Novel transgenic rice overexpressing anthocyanidin synthase accumulates a mixture of flavonoids leading to an increased antioxidant potential

Metabolic Engineering

Volumn 9, Issue 1, 2007, Pages 95-111

  Reddy, Ambavaram M ^a   Reddy, Vaka S ^a,b   Scheffler, Brian E ^b   Wienand, Udo ^b   Reddy, Arjula R ^a  

^a INSTITUTE OF LIFE SCIENCES   (India)

^b UNIVERSITY OF HAMBURG   (Germany)

Author keywords

Anthocyanidin synthase; Antioxidants; Dioxygenases; Flavonoids; Metabolic engineering; Procyanidins

Indexed keywords

ANTHOCYANIDIN SYNTHASE; DIOXYGENASES; FLAVONOIDS; METABOLIC ENGINEERING;

ENZYME KINETICS; FREE RADICALS; GENETIC ENGINEERING; MUTAGENESIS; PLANTS (BOTANY); PROTEINS; VEGETATION;

ANTIOXIDANTS;

ANTHOCYANIDIN DERIVATIVE; ANTHOCYANIDIN SYNTHASE; ANTHOCYANIN; ANTIOXIDANT; COMPLEMENTARY DNA; FLAVONE SYNTHASE I; FLAVONOID; FLAVONOL SYNTHASE; FLAVONONE 3BETA HYDROXYLASE; FREE RADICAL; LEUCOANTHOCYANIDIN DERIVATIVE; PROANTHOCYANIDIN DERIVATIVE; QUERCETIN; SYNTHETASE; TAXIFOLIN; UNCLASSIFIED DRUG;

ALEURONE; ANTIOXIDANT ACTIVITY; ARTICLE; BETA SHEET; BIOSYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MECHANISM; GENE OVEREXPRESSION; GENETIC COMPLEMENTATION; GENETIC ENGINEERING; HEALTH PROMOTION; MAIZE; MOLECULAR CLONING; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PERICARP; PRIORITY JOURNAL; PROTEIN EXPRESSION; RICE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; TRANSGENIC CROP;

AMINO ACID SEQUENCE; ANTHOCYANINS; ANTIOXIDANTS; CATALYSIS; FLAVONOIDS; FLAVONOLS; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; OXYGENASES; PLANTS, GENETICALLY MODIFIED; QUERCETIN; ZEA MAYS;

ANIMALIA; ZEA MAYS;

EID: 33845742984     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2006.09.003     Document Type: Article

References (81)

