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Flavonoids in seeds and grains: physiological function, agronomic importance and the genetics of biosynthesis

Published online by Cambridge University Press:  19 September 2008

Brenda Winkel Shirley
Brenda Winkel Shirley*
Affiliation:
Department of Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061-0406, USA
*
Fax: 540 231 9307 E-mail: shirley@vt.edu
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Abstract

Flavonoids are secondary metabolites that are present at high levels in most plant seeds and grains. These compounds appear to play vital roles in defence against pathogens and predators and contribute to physiological functions such as seed maturation and dormancy. At the same time, particular subclasses of flavonoids, such as the proanthocyanidins (condensed tannins), negatively impact the use of seeds and grains in animal feed and can add undesirable qualities to food products for human consumption. This article presents an overview of investigations into the physiological and agronomic aspects of seed and grain flavonoids as well as a review of molecular genetic studies, particularly in maize, Arabidopsis and soybean, where mutants deficient in flavonoid biosynthesis provide useful tools for stydying the metabolic machinery underlying the accumulation of these compounds in reproductive structures.

Keywords

Arabidopsisbarleymaizesorghumsoybeandefencefoodanimal feed
Type
Invited Review
Information
Seed Science Research , Volume 8 , Issue 4 , December 1998 , pp. 415 - 422
Copyright
Copyright © Cambridge University Press 1998

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References

Aastrup, S., Outtrup, H. and Erdal, K. (1984) Location of the proanthocyanidins in the barley grain. Carlsberg Research Communications 49, 105–109.CrossRefGoogle Scholar
Addy, E.O.H., Salami, L.I., Igboeli, L.C. and Remawa, H.S. (1995) Effect of processing on nutrient composition and anti-nutritive substances of African locust bean (Parkia filcoidea) and baobab seed (Adansonia digitata). Plant Foods for Human Nutrition 48, 113–117.CrossRefGoogle ScholarPubMed
Albert, S., Delseny, M. and Devic, M. (1997) BANYULS, a novel negative regulator of flavonoid biosynthesis in the Arabidopsis seed coat. Plant Journal 11, 289–299.CrossRefGoogle ScholarPubMed
Bernard, R.L. and Weiss, M.G. (1973) Qualitative genetics. pp 117–149in Caldwell, B.E. (Ed.) Soybeans: improvement, production and uses. Madison, WI, American Society of Agronomy.Google Scholar
Britt, A.B. and Walbot, V. (1991) Germinal and somatic products of Mul excision from the Bronze-1 gene of Zea mays. Molecular and General Genetics 227, 267–276.CrossRefGoogle Scholar
Bullard, R.W. and York, J.O. (1996) Screening grain sorghums for bird tolerance and nutritional quality. Crop Protection 15, 159–165.CrossRefGoogle Scholar
Burbulis, I.E., Pelletier, M.K., Cain, C.C. and Shirley, B.W. (1996) Are flavonoids synthesized by a multi-enzyme complex? Southern Association of Agricultural Scientists Bulletin 9, 29–36.Google ScholarPubMed
Butler, L.G. (1982) Relative degree of polymerization of sorghum tannin during seed development and maturation. Journal of Agricultural and Food Chemistry 30, 1090–1094.CrossRefGoogle Scholar
Castle, L.A. and Meinke, D.W. (1994) A FUSCA gene of Arabidopsis encodes a novel protein essential for plant development. Plant Cell 6, 25–41.Google ScholarPubMed
Coelho, J.V. and Majolo, F.M. (1993) Evolution of phenolic compounds and condensed tannins (proanthocyanidins) during the development of bean seeds (Phaseolus vulgaris L.). Archives of Latinoamerican Nutrition 43, 61–65.Google ScholarPubMed
