Flavonoids of leguminous plants: Structure, biological activity, and biosynthesis

Journal of Plant Research

Volumn 113, Issue 4, 2000, Pages 475-488

  Aoki, Toshio ^a   Akashi, Tomoyoshi ^a   Ayabe, Shin Ichi ^a  

^a NIHON UNIVERSITY   (Japan)

Author keywords

Biosynthesis; Cytochrome P450; Flavonoid; Isoflavonoid; Phytoalexin; Plant Microbe interaction; Symbiotic signal

Indexed keywords

ANIMALIA; FABACEAE; TRACHEOPHYTA;

EID: 0034349180     PISSN: 09189440     EISSN: None     Source Type: Journal    
DOI: 10.1007/pl00013958     Document Type: Article

References (139)

1. Akada, S. and Dube, S.K. 1995. Organization of soybean chalcone synthase gene clusters and characterization of a new member of the family. Plant Molec. Biol. 29: 189-199.
2. Akashi, T., Furuno, T., Futami, K., Honda, M., Takahashi, T., Welle, R. and Ayabe, S. 1996. A cDNA for polyketide reductase (accession no. D83718) that catalyzes the formation of 6′-deoxychalcone from cultured Glycyrrhiza echinata L. cells (PGR 96-023). Plant Physiol. 111: 347.
3. Akashi, T., Saito, N., Hirota, H. and Ayabe, S. 1997a. Anthocyanin-producing dandelion callus as a chalcone synthase source in recombinant polyketide reductase assay. Phytochemistry 46: 283-287.
4. Akashi, T., Aoki, T., Takahashi, T., Kameya, N., Nakamura, I. and Ayabe, S. 1997b. Cloning of cytochrome P450 cDNAs from cultured Glycyrrhiza echinata L. cells and their transcriptional activation by elicitor treatment. Plant Sci. 126: 39-47.
5. Akashi, T., Aoki, T., Kameya, N., Nakamura, I. and Ayabe, S. 1997c. Two new cytochrome P450 cDNAs (accession nos. AB001379 and AB001380) from elicitor-induced licorice (Glycyrrhiza echinata L.) cells (PGR97-167). Plant Physiol. 115: 1288.
6. Akashi, T., Aoki, T. and Ayabe, S. 1998a. CYP81E1, a cytochrome P450 cDNA of licorice (Glycyrrhiza echinata L.), encodes isoflavone 2′-hydroxylase. Biochem. Biophys. Res. Commun. 251: 67-70.
7. Akashi, T., Aoki, T. and Ayabe, S. 1998b. Identification of a cytochrome P450 cDNA encoding (2S)-flavanone 2-hydroxylase of licorice (Glycyrrhiza echinata L.; Fabaceae) which represents licodione synthase and flavone synthase II. FEBS Lett. 431: 287-290.
8. Akashi, T., Aoki, T. and Ayabe, S. 1999a. Cloning and functional expression of a cytochrome P450 cDNA encoding 2-hydroxyisoflavanone synthase involved in biosynthesis of the isoflavonoid skeleton in licorice. Plant Physiol. 121: 821-828.
9. Akashi, T., Fukuchi-Mizutani, M., Aoki, T., Ueyama, Y., Yonekura-Sakakibara, K., Tanaka, Y., Kusumi, T. and Ayabe, S. 1999b. Molecular cloning and biochemical characterization of a novel cytochrome P450, flavone synthase II, that catalyzes direct conversion of flavanones to flavones. Plant Cell Physiol. 40: 1182-1186.
10. Akashi, T., Sawada, Y., Aoki, T. and Ayabe, S. 2000. New scheme of the biosynthesis of formononetin involving 2, 7,4′-trihydroxyisoflavanone but not daidzein as the methyl acceptor. Biosci. Biotechnol. Biochem. 64: 2276-2279.
11. Asamizu, E., Nakamura, Y., Sato, S. and Tabata, S. 2000. Generation of 7,137 Non-redundant expressed sequence tags from a legume, Lotus japonicus. DNA Research 7: 127-130.
12. Ayabe, S. and Furuya, T. 1982. Studies on plant tissue cultures. Part 36. Biosynthesis of a retrochalcone, echinatin, and other flavonoids in the cultured cells of Glycyrrhiza echinata. A new route to a chalcone with transposed A-and B-rings. J. Chem. Soc. Perkin Trans. 1: 2725-2734.
13. Ayabe, S., Kobayashi, M., Hikichi, M., Matsumoto, K. and Furuya, T. 1980a. Flavonoids from the cultured cells of Glycyrrhiza echinata. Phytochemistry 19: 2179-2183.
