Role of Flavonoid and Isoflavonoid Molecules in Symbiotic Functioning and Host-Plant Defence in the Leguminosae

Chapter

Abstract

Inoculating symbiotic legumes with infective rhizobial symbionts increases the nod-gene-inducing activity of root exudates, and alters the profile of nod gene inducers. The application of Sinorhizobium meliloti cells to the roots of alfalfa seedlings specifically causes the release of the aglycone and glycoside forms of the phytoalex in medicarpin, and a formononetin—O-(6″-O-malnylglycoside). Similarly, in the presence of Rhizobium leguminosarum biovar phaseoli bacteria, root exudates of common bean also contain more of the phytoalexin coumestrol, and its isoflavonoid precursor daidzein than exudates of uninoculated plants. This paper discusses the effects of root-nodule bacteria (hereafter called “rhizobia”) on the synthesis and release of flavonoid and isoflavonoid signal compounds, and explores the biological significance of phytoalexin production in legume plant nodulation and defense against pathogens and insect pests.

Keywords

Arbuscular Mycorrhizal Fungus Root Exudate Phenylpropanoid Pathway Rhizobium Leguminosarum Bradyrhizobium Japonicum 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Caetano-Annoles G, Christ-Estes D, Bauer WD (1988) Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J Bacteriol 170:3164–3169Google Scholar
  2. 2.
    Harwig UA, Joseph CM, Phillips DA (1991) Flavonoids released naturally from alfalfa seeds enhance growth rate of Rhizobium meliloti. Plant Physiol 95:797–803CrossRefGoogle Scholar
  3. 3.
    Peters NK, Frost JW, Long SR (1986) A plant flavone.luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977–980CrossRefGoogle Scholar
  4. 4.
    Redmond JW, Batley M, Djordjevic MA, Innes RW, Kuempel PL, Rolfe BG (1986) Flavones induce expression of nodulation genes in Rhizobium. Nature 323:632–635CrossRefGoogle Scholar
  5. 5.
    Harwig UA, Maxwell CA, Joseph CM, Phillips DA (1990) Chrysoeriol and luteolin released from alfalfa seeds induce nod genes in Rhizobium meliloti. Plant Physiol 92:116–122CrossRefGoogle Scholar
  6. 6.
    Maxwell CA, Hartwig UA, Joseph CM, Phillips DA (1989) Achalcone and two related flavonoids released from alfalfa roots induce nod genes of Rhizobium meliloti. Plant Physiol 91:842–847CrossRefGoogle Scholar
  7. 7.
    Phillips DA, Joseph CM, Maxwell CA (1992) Trigonelline and stachydrine released from alfalfa seeds activate NodD2 protein in Rhizobium meliloti. Plant Physiol 99:1526–1531CrossRefGoogle Scholar
  8. 8.
    Hungria M, Joseph CM, Phillips DA (1991) Anthocyanidins and flavonols, major nod-gene inducers from seeds of a black-seeded common bean. Plant Physiol 97:751–758CrossRefGoogle Scholar
  9. 9.
    Hungria M, Joseph CM, Phillips DA (1991) Rhizobium nod-gene inducers exuded naturally from roots of common bean (Phaseolus vulgaris L.). Plant Physiol 97:759–764CrossRefGoogle Scholar
  10. 10.
    Recourt K, Schripsema J, Kinje JW, Van Brussel AAN, Lugtenberg BJJ (1991) Inoculation of Vicia sativa subsp. nigra roots with Rhizobium leguminosarum biovar viciae results in release of nod gene activating tlavanones and chalcones. Plant Mol Biol 16:841–852CrossRefGoogle Scholar
  11. 11.
    Fisher RF, Long SR (1993) Rhizobium—plant signal exchange. Nature 357:655–659CrossRefGoogle Scholar
  12. 12.
    Rolfe BG, Batley M, Redmond JW, Richardson AE, Simpson RJ, Bassam B, Sargent CL, Weinman JI, Djordjevic MA, Dasso FB (1988) Phenolic compounds secreted by legumes. In: Bothe H, de Bruijn FJ, Newton WE (eds) Nitrogen fixation: hundred years after. Gustav Fischer, Stuttgart, p 405Google Scholar
  13. 13.
    Van Brussel AAN, Recourt K, Pees E, Spaink H, Tak T, Wijffelman CA, Kijne JW, Lugtenberg BJ (1990) A biovar-specific signal of Rhizobium leguminosarum bv. viciae induces increased nodulation gene-inducing activity in root exudate of Vicia sativa subsp. nigra. J Bacteriol 172:5394–5401Google Scholar
  14. 14.