Cone, K.C., Burr, F.A. and Burr, B. (1986) Molecular analysis of the maize anthocyanin regulatory locus Cl. Proceedings of the National Academy of Sciences, USA 83, 9631–9635.CrossRefGoogle Scholar
De Meyer, N., Haemers, A., Mishra, L., Pandey, H.-K., Pieters, L.A.C., Vanden Berghe, D.A. and Vlietinck, A.J. (1991) 4′-Hydroxy-3-methoxyflavones with potent antipicornavirus activity. Journal of Medicinal Chemistry 34, 736–746.CrossRefGoogle ScholarPubMed
de Vetten, N., Quattrocchio, F., Mol, J. and Koes, R. (1997) The an11 locus controlling flower pigmentation in petunia encodes a novel WD-repeat protein conserved in yeast, plants, and animals. Genes and Development 11, 1422–1434.CrossRefGoogle ScholarPubMed
Dooner, H.K. and Robbins, T.P. (1991) Genetic and developmental control of anthocyanin biosynthesis. Annual Review of Genetics 25, 173–199.CrossRefGoogle ScholarPubMed
Douglas, J.H., Sullivan, T.W., Gonzalez, N.J. and Beck, M.M. (1993) Differential age response of turkeys to protein and sorghum tannin levels. Poultry Science 72, 1944–1951.CrossRefGoogle Scholar
Elkin, R.G., Rogler, J.C. and Sullivan, T.W. (1991) Differential response of ducks and chicks to dietary sorghum tannins. Journal of the Science of Food and Agriculture 57, 543–553.CrossRefGoogle Scholar
Ene-Obong, H.N. and Obizoba, I.C. (1996) Effect of domestic processing on the cooking time, nutrients, antinutrients and in vitro protein digestibility of the African yambean (Sphenostylis stenocarpa). Plant Foods for Human Nutrition 49, 43–52.CrossRefGoogle ScholarPubMed
Goff, S.A., Cone, K.C. and Chandler, V.L. (1992) Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. Genes and Development 6, 864–875.CrossRefGoogle ScholarPubMed
Graham, T.L. (1991) Flavonoid and isoflavonoid distribution in developing soybean tissues and in seed and root exudates. Plant Physiology 95, 594–603.CrossRefGoogle ScholarPubMed
Grotewold, E., Athma, P. and Peterson, T. (1991) A possible hotspot for Ac insertion in the maize P gene. Molecular and General Genetics 230, 329–331.CrossRefGoogle Scholar
Harris, L.J., Currie, K. and Chandler, V.L. (1994) Large tandem duplication associated with a Mu2 insertion in Zea mays B-Peru gene. Plant Molecular Biology 25, 817–828.CrossRefGoogle ScholarPubMed
Hedin, P.A. and Waage, S.K. (1986) Roles of flavonoids in plant resistance to insects. pp. 87–100in Cody, V., Middleton, E., Harborne, J.B. (Eds) Plant flavonoids in biology and medicine: biochemical, pharmacological, and structure-activity relationships. New York, Alan R. Liss.Google Scholar
Hoeker, U., Vasil, I.K. and McCarty, D.R. (1995) Integrated control of seed maturation and germination programs by activator and repressor functions of viviparousl of maize. Genes and Development 9, 2459–2469.CrossRefGoogle Scholar
Horsley, A.D., Schwartz, P.B. and Foster, A.E. (1991) Effects of gene ant13 on agronomic and malt quality traits of barley. Crop Science 31, 593–598.CrossRefGoogle Scholar
House, W.A. and van Campen, D.R. (1994) Iron absorption by rats fed tannins extracted from bean hulls. Nutrition Research 14, 1043–1053.CrossRefGoogle Scholar
Huang, A.S., Hsieh, O.A.L. and Chang, S.S. (1981) Characterization of the nonvolatile minor constituents responsible for the objectionable taste of defatted soybean flour. Journal of Food Science 47, 19–23.CrossRefGoogle Scholar
Jambunathan, R., Butler, L.J., Bandyopadhyay, R. and Mughogho, L.K. (1986) Polyphenol concentrations in grain, leaf, and callus tissues of mould-susceptible and mould-resistant sorghum cultivars. Journal of Agricultural and Food Chemistry 34, 425–429.CrossRefGoogle Scholar