14. Ayabe, S., Yoshikawa, T., Kobayashi, M. and Furuya, T. 1980b. Biosynthesis of a retrochalcone, echinatin: involvement of O-methyltransferase to licodione. Phytochemistry 19: 2331-2336.
15. Ayabe, S., Iida, K. and Furuya, T. 1986. Stress-induced formation of echinatin and a metabolite, prenyllicodione, in cultured Glycyrrhiza echinata cells. Phytochemistry 25: 2803-2806.
16. Ayabe, S., Udagawa, A. and Furuya, T. 1988. NAD(P)H-Dependent 6′-deoxychalcone synthase activity in Glycyrrhiza echinata cells induced by yeast extract. Arch. Biochem. Biophys. 261: 458-462.
17. Ballance, G.M. and Dixon, R.A. 1995. Medicago sativa cDNAs encoding chalcone reductase. Plant Physiol. 107: 1027-1028.
18. Bavage, A.D., Davies, I.G., Robbins, M.P. and Morris, P. 1997. Expression of an antirrhinum dihydroflavonol reductase gene results in changes in condensed tannin structure and accumulation in root cultures of Lotus corniculatus (bird's foot trefoil). Plant Molec. Biol. 35: 443-458.
19. Boland, M.J. and Wong, E. 1975. Purification and kinetic properties of chalcone-flavanone isomerase from soya bean. Eur. J. Biochem. 50: 383-389.
20. Bolwell, G.P., Bozak, K. and Zimmerlin, A. 1994. Plant cytochrome P450. Phytochemistry 37: 1491-1506.
21. Bozak, K.R., Yu, H., Sirevåg, R. and Christoffersen, R.E. 1990. Sequence analysis of ripening-related cytochrome P-450 cDNAs from avocado fruit. Proc. Natl. Acad. Sci. USA 87: 3904-3908.
22. Bonde, M.R., Millar, R.L. and Ingham, J.L. 1973. Induction and identification of sativan and vestitol as two phytoalexins from Lotus corniculatus. Phytochemistry 12: 2957-2959.
23. Burbulis, I.E. and Winkel-Shirley, B. 1999. Interactions among enzymes of the Arabidopsis flavonoid biosynthetic pathway. Proc. Natl. Acad. Sci. USA 96: 12929-12934.
24. Cardenas, L., Dominguez, J., Quinto, C., Lopez-Lara, I., Lugtenberg, B., Spaink, H., Rademaker, G., Haverkamp, J. and Thomas-Oates, J. 1995. Isolation, chemical structures and biological activity of the lipo-chtin oligosaccharide nodulation signals from Rhizobium etli. Plant Molec. Biol. 29: 453-464.
25. Chan, B.G., Waiss, A.C. and Lukefahr, M. 1978. Condensed tannin and antibiotic chemical from Gossypium hirsutum. J Insect Physiol. 24: 113-118.
26. Chappell, J. and Hahlbrock, K. 1984. The transcription of plant defense genes in response to UV light or fungal elicitor. Nature 311: 76-78.
27. Charrier, B., Trinh, H., Poirier, S., Kondorosi, A. and Ratat, P. 1998. Flavanone 3-hydroxylase (F3H) expression and flavonoid localization in nodules of three legume plants reveal distinct tissue specificities. Molec. Plant Microbe Interact. 9: 924-932.
28. Clemens, S. and Barz, W. 1996. Cytochrome P450-dependent methylenedioxy bridge formation in Cicer arietinum. Phytochemistry 41: 457-460.
29. Colliver, S.P., Morris, P. and Robbins, M.P. 1997. Differential modification of flavonoid and isoflavonoid biosynthesis with an antisense chalcone synthase construct in transgenic Lotus corniculatus. Plant Molec. Biol. 35: 509-522.
30. Crombie, L. and Whiting, D.A. 1992. The mechanism of the enzymic induced flavanone-isoflavone change. Tetrahedron Lett. 33: 3663-3666.
31. Daniell, T., O'Hagan, D. and Edwards, R. 1997. Alfalfa cell cultures treated with a fungal elicitor accumulate flavone metabolites rather than isoflavones in the presence of the methylation inhibitor tubericidin. Phytochemistry 44: 285-291.
32. Devic, M., Guilleminot, J., Debeaujon, I., Bechtold, N., Bensaude, E., Koornneef, M., Pelletier, G. and Delseny, M. 1999. The BANYULS gene encodes a DFR-like protein and is a marker of early seed coat development. Plant J. 19: 387-398.
33. Dewick, P.M. 1983. Isoflavonoids. In J.B. Harborne and T.J. Mabry, eds., The Flavonoids. Advances in Research, Chapman and Hall, London, pp. 535-640.