1. Altschul S.F., Thomas L.M., Alejandro A.S., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
2. Borevitz J.O., Xia Y., Blount J., Dixon R.A., and Lamb C. Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12 (2000) 2383-2394
3. Bovy A., de Vos R., Kemper M., Schijlen E., Pertejo A.M., Muir S., Collins G., Robinson S., Verhoeyen M., Hughes S., Santos-Buelga C., and van Tunen A. High-flavonol tomatoes resulting from the heterologous expression of the maize transcription factor genes LC and C1. Plant Cell 14 (2002) 2509-2526
4. Cao G., Sofic E., and Prior R.L. Antioxidant capacity of tea and common vegetables. J. Agri. Food Chem. 44 (1996) 3426-3431
5. Chu C.C., Wang C.C., Sun C.S., Hsu C., Yin K.C., Chu C.Y., and Bi F.Y. Establishment of an efficient medium for anther culture of rice through comparative experiments on the nitrogen sources. Sci. Sinica 18 (1975) 659-668
6. Colliver S., Bovy A., Collins G., Muir S., Robinson S., de Vos C.H.R., and Verhoeyen M.E. Improving the nutritional content of tomatoes through reprogramming their flavonoid biosynthetic pathway. Photochem. Rev. 1 (2002) 113-123
7. de Kochko A., Qu R., Marmey P., Rance I., Beachy R.N., and Fauquet C. Protein slot blotting, an easy fast and reliable technique to identify the expression of a protein in transgenic plants. Plant Mol. Biol. Rep. 12 (1994) 274-278
8. Dixon R.A., and Paiva N. Stress-induced phenylpropanoid metabolism. Plant Cell 7 (1995) 1085-1097
9. Dixon R.A., Xie D.Y., and Sharma S.B. Proanthocyanidins-a final frontier in flavonoid research?. New Phytol. 165 (2005) 9-28
10. Dooner H.K., Robbins T.P., and Jorgensen R.A. Genetic and developmental control of anthocyanin biosynthesis. Annu. Rev. Genet. 25 (1991) 173-199
11. Elomaa P., Uimari A., Mehto M., Albert V.A., Laitinen R.A., and Teeri T.H. Activation of anthocyanin biosynthesis in Gerbera hybrida (Asteraceae) suggests conserved protein-protein and protein-promoter interactions between the anciently diverged monocots and eudicots. Plant Physiol. 133 (2003) 1831-1842
12. Forkmann G., and Heller W. Biosynthesis of flavonoids. Comprehensive Natural Products Chemistry (1999), Amsterdam, Elsevier 713-748
13. Gandikota M., Alexandre de Kochko, Chen L., Ithal N., and Claude Fauquet Reddy A.R. Development of transgenic rice expressing maize anthocyanin genes and increased blast resistance. Mol. Breed. 7 (2001) 73-83
14. Gebhardt Y., Witte S., Forkmann G., Lukacin R., Martern U., and Martens S. Molecular evolution of flavonoid dioxygenases in the family apiaceae. Phytochemistry 66 (2005) 1273-1284
15. Goff S.A., Klein T.M., Roth B.A., Fromm M.E., Cone K.C., Radicella J.P., and Chandler V.L. Transactivation of anthocyanin biosynthetic genes following transfer of B regulatory genes into maize tissues. EMBO J. 9 (1990) 2517-2522
16. Grotewold E., Chamberlin M., Snook M., Siame B., Butler L., Swenson J., Maddock S., St. Clair G., and Bowen B. Engineering secondary metabolism in maize cell by ectopic expression of transcription factors. Plant Cell 10 (1998) 721-740
17. Harborne J.B. Comparative Biochemistry of the Flavonoids (1967), Academic Press, London
18. Hiei Y., Ohta S., Komari T., and Kumashiro T. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6 (1994) 271-282
19. Holton T.A., and Cornish E.C. Genetics and biochemistry of anthocyanin biosynthesis. Trends Biotechnol. 12 (1995) 40-42
20. Hu J., Anderson B., and Wessler S.R. Isolation and characterization of rice R genes: evidence for distinct evolutionary paths in rice and maize. Genetics 142 (1996) 1021-1031