Jende-Strid, B. (1991) Gene-enzyme relations in the pathway of flavonoid biosynthesis in barley. Theoretical and Applied Genetics 81, 668–674.CrossRefGoogle ScholarPubMed
Kao, C.-Y., Cocciolone, S.M., Vasil, I.K. and McCarty, D.R. (1996) Localization and interaction of the cis-acting elements for abscisic acid, VIVIPAROUSl, and light activation of the Cl gene of maize. Plant Cell 8, 1171–1179.Google Scholar
Keung, W.M. and Vallee, B.L. (1998) Daidzin and its antidipsotropic analogs inhibit serotonin and dopamine metabolism in isolated mitochondria. Proceedings of the National Academy of Sciences USA 95, 2198–2203.CrossRefGoogle ScholarPubMed
Knight, D.C. and Eden, J.A. (1996) A review of the clinical effects of phytoestrogens. Obstetrics and Gynocology 87, 897–904.Google ScholarPubMed
Koornneef, M. (1981) The complex syndrome of ttg mutants. Arabidopsis Information Service 18, 45–51.Google Scholar
Lechelt, C., Peterson, T., Laird, A., Chen, J., Dellaporta, S.L., Dennis, E., Peacock, W.J. and Starlinger, P. (1989) Isolation and molecular analysis of the maize P locus. Molecular and General Genetics 219, 225–234.CrossRefGoogle ScholarPubMed
Levy, A.A. and Walbot, V. (1990) Regulation of the timing of transposable element excision during maize development. Science 248, 1534–1537.CrossRefGoogle ScholarPubMed
Lindstrom, J.T. and Vodkin, L.O. (1991) A soybean cell wall protein is affected by seed colour genotype. Plant Cell 3, 561–571.Google ScholarPubMed
Lloyd, A.M., Walbot, V. and Davis, R.W. (1992) Arabidopsis and Nicotiana anthocyanin production activated by maize regulators R and Cl. Science 258, 1773–1775.CrossRefGoogle Scholar
Loidl, A. and Loidl, P. (1996) Oncogene- and tumor-suppressor gene-related proteins in plants and fungi. Critical Reviews in Oncogenesis 7, 49–64.CrossRefGoogle ScholarPubMed
Marrs, K.A., Alfenito, M.R., Lloyd, A.M. and Walbot, V. (1995) A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 375, 397–400.CrossRefGoogle ScholarPubMed
Matsuura, M. and Obata, A. (1993) β-glucosidases from soybeans hydrolyze daidzin and genistin. Journal of Food Science 58, 144–147.CrossRefGoogle Scholar
Matsuura, M., Obata, A. and Fukushima, D. (1989) Objectionable flavour of soy milk developed during the soaking of soybeans and its control. Journal of Food Science 54, 602–605.CrossRefGoogle Scholar
McCarty, D.R. (1995) Genetic control and integration of maturation and germination pathways in seed development. Annual Review of Plant Physiology and Plant Molecular Biology 46, 71–93.CrossRefGoogle Scholar
McClintock, B. (1984) The significance of responses of the genome to challenge. Science 226, 792–801.CrossRefGoogle ScholarPubMed
McLaughlin, M. and Walbot, V. (1987) Cloning of a mutable bz2 allele of maize by transposon tagging and differential hybridization. Genetics 117, 771–776.CrossRefGoogle ScholarPubMed
Melake-Berhan, A., Butler, L.G., Ejeta, G. and Menkir, A. (1996) Grain mould resistance and polyphenol accumulation in sorghum. Journal of Agricultural and Food Chemistry 44, 2428–2434.CrossRefGoogle Scholar
Menkir, A., Ejeta, G., Butler, L. and Melake-Berhan, A. (1996) Physical and chemical kernel properties associated with resistance to grain mould in sorghum. Cereal Chemistry 73, 613–617.Google Scholar
Menssen, A., Höhmann, S., Martin, W., Schnable, P.S., Peterson, P.A., Saedler, H. and Gierl, A. (1990) 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 Journal 9, 3051–3057.CrossRefGoogle ScholarPubMed
Miséra, S., Müller, A.J., Weiland-Heidecker, U. and Jürgens, G. (1994) The FUSCA genes of Arabidopsis: negative regulators of light responses. Molecular and General Genetics 244, 242–252.CrossRefGoogle ScholarPubMed