34. Dewick, P.M. 1994. Isoflavonoids. In J.B. Harborne, ed., The Flavonoids. Advances in Research since 1986, Chapman and Hall, London, pp. 117-238.
35. Dixon, R.A. 1999. Isoflavonoids: biochemistry, molecular biology, and biological functions. In U. Sankawa, ed., Comprehensive natural products chemistry. Volume 1. Polyketides and other secondary metabolites including fatty acids and their derivatives, Elsevier, Oxford, pp. 773-823.
36. Dixon, R.A. and Steele, C.L. 1999. Flavonoids and isoflavonoids - a gold mine for metabolic engineering. Trends Plant Sci. 4: 394-400.
37. Dixon, R.A., Dey, P.M. and Whitehead, I.M. 1982. Purification and properties of chalcone isomerase from cell suspension cultures of Phaseolus vulgaris. Biochim. Biophys. Acta 715: 25-33.
38. Dixon, R.A., Blyden, E.R., Robbins, M.P., van Tunen, A.J. and Mol, J.N. 1988. Comparative biochemistry of chalcone isomerases. Phytochemistry 27: 2801-2808.
39. Dixon, R.A., Lamb, C.J., Masoud, S., Sewalt, V.J. and Paiva, N.L. 1996. Metabolic engineering: prospects for crop improvement through the genetic manipulation of phenylpropanoid biosynthesis and defense responses - a review. Gene 179: 61-71.
40. Dixon, R.A., Howles, P.A., Lamb, C., He, X.Z. and Reddy, J.T. 1998. Prospects for the metabolic engineering of bioactive flavonoids and related phenylpropanoid compounds. Adv. Expr. Med. Biol. 439: 55-66.
41. Dixon, R.A., Canovas, P., Guo, Z.J, He, X.Z., Lamb, C. and McAlister, F. 1999. Molecular controls for isoflavonoid bisynthesis in relation to plant and human health. In J. T. Romeo, ed., Phytochemicals in Human Health Protection, Nutrition and Plant Defense, Kluwer Academic, New York, pp. 133-159.
42. Enkerli, J., Bhatt, G. and Covert, S.F. 1998. Maackiain detoxification contributes to the virulence of Nectria haematococca MP VI on chickpea. Molec. Plant Microbe Interact, 11: 317-326.
43. Ferrer, J.-L., Jez, J.M., Bowman, M.E., Dixon, R.A. and Noel, J.P. 1999. Structure of chalcone synthase and the molecular basis of plant polyketide biosynthesis. Nature Struct. Biol. 6: 775-784.
44. Forkmann, G. and Heller, W. 1999. Biosynthesis of flavonoids. In U. Sankawa, ed., Comprehensive Natural Products Chemistry. Volume 1. Polyketides and Other Secondary Metabolites Including Fatty Acids and their Derivatives, Elsevier, Oxford, pp. 713-748.
45. Frank, M.R., Deyneka, J.M. and Schuler, M.A. 1996. Cloning of wound induced cytochrome P450 monooxygenases expressed in pea. Plant Physiol. 110: 1035-1046.
46. Gagnon, H. and Ibrahim, R.K. 1998. Aldonic acids: A novel family of nod gene inducers of Mesorhizobium loti, Rhizobium lupini, and Sinorhizobium meliloti. Molec. Plant Microbe Intract. 11: 988-998.
47. Goormachtig, S., Lievens, S., Herman, S., Van Montagu, M. and Holsters, M. 1999. Chalcone reductase-homologous transcripts accumulate during development of stem-borne nodules on the tropical legume Sesbania rostrata. Planta 209: 45-52.
48. Grant, W.F., Bullen, M.R. and de Nettancourt, D. 1962. The cytogenetics of Lotus. I. Embryo-cultured interspecific diploid hybrids closely related to Lotus corniculatus L. Canad. J. Genet. Cytol. 4: 105-128.
49. Guo, L., Dixon, R.A. and Paiva, N.L. 1994a. Conversion of vestitone to medicarpin in alfalfa (Medicago sativa L.) is catalyzed by two independent enzymes. Identification, purification, and characterization of vestitone reductase and 7,2′-dihydroxy-4′-methoxyisoflavanol dehydratase. J. Biol. Chem. 269: 22372-22378.
50. Guo, L., Dixon, R.A. and Paiva, N.L. 1994b. The 'pterocarpan synthase' of alfalfa: association and co-induction of vestitone reductase and 7, 2′-dihydroxy-4′-methoxyisoflavanol (DMI) dehydratase, the two final enzymes in medicarpin biosynthesis. FEBS Lett. 356: 221-225.
