferase from higher plants. Phytochemistry 18, 929-933. doi: 10.1016/S0031-9422(00)83782-6
77. Vanholme, B., Cesarino, I., Goeminne, G., Kim, H., Marroni, F., Van Acker, R., et al. (2013). Breeding with rare defective alleles (BRDA): a natural Populus nigra HCT mutant with modified lignin as a case study. New Phytol. 198, 765-776. doi: 10.1111/nph.12179
78. Villegas, R., and Kojima, M. (1986). Purification and characterization of hydroxycinnamoyl D-glucose: quinate hydroxycinnamoyl transferase in the root of sweet potato, Ipomoea batatas Lam. J. Biol. Chem. 261, 8729-8733.
79. Wagner, A., Ralph, J., Akiyama, T., Flint, H., Phillips, L., Torr, K., et al. (2007). Exploring lignification in conifers by silencing hydroxycinnamoyl-CoA: shikimate hydroxycinnamoyltransferase in Pinus radiata. Proc. Natl. Acad. Sci. U.S.A. 104, 11856-11861. doi: 10.1073/pnas.0701428104
80. Wang, M., Simon, J., Aviles, I., He, K., Zheng, Q., and Tadmor, Y. (2003). Analysis of antioxidative phenolic compounds in artichoke (Cynara scolymus L.). J. Agric. Food Chem. 51, 601-608. doi: 10.1021/jf020792b
81. Wijekoon, C., and Facchini, P. (2012). Systematic knockdown of morphine pathway enzymes in opium poppy using virus-induced gene silencing. Plant J. 69, 1052-1063. doi: 10.1111/j.1365-313X.2011.04855.x
82. Xia, Y., Nikolau, B. J., and Schnable, P. S. (1996). Cloning and characterization of CER2, an Arabidopsis gene that affects cuticular wax accumulation. Plant Cell 8, 1291-1304. doi: 10.1105/tpc.8.8.1291
83. Xu, J., Hu, Q., and Liu, Y. (2012). Antioxidant and DNA-protective activities of chlorogenic acid isomers. J. Agric. Food Chem. 60, 11625-11630. doi: 10.1021/jf303771s
84. Yu, X., Chen, M., and Liu, C. (2008). Nucleocytoplasmic-localized acyltransferases catalyze the malonylation of 7-O-glycosidic (iso)flavones in Medicago truncatula. Plant J. 55, 382-396. doi: 10.1111/j.1365-313X.2008.03509.x
85. Zhu, Y., Wang, H., Peng, Q., Tang, Y., Xia, G., Wu, J., et al. (2015). Functional characterization of an anthocyanidin reductase gene from the fibers of upland cotton (Gossypium hirsutum). Planta 241, 1075-1089. doi: 10.1007/s00425-014-2238-4