Naim, M., Gestetner, B., Zilkah, S., Birk, Y. and Bondi, A. (1974) Soybean isoflavones, characterization, determination and antifungal activity. Journal of Agricultural and Food Chemistry 22, 806–810.CrossRefGoogle ScholarPubMed
Neer, E.J., Schmidt, C.J., Nambudripad, R. and Smith, T.F. (1994) The ancient regulatory-protein family of WD-repeat proteins. Nature 371, 297–300.CrossRefGoogle ScholarPubMed
Nicholas, C.D., Lindstrom, J.T. and Vodkin, L.O. (1993) Variation of proline rich cell wall proteins in soybean lines with anthocyanin mutations. Plant Molecular Biology 21, 145–156.CrossRefGoogle ScholarPubMed
O'Reilly, C., Shepherd, N.S., Pereira, A., Schwarz-Sommer, Z., Bertram, I., Robertson, D.S., Peterson, P.A. and Saedler, H. (1985) Molecular cloning of the al locus of Zea mays using the transposable elements En and Mul. EMBO Journal 4, 877–882.CrossRefGoogle Scholar
Obizoba, I.C. and Atu, L.N. (1993) Production and chemical evaluation of some food condiments of Nigeria. Plant Foods for Human Nutrition 44, 249–254.CrossRefGoogle ScholarPubMed
Oigiangbe, N.O. and Onigbinde, A.O. (1996) The association between some physico-chemical characteristics and susceptibility of cowpea (Vigna unguiculata (L.) Walp.) to Callosobruchus maculatus (F.). Journal of Stored Products Research 32, 7–11.CrossRefGoogle Scholar
Olsen, O., Wang, X. and von Wettstein, D. (1993) Sodium azide mutagenesis: Preferential generation of A • T → G • C transitions in the barley Ant18 gene. Proceedings of the National Academy of Sciences USA 90, 8043–8047.CrossRefGoogle Scholar
Ortiz, L.T., Alzueta, C., Trevino, J. and Castano, M. (1994) Effects of faba bean tannins on the growth and histological structure of the intestinal tract and liver of chicks and rats. British Poultry Science 35, 743–757.CrossRefGoogle ScholarPubMed
Parcy, F., Valon, C., Raynal, M., Gaubier-Comella, P., Delseny, M. and Giraudat, J. (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6, 1567–1582.Google ScholarPubMed
Pelletier, M.K., Murrell, J. and Shirley, B.W. (1997) Arabidopsis flavonol synthase and leucoanthocyanidin dioxygenase: further evidence for distinct regulation of “early” and “late” flavonoid biosynthetic genes. Plant Physiology 113, 1437–1445.CrossRefGoogle Scholar
Pratt, D.E. and Birac, P.M. (1979) Source of antioxidant activity of soybeans and soy products. Journal of Food Science 44, 1720–1722.CrossRefGoogle Scholar
Procissi, A., Dolfini, S., Ronchi, A. and Tonelli, C. (1997) Light-dependent spatial and temporal expression of pigment regulatory genes in developing maize seeds. Plant Cell 9, 1547–1557.CrossRefGoogle ScholarPubMed
Ralston, E.J., English, J.J. and Dooner, H.K. (1988) Sequence of three bronze alleles of maize and correlation with the genetic fine structure. Genetics 119, 185–197.CrossRefGoogle ScholarPubMed
Sainz, M.B., Grotewold, E. and Chandler, V.L. (1997) Evidence for direct activation of an anthocyanin promoter by the maize Cl protein and comparison of DNA binding by related Myb domain proteins. Plant Cell 9, 611–625.Google Scholar
Salunkhe, D.K., Jadhav, S.J., Kadam, S.S. and Chavan, J.K. (1982) Chemical, biochemical, and biological significance of polyphenols in cereals and legumes. CRC Critical Reviews in Food Science and Nutrition 17, 277–305.CrossRefGoogle ScholarPubMed
Shirley, B.W. (1996) Flavonoid biosynthesis: “new” functions for an “old” pathway. Trends in Plant Science 1, 377–382.Google Scholar
Shirley, B.W., Kubasek, W.L., Storz, G., Bruggemann, E., Koornneef, M., Ausubel, F.M. and Goodman, H.M. (1995) Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant Journal 8, 659–671.CrossRefGoogle ScholarPubMed