    Hargreaves JA, Mansfield JW, Coxon DT (1976) Identification of medicarpin as a phytoalexin in the broad bean plant (Vicia faba L.). Nature 262:318–319CrossRefGoogle Scholar
  15. 15.
    Dakora FD, Joseph CM, Phillips DA (1993) Alfalfa (Midicago sativum L.) root exudates contain isoflavonoids in the presence of Rhizobium meliloti. Plant Physiol 101:819–824Google Scholar
  16. 16.
    Dakora FD, Joseph CM, Phillips DA (1993) Common bean root exudates contain elevated levels of diadzein and coumestrol in response to Rhizobium inoculation. Mol Plant Microbe Interact 6:665–668CrossRefGoogle Scholar
  17. 17.
    Schmidt PE, Parniske M, Werner D (1992) Production of the phytoalexin glyceollin I by soyabean roots in response to symbiotic and pathogenic infection. Bot Acta 105:18–25Google Scholar
  18. 18.
    Morandi D, Bailey J, Gianinazzi-Pearson V (1984) Isoflavonoid accumulation in soyabean roots infected with vesicular-arbuscular fungi. Physiol Plant Pathol 24:357–364CrossRefGoogle Scholar
  19. 19.
    VolPin H, Elking Y, Okon Y, Kapulnik Y (1994) A vesicular-arbuscular mycorrhizal fungus (Glomus intraradix) induces a defence response in alfalfa roots. Plant Physiol 104:683–689Google Scholar
  20. 20.
    Wyss P, Boller T, Wiemken A (1991) Phytoalexin response is elicited by a pathogen (Rhizoctonia solani) but not by a mycorrhizal fungus (Glomus mosseae) in soyabean roots. Experientia 47:395–399CrossRefGoogle Scholar
  21. 21.
    Werner D, Mellor RB, Hahn MG, Grisebach H (1985) Soyabean root response to symbiotic infection. Glyceollin I accumulation in an ineffective type of soyabean nodules with an early loss of the peribacteroid membrane. Z Narurforsch 40:179–181Google Scholar
  22. 22.
    Wyss P, Mellor RB, Wiemken A (1990) Vesicular-arbuscular mycorrhizas of wild-type soyabean and non-nodulating mutants with Glomus mosseae contain symbiosis-specific polypeptides (mycorrizins). Immunologically cross-reactive with nodulins. Planta 182:22–26CrossRefGoogle Scholar
  23. 23.
    Morris PF, Ward EWB (1992) Chemoattraction of zoospores of the soyabean pathogen, Phytophthora sojae, by isoflavones. Physiol Mol Plant Pathol 40:17–22CrossRefGoogle Scholar
  24. 24.
    Cruickshank LAM (1962) Studies on phytoalexins. IV. The antimicrobial spectrum of pisatin. Aust J Biol Sci 15:147–159Google Scholar
  25. 25.
    Pankhurst CE, Biggs DR (1980) Sensitivity of Rhizobium to selected isoflavonoids. Can J Microbiol 26:542–545CrossRefGoogle Scholar
  26. 26.
    Parsnike M, Ahlborn B, Werner D (1991) Isoflavonoid-inducible resistance to phytoalexin glyceollin in soyabean rhizobia. J Bacteriol 173:3432–3439Google Scholar
  27. 27.
    Vanetten HD, Mathews DE, Mathews PS (1989) Phytoalexin detoxification: importance for pathogenicity and practical implications. Ann Rev Phytopathol 27:143–164CrossRefGoogle Scholar
  28. 28.
    Rao JR, Sharma ND, Hamilton JTG, Boyd DR, Cooper IE (1991) Biotransformation of the pentahydroxy flavone quercetin by Rhizobium loti and Bradyrhizobium strains (lotus). Appl Environ Microbiol 57:1563–1565Google Scholar
  29. 29.
    Kape R, Parniske M, Brandt S, Werner D (1992) Isoliquiritigenin, a strong nod gene- and glyceollin resistance-inducing flavonoid from soyabean root exudate. Appl Environ Microbiol 58:1705–1710Google Scholar
  30. 30.
    Denny TP, Vanetten HD (1983) Tolerance of Nectria haematococca MP VI to the phytoalexin pisatin in the absence of detoxification. J Gen Microbiol 129:2893–2901Google Scholar
  31. 31.