51. Guo, L. and Paiva, N.L. 1995. Molecular cloning and expression of alfalfa (Medicago sativa L.) vestitone reductase, the penultimate enzyme in medicarpin biosynthesis. Arch. Biochem. Biophys. 320: 353-60.
52. Haga, M., Akashi, T., Aoki, T. and Ayabe, S. 1997. A cDNA for S-adenosyl-L-methionine: isoliquiritigenin/ licodione 2′-O-methyltransferase (accession no. D88742) from cultured licorice (Glycyrrhiza echinata L.) cells (PGR 97-014). Plant Physiol. 113: 663.
53. Hagmann, M.L., Heller, W. and Grisebach, H. 1984. Induction of phytoalexin synthesis in soybean. Stereospecific 3,9-dihydroxypterocarpan 6a-hydroxylase from elicitor-induced soybean cell cultures. Eur. J. Biochem. 142: 127-131.
54. Hakamatsuka, T., Hashim, M.F., Ebizuka, Y. and Sankawa, U. 1991. P-450-dependent oxidative rearrangement in isoflavone biosynthesis: Reconstitution of P-450 and NADPH: P-450 reductase. Tetrahedron 47: 5969-5978.
55. Hakamatsuka, T., Mori, K., Ishida, S., Ebizuka, Y. and Sankawa, U. 1998. Purification of 2-hydroxyisoflavanone dehydratase from the cell cultures of Pueraria lobata. Phytochemistry 49: 497-505.
56. Harano, K., Okada, N., Furuno, T., Takahahi, T., Ayabe, S. and Welle, R. 1993. Enzymatic synthesis of 6′-deoxychalcone in cultured Glycyrrhiza echinata cells. Plant Cell Rep. 12: 66-69.
57. Harborne, J.B. 1994. Phytochemistry of the Leguminosae. In F.A. Bisby, J. Buckingham and J.B. Harborne, eds., Phytochemical Dictionary of the Leguminosae, Chapman & Hall, London, pp. xx-xxii.
58. Harney, P.M. and Grant, W.F. 1965. A polygonal presentation of chromatographic investigations on the phenolic content of certain species of Lotus. Canad. J. Genet. Cytol. 7: 40-51.
59. Hashim, M.F., Hakamatsuka, T., Ebizuka, Y. and Sankawa, U. 1990. Reaction mechanism of oxidative rearrangement of flavanone in isoflavone biosynthesis. FEBS Lett. 271: 219-222.
60. Haslam, E. 1998. Practical Polyphenolics: From Structure to Molecular Recognition and Physiological Action, Cambridge University Press, Cambridge.
61. Hayashi, H., Murayama, K., Hiraoka, N. and Ikeshiro, Y. 1996. Nucleotide sequences of cDNAs (accession nos. D86558 and D86559) for Glycyrrhiza glabra polyketide reductase (PGR96-095). Plant Physiol. 112: 864.
62. He, X.Z. and Dixon, R.A. 1996. Affinity chromatography, substrate/product specificity, and amino acid sequence analysis of an isoflavone O-methyltransferase from alfalfa (Medicago sativa L.). Arch. Biochem. Biophys. 336: 121-129.
63. He, X.Z., Reddy, J.T. and Dixon, R.A. 1998. Stress responses in alfalfa (Medicago sativa L). XXII. cDNA cloning and characterization of an elicitor-inducible isoflavone 7-O-methyltransferase. Plant Molec. Biol. 36: 43-54.
64. Hegnauer, R. and Grayer-Barkmeijer, R.J. 1993. Relevance of seed polysaccharides and flavonoids for the classification of the Leguminosae: a chemotaxonomic approach. Phytochemistry 34: 3-16.
65. Heller, W. and Forkmann, G. 1994. Biosynthesis of Flavonoids. In J.B. Harborne, ed., The Flavonoids. Advances in Research since 1986, Chapman and Hall, London, pp. 499-535.
66. Hinderer, W., Fletje, U. and Barz, W. 1987. Microsomal isoflavone 2′-and 3′-hydroxylases from chickpea (Cicer arietinum L.) cell suspensions induced for pterocarpan phytoalexin formation. FEBS Lett. 214: 101-106.
67. Holton, T.A., Brugliera, F., Lester, D.R., Tanaka, Y., Hyland, C.D., Meriting, J.G., Lu, C.Y., Farcy, E., Stevenson, T.W. and Cornish, E.C. 1993. Cloning and expression of cytochrome P450 genes controlling flower colour. Nature 366: 276-279.