Siddhuraju, P., Vijayakumari, K. and Janardhanan, K. (1994) Chemical analysis and nutritional assessment of the less known pulses, Vigna aconitifolia (Jacq.) Marechal and Vigna vexillata (L.) A. Rich. Plant Foods for Human Nutrition 45, 103–111.CrossRefGoogle ScholarPubMed
Sommer, H., Bonas, U. and Saedler, H. (1988) Transposon-induced alterations in the promoter region affect transcription of the chalcone synthase gene of Antirrhinum majus. Molecular and General Genetics 211, 49–55.CrossRefGoogle ScholarPubMed
Stafford, H.A. (1988) Proanthocyanidins and the lignin connection. Phytochemistry 27, 1–6.CrossRefGoogle Scholar
Stafford, H.A. (1990) Flavonoid metabolism. Boca Raton, CRC Press.Google Scholar
Stanton, W.R. and Francis, B.J. (1966) Ecological significance of anthocyanins in the seed coats of the Phaseoleae. Nature 211, 970–971.CrossRefGoogle Scholar
Tanaka, A., Shigemitsu, T., Yokota, Y. and Shika, N. (1997) A new Arabidopsis mutant induced synthesis with spotted pigmentation. Genes and Genetic Systems 72, 141–148.CrossRefGoogle ScholarPubMed
Thatiparthi, V.R., Dinesh-Kumar, S.P. and Peterson, P.A. (1995) Permanent fixation of a transposable element insert in the A2 gene of maize (Zea mays L.). Journal of Heredity 86, 167–171.CrossRefGoogle ScholarPubMed
Todd, J.J. and Vodkin, L.O. (1996) Duplications that suppress and deletions that restore expression from a chalcone synthase multigene family. Plant Cell 8, 687–699.CrossRefGoogle ScholarPubMed
Tsuda, T., Shiga, K., Ohshima, K., Kawakishi, S. and Osawa, T. (1996) Inhibition of lipid peroxidation and the active oxygen radical scavenging effect of anthocyanin pigments isolated from Phaseolus vulgaris L. Biochemical Pharmacology 52, 1033–1039.CrossRefGoogle ScholarPubMed
van der Meer, I.M., Stuitje, A.R. and Mol, J.N.M. (1993) Regulation of general phenylpropanoid and flavonoid gene expression. pp. 125–155in Verma, D.P.S. (Ed.) Control of plant gene expression. Boca Raton, CRC Press.Google Scholar
van der Poel, A.F.B., Dellaert, L.M.W., van Norel, A. and Helsper, J.P.F.G. (1992) The digestibility in piglets of faba bean (Vicia faba L.) as affected by breeding towards the absence of condensed tannins. British Journal of Nutrition 68, 793–800.CrossRefGoogle ScholarPubMed
von Wettstein, D., Jende-Strid, B., Ahrenst-Larsen, B. and Sørensen, J.A. (1977) Biochemical mutant in barley renders chemical stabilization of beer superfluous. Carlsberg Research Communications 42, 341–351.CrossRefGoogle Scholar
von Wettstein, D., Nilan, R.A., Ahrenst-Larsen, B., Erdal, K., Ingversen, J., Jende-Strid, B., Kristiansen, K.N., Larsen, J., Outtrup, H. and Ullrich, S.E. (1985) Proanthocyanidin-free barley for brewing: -progress in breeding for high yield and research tool in polyphenol chemistry. Technical Quarterly of the Master Brewers Association of America 22, 41–52.Google Scholar
Wienand, U., Weydemann, U., Niesbach-Kösgen, U., Peterson, P.A. and Saedler, H. (1986) Molecular cloning of the c2 locus of Zea mays, the gene coding for chalcone synthase. Molecular and General Genetics 203, 202–207.CrossRefGoogle Scholar
Yu, F., McNabb, W.C., Barry, T.N. and Waghorn, G.C. (1995) Effect of condensed tannin in cottonseed hulls upon the in vitro degradation of cottonseed kernel proteins by rumen microorganisms. Journal of the Science of Food and Agriculture 69, 223–234.CrossRefGoogle Scholar
Zanta, C.A., Yang, X., Axtell, J.D. and Bennetzen, J.L. (1994) The candystripe locus, y-cs, determines mutable pigmentation of the sorghum leaf, flower, and pericarp. Journal of Heredity 85, 23–29.Google Scholar