21. Hu J., Reddy V.S., and Wessler S.R. The rice R gene family: two distinct subfamilies containing several miniature inverted-repeat transposable elements. Plant Mol. Biol. 42 (2000) 667-678
22. Ithal N., and Reddy A.R. Rice flavonoid pathway genes, OsDfr and OsAns, are induced by dehydration, high salt and ABA, and contain stress responsive promoter elements that interact with the transcription activator, OsC1-MYB. Plant Sci. 166 (2004) 1505-1513
23. Jovanoic S.V., Steenken S., Tosic M., Marjanovic B., and Simic M.G. Flavonoids as antioxidants. J. Am. Chem. Soc. 116 (1994) 4846-4851
24. Kioshita T., and Takahashi M. The one-hundredth report of genetical studies on rice plant. Linkage studies and future prospects. J. Fac. Agric. Hokkaido Univ. 65 (1991) 1-61
25. Kong J.M., Lian-Sai C., Ngoh-Khang G., Tet-Fatt C., and Brouillard R. Analysis and biological activities of anthocyanins. Phytochemistry 64 (2003) 923-933
26. Kootstra A. Protection from UV-B-induced DNA damage by flavonoids. Plant Mol. Biol. 26 (1994) 771-774
27. Kumar R., and Singh M. Tannins: their adverse role in ruminant nutrition. J. Agric. Food Chem. 32 (1984) 447-453
28. Kumaria R., Waie B., and Rajam M.V. Plant regeneration from transformed embryogenic callus of an elite indica rice via Agrobacterium. Plant Cell Tiss. Org. Culture 67 (2001) 63-71
29. Liu C.J., Blount J.W., Steele C.L., and Dixon R.A. Bottlenecks for metabolic engineering of isoflavone glycoconjugates in Arabidopsis. Proc. Natl. Acad. Sci. USA 99 (2002) 14578-14583
30. Lloyd A.M., Walbot V., and Davis R.W. Arabidopsis and Nicotiana anthocyanin production activated by maize regulators R and C1. Science 258 (1992) 1773-1775
31. Lukaszewicz M., Matysiak-Kata, Skala J., Fecka I., Cisowski W., and Szopa J. Antioxidant capacity manipulation in transgenic potato tuber by changes in phenolic compounds content. J. Agric. Food Chem. 52 (2004) 1526-1533
32. Madhuri G., and Reddy A.R. Plant biotechnology of flavonoids. Plant Biotechnol. 16 (1999) 179-199
33. Martens S., Knott J., Seitz C.A., Janvari L., Yu S.N., and Forkmann G. Impact of biochemical pre-studies on specific metabolic engineering strategies of flavonoid biosynthesis in plant tissues. Biochem. Eng. J. 14 (2003) 227-235
34. Mathews H., Clendennen S.K., Caldwell C.G., Liu X.L., Connors K., Matheis N., Schuster D.K., Menasco D.J., Wagoner W., Lightner J., and Wagner D.R. Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport. Plant Cell 15 (2003) 1689-1703
35. Menssen A., Hohmann S., Martin W., Patrick S.S., Peterson P.A., Saedler H., and Gierl A. The En/Spm transposable element of Zea mays contains splice sites at the termini generating a novel intron from a dSpm element in the A2 gene. EMBO J. 9 (1990) 3051-3057
36. Middleton E., Kandaswami C., and Theoharides T.C. The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. Pharmacol. Rev. 52 (2000) 673-751
37. Mol J., Grotewold E., and Koes R. How genes paint flowers and seeds. Trends Plant Sci. 3 (1998) 212-217
38. Mol J., Cornish E., Mason J., and Koes R. Novel coloured floweres. Curr. Opin. Biotechnol. 10 (1999) 198-201
39. Moreno S. Review: methods used to evaluate the free radical scavenging activity in foods and biological systems. Food Sci. Tech. Int. 8 (2002) 2002
40. Muir S.R., Collins G.J., Robinson S., Hughes S., Bovy A., De Vos C.H.R., van Tunen A.J., and Verhoeyen M.E. Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nat. Biotechnol. 19 (2001) 470-474
41. Naik G.H., Priyadarsini K.I., Sata J.G., Banavalikar M.M., Sohoni D.P., Biyani M.K., and Mohan H. Comparative antioxidant activity of individual herbal components used in ayurvedic medicine. Phytochemistry 63 (2003) 97-104