    Denny TP, Vanetten HD (1983) Characterisation of an inducible, non-degradative tolerance of Netria haematococca MP VI to phytoalexins. J Gen Microbiol 129:2903–2913Google Scholar
  32. 32.
    Giannini Jl, Briskin DP, Holt JS, Paxton JD (1988) Inhibition of plasma membrane and tonoplast H+-transporting ATPases by glyceollin. Phytopathology 70:894–896Google Scholar
  33. 33.
    Boydstron R, Paxton JD, Koeppe DE (1983) Glyceollin: a site-specific inhibitor of electron transport in isolated soyabean mitochondrion. Plant Physiol 72:151–155CrossRefGoogle Scholar
  34. 34.
    Hungria M, Phillips DA (1993) Effects of a seed colour mutation on rhizobial nod-gene-inducing flavonoids and nodulation in common bean. Mol Plant Microbe Interact 6:418–422CrossRefGoogle Scholar
  35. 35.
    Kapulnik Y, Joseph CM, Phillips DA (1987) Flavone limitations to root nodulation and symbiotic nitrogen fixation in alfalfa. Plant Physiol 84:1193–1196CrossRefGoogle Scholar
  36. 36.
    Smit G, Puvanesarajah V, Carlson RW, Barbour WM, Stacey G (1992) Bradyrhizobium japonicum nodD I can be specifically induced by soyabean tlavonoids that do not induce the nodY ABCSUIJ operon. J Biol Chem 267:310–318Google Scholar
  37. 37.
    Kosslak RM, Bookland R, Barkei J, Paaren HE, Appelbaum ER (1987) Induction of bradyrhizobium japonicum common nod genes by isoflavones isolated from glycine max. Proc Natl Acad Sci U S A 84:7428–7432CrossRefGoogle Scholar
  38. 38.
    Kosslak RM, Joshi RS, Bowen BA, Paaren HE, Appelbaum ER (1990) Strain-specific inhibition of nod-gene induction in Bradyrhizobium japonicum by flavonoid compounds. Appl Environ Microbiol 56:1333–1341Google Scholar
  39. 39.
    Morris PF, Savard ME, Ward EWB (1991) Identification and accumulation of isoflavonoids and isoflavone glucosides in soyabean leaves and hypocotyls in resistance responses to Phytophthora megasperma f.sp. glycinea. Physiol Mol Plant Pathol 39:229–244CrossRefGoogle Scholar
  40. 40.
    Hahlbrock K, Grisebach H (1975) Biosynthesis offlavonoids. In: Harbome JB, Mabry TJ, Mabry H (eds) The flavonoids Part 2. Academic Press, New York, pp 866–915Google Scholar
  41. 41.
    Masaoka Y, Kojima M, Suguhara S, Yoshihara T, Koshino M, Ichihara A (1993) Dissolution of ferric phosphate by alfalfa (Medicago satim L.) root exudates. Plant Soil 155(156):75–78CrossRefGoogle Scholar
  42. 42.
    Essalmani H, Lahlou H (2003) Bioprotection mechanisms of the lentil plant by Rhizobium leguminosarum against Fusarium oxysporum f. sp. lentis. Curr Biol 326(12):1163–1173CrossRefGoogle Scholar
  43. 43.
    Mishra RPN, Singh RK, Jaiswal HK, Kumar V, Maurya S (2006) Rhizobium-mediated induction of phenolics and plant growth promotion in rice (Oryza sativa L.). Curr Microbiol 52:383–389CrossRefGoogle Scholar
  44. 44.
    Khaosaad T, Garcia-Garrido JM, Steinkellner S, Vierheilig H (2007) Take-all disease is systematically reduced in roots of mycorhizal barley plants. Soil Biol Biochem 39:727–734CrossRefGoogle Scholar
  45. 45.
    Rabie GH (1998) Induction of fungal disease resistance in vicia faba by dual inoculation with Rhizobium leguminosarum and vesicular-arbuscular mycorrhizal fungi. Mycopathologia 141:3CrossRefGoogle Scholar
  46. 46.
    Tu JC (1979) Evidence of deferential tolerance among some root rot rhizobial parasitism in vitro. Physiol Plant Pathol 14:171–177CrossRefGoogle Scholar
  47. 47.
    Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande CR (1998) Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effects on radishes (Raphanus sativus L.). Plant Soil 204:57–67CrossRefGoogle Scholar
  48. 48.