68. Holton, T.A. and Lester, D.R. 1996. Cloning of novel cytochrome P450 gene sequences via polymerase chain reaction amplification. In Johnson, E.F. and Waterman, M.R. eds., Methods in Enzymology. vol. 272. Cytochrome P450 Part B, Academic Press, San Diego, pp. 275-283.
69. Hrazdina, G. and Wagner, G.J. 1985. Metabolic pathways as enzyme complexes: evidence for the synthesis of phenylpropanoids and flavonoids on membrane associated enzyme complexes. Arch. Biochem. Biophys. 237: 88-100.
70. Hrazdina, G., Zobel, A.M. and Hoch, H.C. 1987. Biochemical, immunological, and immunocytochemical evidence for the association of chalcone synthase with endoplasmic reticulum membranes. Proc. Natl. Acad. Sci. USA 84: 8996-8970.
71. Hrazdina, G. and Jensen, R.A. 1992. Spatial organization of enzymes in plant metabolic pathways. Annual. Rev. Plant Physiol. Plant Molec. Biol. 43: 241-267.
72. Ichimura, M., Furuno, T., Takahashi, T., Dixon, R.A. and Ayabe, S. 1997. Enzymatic O-methylation of isoliquiritigenin and licodione in alfalfa and licorice cultures. Phytochemistry 44: 991-995.
73. Ingham, J.L. 1977. Isoflavan phytoalexins from Anthyllis, Lotus and Tetragonolobus. Phytochemistry 16: 1279-1282.
74. Ito, M., Ichinose, Y., Kato, H., Shiraishi, T. and Yamada, T. 1997. Molecular evolution and functional relevance of the chalcone synthase genes of pea. Molec. Gen. Genet. 255: 28-37.
75. Jacobs, M. and Rubery, P.H. 1988. Naturally occurring auxin transport regulators. Science 241: 346-349.
76. Jez, J.M., Bowman, M.E., Dixon, R.A. and Noel, J.P. 2000. Structure and mechanism of the evolutionary unique plant enzyme chalcone isomerase. Nat. Struct. Biol. 7: 786-791.
77. Jones, W.T. and Lyttleton, J.W. 1971. Bloat in cattle. XXXIV. A survey of forages that do and do not produce bloat. New Zealand J. Agricultural Res. 13: 101-107.
78. Jones, W.T., MacDonald, P.E., Jones, S.D. and Pankhurst, C.E. 1987. Peptidoglycan-bound polysaccharide associated with resistance of Rhizobium Iti strain NZP2037 to Lotus pedunculatus root flavolan. J. Gen. Microbiol. 133: 2617-2629.
79. Jung, W., Yu, O., Lau, S.M., O'Keefe, D.P., Odell, J., Fader, G. and McGonigle, B. 2000. Identification and expression of isoflavone synthase, the key enzyme for biosynthesis of isoflavones in legumes. Nat. Biotechnol. 18: 208-212.
80. Kessmann, H., Choudhary, A.D. and Dixon, R.A. 1990. Stress responses in alfalfa (Medicago sativa L.) III. Induction of medicarpin and cytochrome P450 enzyme activities in elicitor-treated cell suspension cultures and protoplasts. Plant Cell Rep. 9: 38-41.
81. Kirikae, Y., Sakurai, M., Furuno, T., Takahashi, T. and Ayabe, S. 1993. Biosynthesis of a dibenzoylmethane, licodione, in cultured alfalfa cells induced by yeast extract. Biosci. Biotechnol. Biochem. 57: 1353-1354.
82. Kochs, G. and Grisebach, H. 1986. Enzymic synthesis of isoflavones. Eur. J. Biochem. 155: 311-318.
83. Kochs, G. and Grisebach, H. 1987. Induction and characterization of a NADPH dependent flavone synthase from cell cultures of soybean. Z. Naturforsch. 42c: 343-348.
84. Kochs, G., Welle, R. and Grisebach, H. 1987. Differential induction of enzyme in soybean cell cultures by elicitor or osmotic stress. Planta 171: 519-524.
85. Lees, G.L. 1986. Condensed tannins in the tissue culture of sainfoin (Onobrychis viciifolia Scop.) and birdsfoot trefoil (Lotus corniculatus L.). Plant Cell Rep. 5: 247-251.
86. Li, J., Ou-Lee, T., Raba, R., Amundson, R.G. and Last, R.L. 1993. Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell 5: 171-179.
87. Long, S.R. 1996. Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8: 1885-1898.
88. López-Lara, I.M., van den Berg, J.D.J., Thomas-Oates, J.E., Glushka, J., Lugtenberg, B.J.J. and Spaink, H.P. 1995. Structure identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti. Molec. Microbiol. 15: 627-638.