42. Nakajima J.I., Tanaka ., Yamazaki M., and Saito K. Reaction mechanism from leucoanthocyanidin to anthocyanidin 3-glucoside, a key reaction for coloring in anthocyanin biosynthesis. J. Biol. Chem. 276 (2001) 25797-25803
43. Nesi N., Debeaujon I., Jond C., Stewart A.J., Jenkins G.I., Caboche M., and Lepiniec L. The transparent testa16 locus encodes the Arabidopsis BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell 14 (2002) 2463-2479
44. Ni M., Cui D., Einstein J., Narasimhulu S., and Gelvin S.B. Strength and tissue specificity of chimeric promoters derived from the octopine and mannopine synthase genes. Plant J. 7 (1995) 661-676
45. Nijveldt R.J., Nood V.E., van. Hoorn D.E.C., Boelens P.G., van Norren K., and van Leeuwen P.A.M. Flavonoids: a review of probable mechanisms of action and potential applications American J. Clin. Nutr. 74 (2001) 418-425
46. Padmavati M., and Reddy A.R. Flavonoid biosynthetic pathway and cereal defence response: an emerging trend in crop biotechnology. J. Plant Biochem. Biotech. 8 (1999) 15-20
47. Padmavati M., Sakthivel N., Thara K.V., and Reddy A.R. Differential sensitivity of rice pathogens to growth inhibition by flavonoids. Phytochemistry 46 (1997) 499-502
48. Pietta P.G. Flavonoids as antioxidants. J. Nat. Prod. 63 (2000) 1035-1042
49. Porter L.J., Hrtisch L.N., and Chan B.G. The conversion of procyanidins and prodelphinidins to cyaniding and delphinidin. Phytochemistry 25 (1986) 223-230
50. Potapovich A.I., and Kostyuk V.A. Comparative study of antioxidant properties and cytoprotective activity of flavonoids. Biochemistry (Mosc) 68 (2003) 514-519
51. Prescott A.G., and John P. Dioxygenases: molecular structure and role in plant metabolism Annu. Rev. Plant Mol. Biol. 47 (1996) 245-271
52. Prescott A.G., Stamford N.P., Wheeler G., and Firmin J.L. In vitro properties of a recombinant flavonol synthase from Arabidopsis thaliana. Phytochemistry 60 (2002) 589-593
53. Quattrocchio F., Wing J.F., van der Woude K., Mol J.N., and Koes R. Analysis of bHLH and MYB domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genes. Plant J 13 (1998) 475-488
54. Rashid H., Yokoi S., Toriyama K., and Hinata K. Transgenic plant production mediated by Agrobacterium in Indica rice. Plant Cell Reports 15 (1996) 727-730
55. Reddy V.S., Goud K.V., Sharma R.P., and Reddy A.R. Ultraviolet-B-responsive anthocyanin production in a rice cultivar is associated with a specific phase of phenylalanine ammonia lyase biosysthesis. Plant Physiol. 105 (1994) 1059-1066
56. Reddy V.S., Dash S., and Reddy A.R. Anthocyanin pathway in rice (Oryza sativa L): identification of a mutant showing dominat inhibition of anthocyanins in leaf and accumulation of proanthocyanidins in pericarp. Theor. Appl. Genet. 91 (1995) 301-312
57. Reddy A.R., Scheffler B.E., Madhuri G., Shrivastava M.N., Arvind Kumar, Sathyanarayanan P.V., Nair S., and Madan Mohan. Chalcone synthase in rice (Oryza sativa L.): Detection of the CHS protein in seedlings and molecular mapping of the chs locus. Plant Mol. Biol. 32 (1996) 735-743
58. Reddy V.S., Scheffler B.E., Wienand U., and Reddy A.R. DFR from rice. Plant Mol. Biol. 32 (1997) 1235-1237
59. Reddy V.S., Scheffler B.E., Wienand U., Wessler S.R., and Reddy A.R. Cloning and characterization of the rice homolog of the maize C1 anthocyanin regulatory gene. Plant Mol. Biol. 36 (1998) 497-498
60. Rice-Evans C. Flavonoid antioxidants. Curr. Med. Chem. 8 (2001) 797-807
61. Saito K., Kobayashi M., Gong Z., Tanaka Y., and Yamazaki M. Direct evidance for anthocyanidin synthase as a 2-oxoglutarate-dependant oxygenase: molecular cloning and functional expression of cDNA from a red forma of Perilla frutescens. Plant J. 17 (1999) 181-189
