The Botanical Review

, Volume 63, Issue 1, pp 27–39

Roles of flavonoids in symbiotic and defense functions in legume roots

  • Helen A. Stafford


The roles of flavonoids in roots of legumes in the symbiotic relationships with nitrogen-fixing bacteria and arbuscular mycorrhizal fungi are compared with defense functions, using examples from three legume genera,Lotus, Medicago, andGlycine. Pathways leading to proanthocyanidins and isoflavonoids are emphasized. The localization of flavonoids in nodules involved in nitrogen fixation and in the apoplastic compartment of mycorrhizal associations is briefly described, with emphasis on the need for more information concerning their precise localization. Also emphasized are the limits of our knowledge about the regulatory genes of the flavonoid pathway involved in both exogenous and endogenous regulation of these complex interrelationships.


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Literature Cited

  1. Barz, W. &R. Welle. 1992. Biosynthesis and metabolism of isoflavones and pterocarpan phytoalexins in chickpea, soybean, and phytopathogenic fungi. Recent Adv. Phytochem.26:139–164.Google Scholar
  2. Bauchrowitz, M. A., D. G. H. Barker &G. Truchet. 1995. Lectin genes are expressed throughout root nodule development and during nitrogen-fixation in theRhizobium-Medicago symbiosis. Pl. J.9: 31–43.CrossRefGoogle Scholar
  3. Bergersen, F. J. 1982. Root nodules of legumes: Structure and functions. John Wiley, New York.Google Scholar
  4. Bonfante, P. &S. Perotto. 1995. Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytol.130: 3–21.CrossRefGoogle Scholar
  5. Brewin, N. J. 1991. Development of the legume root nodule. Ann. Rev. Cell Biol.7: 191–226.PubMedGoogle Scholar
  6. Brown, S. M. &K. B. Walsh. 1994. Anatomy of the legume nodule cortex with respect to nodule permeability. Austral. J. Pl. Physiol.21: 49–68.CrossRefGoogle Scholar
  7. Carron, T. R., M. P. Robbins &P. Morris. 1994. Genetic modification of condensed tannin biosynthesis inLotus corniculatus. 1. Heterologous antisense dihydroflavonol reductase down-regulated tannin accumulation in “hairy root” cultures. Appl. Genet.87: 1006–1015.Google Scholar
  8. Charrier, B. C., P. Cornonao, A. Kondorosi &P. Ratet. 1995. Molecular characterization and expression of alfalfa (Medicago sativa L.) flavanone-3-hydroxylase and dihydroflavonol-4-reductase encoding genes. PL Molec. Biol.29: 773–786.CrossRefGoogle Scholar
  9. Cooper, J. E. &J. R. Rao. 1992. Localized changes in flavonoid biosynthesis in roots ofLotus pedunculatus after infection byRhizobium loti. Pl. Physiol.100: 444–450.Google Scholar
  10. Cronquist, A. 1988. The evolution and classification of flowering plants. Ed. 2. New York Botanical Garden, Bronx.Google Scholar
  11. Dalton, D. A., L. M. Baird, L. Langeberg, C. Y. Taugher, W. R. Anyan, C. P. Vance &G. Sarath. 1993. Subcellular localization of oxygen defense enzymes in soybean (Glycine max L. Men.) root nodules. Pl. Physiol.102: 481–489.Google Scholar
  12. Dewick, P. M. 1994. Isoflavonoids. Pages 117–238 in J. B. Harborne (ed.), The flavonoids. Chapman & Hall, London.Google Scholar
  13. Dixon, R. A. &N. L. Paiva. 1995. Stress-induced phenylpropanoid metabolism. Pl. Cell7: 1085–1097.Google Scholar
  14. —,M. J. Harrison &N. L. Paiva. 1995. The isoflavonoid phytoalexin pathway: From enzymes to genes to transcription factors. Physiol. Pl.93: 385–392.CrossRefGoogle Scholar
  15. Foo, L. Y. &L. J. Porter. 1980. The phytochemistry of proanthocyanidin polymers. Phytochemistry19: 1747–1754.CrossRefGoogle Scholar
  16. —,R. Newman, G. Waghorn, W. C. McNabb &M. J. Ulyatt. 1996. Proanthocyanidins fromLotus comiculatus. Phytochemistry41: 617–624.CrossRefGoogle Scholar
  17. Forkman, G. 1994. Genetics of flavonoids. Pages 537–564 in J. B. Harborne (ed.), The flavonoids. Chapman & Hall, London.Google Scholar