89. Martens, S. and Forkmann, G. 1999. Cloning and expression of flavone synthase II from Gerbera hybrids. Plant J. 20: 611-618.
90. Mathesius, U., Schlaman, H.R.M., Spaink, H.P., Sautter, C., Rolfe, B.G. and Djordjevic, M.A. 1998. Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J. 14: 23-34.
91. Maxwell, C.A., Harrison, M.J. and Dixon, R.A. 1993. Molecular characterisation and expression of alfalfa isoliquiritigenin 2′-O-methyltransferase, an enzyme specifically involved in the biosynthesis of an inducer of Rhizobium meliloti nodulation genes. Plant J. 4: 971-981.
92. McKhann, H.I. and Hirsch, A.M. 1994. Isolation of chalcone synthase and chalcone isomerase cDNAs from alfalfa (Medicago sativa L.): highest transcript levels occur in young roots and root tips. Plant Molec. Biol. 24: 767-777.
93. Meijer, A.H., Souer, E., Verpoorte, R. and Hoge, J.H.C. 1993. Isolation of cytochrome P-450 cDNA clones from the higher plant Catharanthus roseus by a PCR strategy. Plant Molec. Biol. 22: 379-383.
94. Morimoto, S., Tateishi, N., Matsuda, T., Tanaka, H., Taura, F., Furuya, N., Matsuyama, N. and Shoyama, Y. 1998. Novel hydrogen peroxide metabolism in suspension cells of Scutellaria baicalensis Georgi. J. Biol. Chem. 273: 12606-12611.
95. Morris, P. and Robbins, M.P. 1992. Condensed tannin formation by Agrobacterium rhizogenes transformed root and shoot organ cultures of Lotus corniculatus. J. Expt. Bot. 43: 221-231.
96. Nakamura, K., Akashi, T., Aoki, T., Kawaguchi, K. and Ayabe, S. 1999. Induction of isoflavonoid and retrochalcone branches of the flavonoid pathway in cultured Glycyrrhiza echinata cells treated with yeast extract. Biosci. Biotechnol. Biochem. 63: 1618-1620.
97. Nakaoki, T., Morita, N, Hiraki, A. and Kurokawa, Y. 1956. Studies on medicinal resources. V. Components of the leaves of Lotus corniculatus L. var. japonicus Regel., Mikrolespedeza striata Makino, Magnolia obovata Thunb., and Abutilon avicennae Gaertn. Yakugaku Zasshi 76: 347-349.
98. Nelson, D.R., Kamataki, T., Waxman, D.J., Guengerich, F.P., Estabrook, R.W., Feyereisen, R., Gonzalez, F.J., Coon, M.J., Gunsalus, I.C., Gotoh, O., Okuda, K. and Nebert, D.W. 1993. The P450 superfamily: update on new sequences, gene mapping, accession numbers, early trivial names of enzymes, and nomenclature. DNA Cell Biol. 12: 1-51.
99. Otani, K., Takahashi, T., Furuya, T. and Ayabe, S. 1994. Licodione synthase, a cytochrome P450 monooxygenase catalyzing 2-hydroxylation of 5-deoxyflavanone, in cultured Glycyrrhiza echinata L. cells. Plant Physiol. 105: 1427-1432.
100. Overkamp, S. and Barz, W. 1999. Cloning of two Cicer arietinum L. cDNA's (accession nos. AJ012581 and AJ238439) encoding cytochrome P450s highly homologous to isoflavone 2′-hydroxylase from licorice (PGR99-102). Plant Physiol. 120: 935.
101. Phillips, D.A. 1992. Flavonoids: plant signals to soil microbes. In H.A. Stafford and R.K. Ibrahim, eds., Recent Advances in Phytochemistry. Vol. 26. Phenolic Metabolism in Plants, Plenum Press, New York, pp. 201-231.
102. Phillips, D.A. 2000. Biosynthesis and release of rhizobial nodulation gene inducers by legumes. In E.W. Triplett, ed., Prokaryotic Nitrogen Fixation: A Model System for Analysis of a Biological Process, Horizon Scientific Press, Wymondham, UK, pp. 349-363.
103. Punkhurst, C.E. and Jones, W.T. 1979. Effectiveness of Lotus root nodules: 2. Relationship between root nodule effectiveness and 'in vitro' sensitivity of fast-growing Lotus rhizobia to flavolans. J. Expt. Bot. 30: 1095-1107.
104. Rasmussen, S. and Dixon, R.A. 1999. Transgene-mediated and elicitor-induced perturbation of metabolic channeling at the entry point into the phenylpropanoid pathway. Plant Cell 11: 1537-1551.