    Malajczuk N, Pearce M, Lichfield RT (1984) Interaction between Phytopythora cinnamoni and Rhizobium isolates. Trans British Mycol Soc 82:491–500CrossRefGoogle Scholar
  49. 49.
    Buonassissi AJ, Copeman RJ, Pepin HS, Eaton GW (1986) Effect of Rhizobium spp. on Fusarium solani f.sp. phaseoli. Can J Plant Pathol 8:140–146CrossRefGoogle Scholar
  50. 50.
    Savoure A, Maygar Z, Perre M, Brown S, Schultze M, Dudits D, Kondorosi A, Kondorosi E (1994) Activation of the cell cycle machinery and the isoflavonoid biosynthesis by active Rhizobium melitoti Nod signal molecules in Midicago microcallus suspensions. EMBO J 13:1093–1102Google Scholar
  51. 51.
    Cordier C, Pozo MJ, Barea JM, Gianianazzi-Pearson V (1998) Cell defence response associated with localised and systemic resistance to Phytophthora parasitica induced in tomato by arbuscula mycorrhizal fungus. Mol Plant Microbe Interact 11:1017–1028CrossRefGoogle Scholar
  52. 52.
    Brimner TA, Boland GJ (2003) A review of the non-target effects of fungi used to biologically control plant diseases. Agric Ecosyst Environ 100:3–16CrossRefGoogle Scholar
  53. 53.
    Phillips DA, Kapulnik Y (1995) Plant isoflavonoids, pathogens and symbionts. Trends Microbiol 3:58–64CrossRefGoogle Scholar
  54. 54.
    Eheshamul-Haque S, Ghaffar A (1993) Use of rhizobia in the control of root rot disease of sunflower, okra, soyabean and mungbean. J Phytopathol 138:157–163CrossRefGoogle Scholar
  55. 55.
    Arfaoui A, Sifi B, Boudabaous A, Hadrami IE, Cherif M (2006) Identification of Rhizobium isolates possessing antagonistic activity against Fusarium oxysporium f.sp. ciceris, the causal agent of Fusarium wilt of chickpea. J Plant Pathol 88:67–75Google Scholar
  56. 56.
    Ruan Y, Kotraiah V, Straney DC (1995) Flavonoids stimulate spore germination in Fusarium solani pathogenic on legumes in a manner sensitive to inhibitors of cAMP-dependent protein kinase. Mol Plant Microbe Interact 8:929–938CrossRefGoogle Scholar
  57. 57.
    Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:1290–1306CrossRefGoogle Scholar
  58. 58.
    Tu JC (1978) Protection from severe phytophthora root rot by Rhizobium. Physiol Plant Pathol 12:233–240CrossRefGoogle Scholar
  59. 59.
    Husain S, Ghaffar A, Aslam M (1990) Biological control of Macrophomina phaseolina charcoal rot sunflower and mungbean. J Phytopathol 130:157–160CrossRefGoogle Scholar
  60. 60.
    Chao WL (1990) Antagonistic activity of Rhizobium spp. against beneficial and plant pathogenic fungi. Lett Appl Microbiol 10:213–215CrossRefGoogle Scholar
  61. 61.
    Huang HC, Kodama F, Akashi K, Konno K (2002) Impact of crop rotation on soilborne diseases of kidney bean: A case study in northern Japan. Plant pathol Bull 11:87–96Google Scholar
  62. 62.
    Matiru VN, Dakora FD (2004) Potential use of rhizobial bacteria as plant growth for increased yield in landraces of African cereal crops. Afr J Biotechnol 3(1):1–7Google Scholar
  63. 63.
    Curir P, Marchesini A, Danielit B, Mariani F (1996) 3-Hydroxyacetophenone in Carnations is a Phytoanticipin active against Fusarium oxysporum f. sp. Dianthi. Phytocheraistr 41(2):447–450CrossRefGoogle Scholar
  64. 64.
    Dakora FD, Vincent JM (1984) Fast-growing bacteria from nodules of cowpea (Vigna unguiculata (L.) Walp.). J Appl Bacteriol 56:327–330CrossRefGoogle Scholar
  65. 65.
    van Rensburg J, Strijdom H, Kriel MM (1976) Necessity for seed inoculation of soybeans in South Africa. Phytophylactica 8:91–96Google Scholar
  66. 66.
    Ververidis F, Trantas E, Douglas C, Vollmer G, Kretzschmar G, Panopoulos N (2007) Biotechnology of flavonoids and other phenylpropanoid-derived natural products. Part II: Reconstruction of multienzyme pathways in plants and microbes. Biotechnol J 2:1235–1249CrossRefGoogle Scholar
  67. 67.