  18. Gianinazzi-Pearson, V., A. Gollotte, J. Lherrminier, B. Tisserant, P. Franken, E. Dumas-Gaudot, M.-C. Lemoine, D. van Tunimen &S. Gianinazzi. 1995. Cellular and molecular approaches in the characterization of symbiotic events in functional arbuscular mycorrhizal associations. Canad. J. Bot.73(Suppl. 1): S526-S532.Google Scholar
  19. Grady, H., R. G. Palmer &J. Imsande. 1995. Isoflavonoids in root and hypocotyl of soybean seedlings (Glycine max, Fabaceae). Amer. J. Bot.82: 964–968.CrossRefGoogle Scholar
  20. Graham, T. L. 1991. Flavonoid and isoflavonoid distribution in developing soybean seedling tissues and in seed and root exudates. Pl. Physiol.95: 594–603.Google Scholar
  21. Grandmaison, J. &R. Ibrahim. 1995. Ultrastructural localization of a diprenylated isoflavone inRhizobium lupini-Lupinus albus symbiotic association. J. Exp. Bot.46: 231–237.CrossRefGoogle Scholar
  22. Grant, W. F. 1995. A chromosome atlas and interspecific-intergenic index forLotus andTetragonolobus (Fabaceae). Canad. J. Bot.73: 1787–1809.Google Scholar
  23. Guo, L. &N. L. Paiva. 1995. Molecular cloning and expression of alfalfa (Medicago sativa L.) vestitone reductase, the penultimate enzyme in medicarpin biosynthesis. Arch. Biochem. Biophys.320: 353–360.PubMedCrossRefGoogle Scholar
  24. Handburg, K. &J. Stougaard. 1992.Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. Pl. J.2: 487–496.CrossRefGoogle Scholar
  25. Harrison, M. J. &R. A. Dixon. 1994. Spatial patterns of expression of flavonoid/isoflavonoid pathway genes during interactions between roots ofMedicago truncatula and the mycorrhizal fungusGlomus versiforme. Pl. J.6: 9–20.CrossRefGoogle Scholar
  26. Heller, W. &G. Forkman. 1994. Biosynthesis of flavonoids. Pages 499–535 in J. B. Harborne (ed.), The flavonoids. Chapman & Hall, London.Google Scholar
  27. Hirsch, A. M. 1992. Developmental biology of legume nodulation. New Phytol.122: 211–237.CrossRefGoogle Scholar
  28. Karr, R. B., D. W. Emerich &A. L. Karr. 1992. Accumulation of the phytoalexin, glyceollin in root nodules of soybean formed by effective and ineffective strains ofBradyrhizobium japonicum. J. Chem. Ecol.18: 997–1008.CrossRefGoogle Scholar
  29. Kuc, J. 1995. Phytoalexins, stress metabolism, and disease resistance in plants. Annual Rev. Phytopath.33: 275–297.CrossRefGoogle Scholar
  30. Lambais, M. R. &M. C. Mehdy. 1995. Differential expression of defense-related genes in arbuscular mycorrhiza. Canad. J. Bot.73(Suppl. 1): S533-S540.Google Scholar
  31. Mellor, R. B. &D. B. Collinge. 1995. A simple model based on known plant defence reactions is sufficient to explain most aspects of nodulation. J. Exp. Bot.46: 1–18.CrossRefGoogle Scholar
  32. Meyer, A. D. &R. B. Mellor. 1993. NOD-active compounds in soya nodules. J. Pl. Physiol.142: 57–60.Google Scholar
  33. Morris, P. &M. P. Robbing. 1992. Condensed tannin formation byAgrobacterium rhizogenes transformed root and shoot organ cultures ofLotus corniculatus. J. Exp. Bot.43: 221–231.CrossRefGoogle Scholar
  34. Müller, P., A. Klaucke &E. Wengel. 1995. TnphoA-induced symbiotic mutants ofBradyrhizobium japonicum that impair cell and tissue differentiation inGlycine max nodules. Planta197: 163–175.Google Scholar
  35. Mylona, P., K. Pawlowski &T. Bisseling. 1995. Symbiotic nitrogen fixation. Pl. Cell7: 869–885.Google Scholar
  36. Oger, P., A. Petit &Y. Desaux. 1996. A simple technique for direct transformation and regeneration of the diploid legume speciesLotus japonicus. Pl. Sci.116: 159–168.CrossRefGoogle Scholar
  37. Pankhurst, C. E. &W. T. Jones. 1979a. Effectiveness ofLotus root sensitivity of fast-growing rhizobia to flavolans. J. Exp. Bot.30:1095–1107.CrossRefGoogle Scholar
  38. — &W. T. Jones. 1979b. Effectiveness ofLotus root nodules. III. Effect of combined nitrogen on nodule effectiveness and flavolan synthesis in plant roots. J. Exp. Bot.30: 1109–1118.CrossRefGoogle Scholar
  39. —,A. S. Craig &W. T. Jones. 1979. Effectiveness of root nodules rhizobia. J. Exp. Bot.30: 1085–1093.CrossRefGoogle Scholar