105. Robbins, M.P., Thomas, B. and Morris, P. 1991. Phenylpropanid defence responses in transgenic Lotus corniculatus 1. Glutathione elicitation of phytoalexins in transformed root cultures. Plant Cell Rep. 10: 59-62.
106. Robbins, M.P., Thomas, B. and Morris, P. 1995. Phenylpropanid defence responses in transgenic Lotus corniculatus II. Modelling plant defence responses in transgenic root cultures using thiol and carbohydrate elicitors. J. Exp. Bot. 46: 513-524.
107. Robbins, M.P., Bavage, A.D., Strudwicke, C. and Morris, P. 1998. Genetic manipulation of condensed tannins in higher plants: II Analysis of birdsfoot trefoil plants harboring antisense dihydroflavonol reductase constructs. Plant Physiol. 116: 1133-1144.
108. Saitoh, T., Shibata, S., Sankawa, U., Furuya, T. and Ayabe, S. 1975. Biosynthesis of echinatin. A new biosynthetical scheme of retrochalcone. Tetrahedron Lett. 4463-4466.
109. Sallaud, C., el-Turk, J., Bigarre, L., Sevin, H., Welle, R. and Esnault, R. 1995. Nucleotide sequences of three chalcone reductase genes from alfalfa. Plant Physiol. 108: 869-870.
110. Sankawa, U., Hakamatsuka, T., Shinkai, K., Yoshida, M., Park, H.-H. and Ebizuka, Y. 1995. Changes of secondary metabolism by elicitor treatment in Pueraria lobata cell cultures. In M. Terzi, R. Cella and A. Falavigna, eds., Current Issues in Plant Molecular and Cellular Biology, Kluwer Academic Publishers, Dordrecht, pp. 595-604.
111. Sankawa, U. and Hakamatsuka, T. 1997. Biosynthesis of isoflavone and related compounds in tissue cultures of Pueraria lobata. In K. Ogura and U. Sankawa, eds., Dynamic Aspects of Natural Products Chemistry-Molecular Biological Approaches, Kodansha/Harwood Academic, Tokyo, pp. 25-48.
112. Schopfer, C.R. and Ebel, J. 1998. Identification of elicitor-induced cytochrome P450s of soybean (Glycine max L.) using differential display of mRNA. Molec. Gen. Genet. 258: 315-322.
113. Schopfer, C.R., Kochs, G., Lottspeich, F. and Ebel, J. 1998. Molecular characterization and functional expression of dihydroxypterocarpan 6a-hydroxylase, an enzyme specific for pterocarpanoid phytoalexin biosynthesis in soybean (Glycine max L.). FEBS Lett. 432: 182-186.
114. Schröder, J. 1999. The chalcone/stilbene synthase-type family of condensing enzymes. In U. Sankawa, ed., Comprehensive natural products chemistry. Volume 1. Polyketides and other secondary metabolites including fatty acids and their derivatives, Elsevier, Oxford, pp. 749-771.
115. Schuler, M.A. 1996. Plant cytochrome P450 monooxygenases. Crit. Rev. Plant Sci. 15: 235-284.
116. Shimada, N., Akashi, T., Aoki, T. and Ayabe, S. 2000. Induction of isoflavonoid pathway in the model legume Lotus japonicus: molecular characterization of enzymes involved in phytoalexin biosynthesis. Plant Sci. 160: 37-47.
117. Shirley, B.W. 1996. Flavonoid biosynthesis - 'new' functions for an 'old' pathway. Trends Plant Sci. 1: 377-381.
118. Skadhauge, B., Gruber, M.Y., Thomsen, K.K. and von Wettstein, D. 1997. Leucocyanidin reductase activity and accumulation of proanthocyanidins in developing legume tissues. Amer. J. Bot. 84: 494-503.
119. Spaink, H. 1998. Flavonoids as regulators of plant development. In J.T. Romeo, K.R. Downum and R. Verpoorte, eds., Phytochemical and Plant-Microbe Interactions, Plenum Press, New York, pp. 167-177.
120. Stapleton, A.E. and Walbot, V. 1994. Flavonoids can protect maize DNA from the induction of ultraviolet radiation damage. Plant Physiol. 105: 881-889.
121. Steele, C.L., Gijzen, M., Qutob, D. and Dixon, R.A. 1999. Molecular characterization of the enzyme catalyzing the aryl migration reaction of isoflavonoid biosynthesis in soybean. Arch. Biochem. Biophys. 367: 146-150.
122. Stotz, G. and Forkmann, G. 1981. Oxidation of flavanones to flavones with flower extracts of Antirrhinum majus (snapdragon). Z. Naturforsch. 36c: 737-741.