    Dixon RA, Paiva NL (1995) Stress-Induced Phenylpropanoid Metabolism. Plant Cell 7(7):1085–1097Google Scholar
  68. 68.
    Vogt T, Pollak P, Tarlyn N, Taylor LP (1994) Pollination-or Wound-lnduced Kaempferol Accumulation in Petunia Stigmas Enhances Seed Production. The Plant Cell 6:11–23Google Scholar
  69. 69.
    Sprent JI (2008) 60 Ma of legume nodulation. What’s new? What’s changing? J Exp Bot 59(5):1081–1084CrossRefGoogle Scholar
  70. 70.
    Dakora FD, Keya SO (1997) Contribution of legume nitrogen fixation to sustainable agriculture in sub-Saharan Africa. Soil and Biochem 29:809–817CrossRefGoogle Scholar
  71. 71.
    Dakora FD, Phillips DA (1996) Diverse functions of isoflavonoids in legumes transcend anti-microbial definitions of phytoalexins. Physiol Mol Plant Pathol 49:1–20CrossRefGoogle Scholar
  72. 72.
    Dakora FD (2000) Commonality of root nodulation signals and nitrogen assimilation in tropical grain legumes belonging to the tribe Phaseoleae. Aust J Plant Physiol 27:885–892Google Scholar
  73. 73.
    Hungria M, Joseph CM, Phillips DA (1991) Rhizobium nod-gene inducers exuded naturally from roots of common bean (Phaseolus vulgaris L.). Plant Physiol 97:759–764CrossRefGoogle Scholar
  74. 74.
    Dakora FD and Muofhe ML (1996) Molecular signals involved in nodulation of the African Bambara groundnut. In: Proceedings of the International Bambara Groundnut Symposium, University of Nottingham, UK pp 171–179Google Scholar
  75. 75.
    Messens E, Geelen D, van Montagu M, Holsters M (1991) 7,4-Dihydroxyflavanone is the major Azorhizobium nod-gene-inducing factor present in Sesbania rostrata seedling exudate. Mol Plant-Microbe Interact 4:262–267CrossRefGoogle Scholar
  76. 76.
    Haby VA, Stout SA, Hons FM, Leonard AT (2006) Nitrogen fixation and transfer in a mixed stand of alfalfa and Bermuda grass. Agron J 98:890CrossRefGoogle Scholar
  77. 77.
    Unkovich MJ, Pate JS (2000) An appraisal of recent field measurements of symbiotic N2 fixation by annual legumes. Field Crops Res 65:211–228CrossRefGoogle Scholar
  78. 78.
    Maskey SL, Bhattarai S, Peoples MB, Herridge DF (2001) On-farm measurements of nitrogen fixation by winter and summer legumes in the Hill and Terai regions of Nepal. Field Crops Res 70:209–221CrossRefGoogle Scholar
  79. 79.
    Azpilicueta CE, Zawoznik MS, Tomaro ML (2004) Phytoalexins synthesis is enhanced in groundnut plants inoculated with Bradyrhizobium sp.( Arachis). Crop Prot 23:1069–1074CrossRefGoogle Scholar
  80. 80.
    De Rijke E. Aardenburg L, Van Dijk J, Ariese F, Ernst WHO, Gooijer C, Brinkman UA (2005). Changed isoflavone levels in red clover (Trifolium pratense L) leaves with disturbed root nodulation in response to water logging. J Chem Ecol 31(6):1285–1298Google Scholar
  81. 81.
    Russell GB, Sutherland ORW, Huchins RFN, Christmas RE (1978) Vestitol: A phytoalexin with insect feeding-deterrent activity. J Chem Ecol 4:571–579CrossRefGoogle Scholar
  82. 82.
    Rich JR, Keen NT, Thomason IJ (1977) Association of coumestans with the hypersensitivity of Lima bean roots to Pratylenchus scribneri. Physiol Plant Pathol 10:105–116CrossRefGoogle Scholar
  83. 83.
    Fukami H, Nakajima M (1971) Rotenone and the rotenoids. In: Jacobson M, Crosby DG (eds) Naturally Occurring Insecticides. Dekker, New York, pp 71–97Google Scholar

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© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Crop Sciences, Faculty of ScienceTshwane University of TechnologyPretoriaSouth Africa
  2. 2.Chemistry Department, Faculty of ScienceTshwane University of TechnologyPretoriaSouth Africa

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