  40. Perlick, A. M., M. Frühling, G. Schroder, S. C. Frosch &A. Pühler. 1996. The broad bean gene VfNOD32 encodes a nodulin with sequence similarities to chitinases that is homologous to (a/b)8-barrel type seed proteins. Pl. Physiol.110:147–154.CrossRefGoogle Scholar
  41. Phillips, D. A. 1992. Flavonoids: Plant signals to soil microbes. Recent Adv. Phytochem.26: 201–231.Google Scholar
  42. Polhill, R. M. &P. H. Raven, eds. 1981. Advances in legume systematics. Part 2. Royal Botanic Gardens, Kew.Google Scholar
  43. Rao, A. S. 1990. Root flavonoids. Bot. Rev. (Lancaster)56: 1–84.Google Scholar
  44. Robbins, M. P., B. Thomas, P. Morris. 1995. Phenylpropanoid defence responses in transgenicLotus corniculatus. J. Exp. Bot.46: 513–524.CrossRefGoogle Scholar
  45. Sagan, M., D. Morandi, E. Tarenghi &G. Duc. 1995. Selection of nodulation and mycorrhizal mutants in the model plantMedicago truncatula (Gaertn.) after γ-ray mutagenesis. Pl. Sci.111: 63–71.CrossRefGoogle Scholar
  46. Sallaud, C., J. El-Turk, C. Breda, D. Bluffard, I. de Kozk &R. Esnault. 1995a. Differential expression of cDNA coding for chalcone reductase, a key enzyme of the 5-deoxyflavonoid pathway, under various stress conditions inMedicago sativa. Pl. Sci.109: 179–190.CrossRefGoogle Scholar
  47. ——,C. L. Bigarre, H. Sevin, R. Welle &R. Esnault. 1995b. Nucleotide sequences of three chalcone reductase genes from alfalfa. Pl. Physiol.108: 869–870.CrossRefGoogle Scholar
  48. Soltis, D. E., P. S. Soltis, D. S. Morgan, S. S. Swensen, B. C. Mullin, J. M. Dowd &B. C. Martin. 1995. Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc. Natl. Acad. Sci.92: 2647–2641.PubMedCrossRefGoogle Scholar
  49. Sprent J. I. &Embrapa. 1980. Root nodule anatomy, type of export product, and evolutionary origin in some Leguminosae. Pl. Cell & Environ.3: 35–43.Google Scholar
  50. Staehelin, C., J. Müller, R. B. Mellor, A. Wiemken &T. Boiler. 1992. Chitinase and peroxidase in effective (fix+) and ineffective (fix) soybean nodules. Planta187: 295–300.CrossRefGoogle Scholar
  51. Stafford, H. A. 1991. Flavonoid evolution: An enzymic approach. Pl. Physiol.96: 680–685.CrossRefGoogle Scholar
  52. —. 1995. Metabolism and regulation of phenolics: Gaps in our knowledge. Pages 15–30 in L. Gustine & H. E. Flores (eds.), Phytochemicals and health. Plenum Press, New York.Google Scholar
  53. Stroczycki, P. M. &A. B. Logocki. 1995. Leghemoglobins from an evolutionarily old legume,Lupinus luteus. Pl. Sci.110: 83–89.CrossRefGoogle Scholar
  54. Thykjaer, T., J. Stiller, K. Handberg, J. Jones &J. Stougaard. 1995. The maize transposable element AC is mobile in the legumeLotus japonicus. Pl. Molec. Biol.27: 981–993.CrossRefGoogle Scholar
  55. Suganuma, N. H., K. Yamauchi &K. Yamamoto. 1995. Enhanced production of ethylene by soybean roots after inoculation withBradyrhizobium japonicum. Pl. Sci.111: 163–168.CrossRefGoogle Scholar
  56. Utrup, L. J. &J. H. Norris. 1996. Nodulin gene expression in effective root nodules of white sweetclover (Melilotos alba Desr.) and in ineffective nodules elicited by mutant strains ofRhizobium meliloti. J. Exp. Bot.47: 195–202.CrossRefGoogle Scholar
  57. Volpin, H., D. A. Phillips, Y. Okon &Y. Kapulnik. 1996. Suppression of an isoflavonid phytoalexin defense response in mycorrhizal alfalfa roots. Pl. Physiol.108: 1449–1454.Google Scholar
  58. Wang, C.-S., J. J. Todd &L. O. Vodkin. 1994. Chalcone synthase mRNA and activity are reduced in yellow soybean seed coats with dominant I alleles. Pl. Physiol.105: 739–748.CrossRefGoogle Scholar
  59. Xie, Z.-P., C. Staehelin, H. Vierheilig, A. Wiemken, S. Jabbouri, W. J. Broughton, R. Vogeli-Lange &T. Boiler. 1995. Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Pl. Physiol.108:1519–1525.Google Scholar

Copyright information

© The New York Botanical Garden 1997

Authors and Affiliations

  • Helen A. Stafford
    • 1
  1. 1.Biology DepartmentReed CollegePortlandUSA

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