123. Suginobu, K., Suzuki, S. and Komatsu, T. 1988. Evaluation of the characteristics in miyakogusa (Lotus corniculatus L. var. japonicus Regel) 3. Characteristics of local strains collected from different regions in Japan. J. Japanese Soc. Grassland Sci. 34: 1-6.
124. Suzuki, G., Ohta, H., Kato, T., Igarashi, T., Sakai, F., Shibata, D., Takano, A., Masuda, T., Shioi, Y. and Takamiya, K. 1996. Induction of a novel cytochrome P450 (CYP93 family) by methyl jasmonate in soybean suspension-cultured cells. FEBS Lett. 383: 83-86.
125. Szczyglowski, K., Hamburger, D., Kapranov, P. and de Bruijn, F.J. 1997. Construction of a Lofus japonicus late nodulin expressed sequence tag library and identification of novel nodule-specific genes. Plant Physiol. 114: 1335-1346.
126. Tahara, S. and Ibrahim, R.K. 1995. Prenylated isoflavonoids - an update. Phytochemistry 38: 1073-1094.
127. Terai, Y., Fujii, I., Byun, S.H., Nakajima, O., Hakamatsuka, T., Ebizuka, Y. and Sankawa, U. 1996. Cloning of chalcone-flavanone isomerase cDNA from Pueraria lobata and its overexpression in Escherichia coli. Protein Expr. Purif. 8: 183-190.
128. Teutsch, H.G., Hasenfratz, M.P., Lesot, A., Stoltz, C., Garnier, J.M., Jeltsch, J.M., Durst, F. and Werck-Reichhart, D. 1993. Isolation and sequence of a cDNA encoding the Jerusalem artichoke cinnamate 4-hydroxylase, a major plant cytochrome P450 involved in the general phenylpropanoid pathway. Proc. Natl. Acad. Sci. USA 90: 4102-4106.
129. Tropf, S., Karcher, B., Schröder, G. and Schröder, J. 1995. Reaction mechanisms of homodimeric plant polyketide synthase (stilbenes and chalcone synthase). A single active site for the condensing reaction is sufficient for synthesis of stilbenes, chalcones, and 6′-deoxychalcones. J. Biol. Chem. 270: 7922-7928.
130. van der Meer, Stam, M.E., van Tunen, A.J., Mol, J.N.M. and Stuitje, A.R. 1992. Antisense inhibition of flavonoid biosynthesis in Petunia anthers results in male sterility. Plant Cell 4: 253-262.
131. Wasmann, C.C. and van Etten, H.D. 1996. Transformation-mediated chromosomes loss and disruption of gene for pisatin demethylase decrease the virulence of Nectria haematococca on pea. Molec. Plant Microbe Interact. 9: 793-803.
132. Welle, R. and Grisebach, H. 1988a. Induction of phytoalexin synthesis in soybean: enzymatic cyclization of prenylated pterocarpans to glyceollin isomers. Arch. Biochem. Biophys. 263: 191-198.
133. Welle, R. and Grisebach, H. 1988b. Isolation of a novel NADPH-dependent reductase which coacts with chalcone synthase in the biosynthesis of 6′-deoxychalcone. FEBS Lett. 236: 221-225.
134. Welle, R., Schröder, G., Schiltz, E., Grisebach, H. and Schröder, J. 1991. Induced plant responses to pathogen attack. Analysis and heterologous expression of the key enzyme in the biosynthesis of phytoalexins in soybean (Glycine max L. Merr. cv. Harosoy 63). Eur. J. Biochem. 196: 423-430.
135. Wingender, R., Rohrig, H., Horicke, C., Wing, D. and Schell, J. 1989. Differential regulation of soybean chalcone synthase genes in plant defence, symbiosis and upon environmental stimuli. Molec. Gen. Genet. 218: 315-322.
136. 2. Plant Physiol. 115: 1405-1412.
137. Ylstra, B., Busscher, J., Franken, J., Hollman, P.C.H., Mol, J.N.M. and van Tunen, A.J. 1994. Flavonols and fertilization in Petunia hybrida: Localization and mode of action during pollen tube growth. Plant J. 6: 201-221.
138. Zava, D.T., Bien, M. and Duwe, G. 1997. Estrogenic activity of natural and synthetic estrogens in human breast cancer cells in culture. Environ. Health Perspect. Suppl. 3: 637-645.
139. Zava, D.T., Dollbaum, C.M. and Blen, M. 1998. Estrogen and progestin bioactivity of foods, herbs, and spices. Proc. Soc. Expt. Biol. Med. 217: 369-378.