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Roles of flavonoids in symbiotic and defense functions in legume roots

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Abstract

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

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bergersen, F. J. 1982. Root nodules of legumes: Structure and functions. John Wiley, New York.

    Google Scholar 

  • Bonfante, P. &S. Perotto. 1995. Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytol.130: 3–21.

    Article  Google Scholar 

  • Brewin, N. J. 1991. Development of the legume root nodule. Ann. Rev. Cell Biol.7: 191–226.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Cronquist, A. 1988. The evolution and classification of flowering plants. Ed. 2. New York Botanical Garden, Bronx.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Dewick, P. M. 1994. Isoflavonoids. Pages 117–238 in J. B. Harborne (ed.), The flavonoids. Chapman & Hall, London.

    Google Scholar 

  • Dixon, R. A. &N. L. Paiva. 1995. Stress-induced phenylpropanoid metabolism. Pl. Cell7: 1085–1097.

    CAS  Google Scholar 

  • —,M. J. Harrison &N. L. Paiva. 1995. The isoflavonoid phytoalexin pathway: From enzymes to genes to transcription factors. Physiol. Pl.93: 385–392.

    Article  CAS  Google Scholar 

  • Foo, L. Y. &L. J. Porter. 1980. The phytochemistry of proanthocyanidin polymers. Phytochemistry19: 1747–1754.

    Article  CAS  Google Scholar 

  • —,R. Newman, G. Waghorn, W. C. McNabb &M. J. Ulyatt. 1996. Proanthocyanidins fromLotus comiculatus. Phytochemistry41: 617–624.

    Article  CAS  Google Scholar 

  • Forkman, G. 1994. Genetics of flavonoids. Pages 537–564 in J. B. Harborne (ed.), The flavonoids. Chapman & Hall, London.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Graham, T. L. 1991. Flavonoid and isoflavonoid distribution in developing soybean seedling tissues and in seed and root exudates. Pl. Physiol.95: 594–603.

    CAS  Google Scholar 

  • Grandmaison, J. &R. Ibrahim. 1995. Ultrastructural localization of a diprenylated isoflavone inRhizobium lupini-Lupinus albus symbiotic association. J. Exp. Bot.46: 231–237.

    Article  CAS  Google Scholar 

  • Grant, W. F. 1995. A chromosome atlas and interspecific-intergenic index forLotus andTetragonolobus (Fabaceae). Canad. J. Bot.73: 1787–1809.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Handburg, K. &J. Stougaard. 1992.Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. Pl. J.2: 487–496.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Heller, W. &G. Forkman. 1994. Biosynthesis of flavonoids. Pages 499–535 in J. B. Harborne (ed.), The flavonoids. Chapman & Hall, London.

    Google Scholar 

  • Hirsch, A. M. 1992. Developmental biology of legume nodulation. New Phytol.122: 211–237.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Kuc, J. 1995. Phytoalexins, stress metabolism, and disease resistance in plants. Annual Rev. Phytopath.33: 275–297.

    Article  CAS  Google Scholar 

  • Lambais, M. R. &M. C. Mehdy. 1995. Differential expression of defense-related genes in arbuscular mycorrhiza. Canad. J. Bot.73(Suppl. 1): S533-S540.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Meyer, A. D. &R. B. Mellor. 1993. NOD-active compounds in soya nodules. J. Pl. Physiol.142: 57–60.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • Mylona, P., K. Pawlowski &T. Bisseling. 1995. Symbiotic nitrogen fixation. Pl. Cell7: 869–885.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Pankhurst, C. E. &W. T. Jones. 1979a. Effectiveness ofLotus root sensitivity of fast-growing rhizobia to flavolans. J. Exp. Bot.30:1095–1107.

    Article  CAS  Google Scholar 

  • — &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.

    Article  CAS  Google Scholar 

  • —,A. S. Craig &W. T. Jones. 1979. Effectiveness of root nodules rhizobia. J. Exp. Bot.30: 1085–1093.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Phillips, D. A. 1992. Flavonoids: Plant signals to soil microbes. Recent Adv. Phytochem.26: 201–231.

    CAS  Google Scholar 

  • Polhill, R. M. &P. H. Raven, eds. 1981. Advances in legume systematics. Part 2. Royal Botanic Gardens, Kew.

    Google Scholar 

  • Rao, A. S. 1990. Root flavonoids. Bot. Rev. (Lancaster)56: 1–84.

    Google Scholar 

  • Robbins, M. P., B. Thomas, P. Morris. 1995. Phenylpropanoid defence responses in transgenicLotus corniculatus. J. Exp. Bot.46: 513–524.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • ——,C. L. Bigarre, H. Sevin, R. Welle &R. Esnault. 1995b. Nucleotide sequences of three chalcone reductase genes from alfalfa. Pl. Physiol.108: 869–870.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Sprent J. I. &Embrapa. 1980. Root nodule anatomy, type of export product, and evolutionary origin in some Leguminosae. Pl. Cell & Environ.3: 35–43.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Stafford, H. A. 1991. Flavonoid evolution: An enzymic approach. Pl. Physiol.96: 680–685.

    Article  CAS  Google Scholar 

  • —. 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 

  • Stroczycki, P. M. &A. B. Logocki. 1995. Leghemoglobins from an evolutionarily old legume,Lupinus luteus. Pl. Sci.110: 83–89.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Suganuma, N. H., K. Yamauchi &K. Yamamoto. 1995. Enhanced production of ethylene by soybean roots after inoculation withBradyrhizobium japonicum. Pl. Sci.111: 163–168.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

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  1. Biology Department, Reed College, 97202, Portland, Oregon, USA

    Helen A. Stafford

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  1. Helen A. Stafford
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Stafford, H.A. Roles of flavonoids in symbiotic and defense functions in legume roots. Bot. Rev 63, 27–39 (1997). https://doi.org/10.1007/BF02857916

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