62. Sakamoto W., Ohmori T., Kageyama K., Miyazaki C., Saito A., Murata M., Noda K., and Maekawa M. The Purple leaf (Pl) locus of rice: the Pl(w) allele has a complex organization and includes two genes encoding basic helix-loop-helix proteins involved in anthocyanin biosynthesis. Plant Cell Physiol. 42 (2001) 982-991
63. Schijlen E.G.W.M., Rice de Vos C.H., Tunen A.J.V., and Bovy A.G. Modification of flavonoid biosynthesis in crop plants. Phytochemistry 65 (2004) 2631-2648
64. Schofield C.J., and Zhang Z.H. Structural and mechanistic studies on 2-oxoglutarate dependent oxygenases and related enzymes. Curr. Opin. Struct. Biol. 9 (1999) 722-731
65. Shirley B.W. Flavonoid biosynthesis: new functions for an old pathway. Trends Plant Sci. 1 (1996) 377-382
66. Shirley W.B. Biosynthesis of flavonoids and effects of stress. Curr. Opin. Plant Biol. 5 (2002) 218-223
67. Springob K., Nakajima J.I., Yamazaki M., and Saito K. Recent advances in the biosynthesis and accumulation of anthocyanins. Nat. Prod. Rep. 20 (2003) 288-303
68. Takahashi M. Genetical studies on rice plants. LXXX. Gene analysis and its related problems. J. Fac. Agr. Hokkaido Univ. 61 (1982) 91-142
69. Tsuda T., Shiga K., Ohshima K., Kawakishi S., and Osawa T. Inhibition of lipid peroxidation and the active oxygen radical scavenging effect of anthocyanin pigments isolated from Phaseolus vulgaris L. Biochem. Pharmacol. 52 (1996) 1033-1039
70. Tsuda T., Watanabe M., Ohshima K., Norinobu S., and Choi S.W. Antioxidative activity of the anthocyanin pigments cyanidin3-O-beta-d-glucoside and cyanidin. J. Agric. Food Chem. 42 (1994) 2407-2410
71. Turnbull J.J., Nakajima J., Welford R.W., Yamazaki M., Saito K., and Schofield C.J. Mechanistic studies on three 2-oxoglutarate-dependent oxygenases of flavonoid biosynthesis. J. Biol. Chem. 279 (2004) 1206-1216
72. Turnbull J.J., Sobey W.J., Aplin R.T., Hassan A., Fimin J.L., Sscofield C.J., and Prescott A.G. Are anthocyanidins the immediate products of anthocyanidin synthase?. Chem. Commun. (2000) 2473-2474
73. Ukeda H., Adachi A., and Sawamura M. Flow injection analysis of DPPH radical based on electron spin resonance. Talanta 58 (2002) 1279-1283
74. Verhoeyen M.E., Bovy A., Collins G., Muir S., Robinson1 S., de Vos C.H.R., and Colliver L.S. Increasing antioxidant levels in tomatoes through modification of the flavonoid biosynthetic pathway. J. Exp. Bot. 53 (2002) 2099-2106
75. Wang H., Cao G., and Prior R.L. The oxygen radical absorbing capacity of anthocyanins. J. Agric. Food Chem. 45 (1997) 304-309
76. Weisshaar B., and Jenkins G.I. Phenylpropanoid biosynthesis and its regulation. Curr. Opin. Plant Biol. 3 (1998) 251-257
77. Wellmann F., Griesser M., Schwab W., Martens S., Eisenreich W., Matern U., and Lukacin R. Anthocyanidin synthase from Gerbera hybrida catalyzes the conversion of (+)-catechin to cyaniding and a novel procyanidin. FEBS Lett. 580 (2006) 1642-1648
78. Wilmouth R.C., Turnbull J.J., Welford W.D., Clifton J.I., and Prescott G. Structure and mechanism of anthocyanidin synthase from Arabidopsis thaliana. Structure 10 (2002) 93-103
79. Xie D.Y., Sharma S.B., Nancy L.P., Ferreira D., and Dixon R.A. Role of anthocyanidin reductase, encoded by BANYULUS in plant flavonoid biosynthesis. Science 299 (2003) 396-399
80. Yan Y., Chemler J., Huang L., Martens S., and Koffas M.A.G. Metabolic engineering of anthocyanin biosynthesis in Escherichia coli. Appl. Environ. Microbiol. 7 (2005) 3617-3623
81. Yoshida S., Foorno D.A., Cock J.H., and Gomez K.A. In Laboratory Manual for Physiological Studies of Rice. third ed (1976), International Rice Research Institute, Philippines pp. 61-66