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Competitiveness and communication for effective inoculation byRhizobium, Bradyrhizobium and vesicular-arbuscular mycorrhiza fungi

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  • Symbiotic Interactions Between Microorganisms and Plants
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Abstract

After a short summary on the ecology and rhizosphere biology of symbiotic bacteria and vesicular-arbuscular (VA) mycorrhiza fungi and their application as microbial inocula, results on competitiveness and communication are summarized. Stress factors such as high temperature, low soil pH, aluminium concentrations and phytoalexins produced by the host plants were studied withRhizobium leguminosarum bv.phaseoli andRhizobium tropici onPhaseolus beans. Quantitative data for competitiveness were obtained by usinggus + (glucoronidase) labelled strains, which produce blue-coloured nodules. ForPhaseolus-nodulating rhizobia, a group specific DNA probe was also developed, which did not hybridize with more than 20 other common soil and rhizosphere bacteria. Results from several laboratories contributing to knowledge of signal exchange and communication in theRhizobium/Bradyrhizobium legume system are summarized in a new scheme, including also defense reactions at the early stages of legume nodule initiation. Stimulating effects of flavonoids on germination and growth of VA mycorrhiza fungi were also found. A constitutive antifungal compound in pea roots, β-isoxazolinonyl-alanine, was characterized.

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References

  1. Barnet, Y. M., Ecology of legume root-nodule bacteria, in: Studies in Plant Science, vol. 1, Biology and Biochemistry of Nitrogen Fixation pp. 199–228. Eds M. J. Dilworth and A. R. Glenn. Elsevier Sci. Publ. Amsterdam-New York 1991.

    Google Scholar 

  2. Bjourson, A. J., Stone, C. E., and Cooper, J. E., Combined subtraction hybridization and polymerase chain reaction amplification procedure for isolation of strain-specificRhizobium DNA sequences. Appl. envir. Microbiol.58 (1992) 2296–2301.

    Article  CAS  Google Scholar 

  3. Bottomley, P.J., Ecology ofBradyrhizobium andRhizobium, in: Biological Nitrogen Fixation, pp. 293–348. Eds G. Stacey, R. H. Burris and H. J. Evans. Chapman & Hall, New York-London 1992.

    Google Scholar 

  4. Bowen, G. D., Microbial dynamics in the rhizosphere: Possible strategies in managing rhizosphere populations, in: The Rhizosphere and Plant Growth, pp. 25–32. Eds D. L. Keister and P. B. Cregan. Kluwer Acad. Publ., Dordrecht 1991.

    Chapter  Google Scholar 

  5. Dakora, F. D., Joseph, C. M., and Phillips, D. A., Alfalfa (Medicago sativa L.) root exudates contain isoflavonoids in the presence ofRhizobium meliloti. Pl. Physiol.101 (1993) 819–824.

    Article  CAS  Google Scholar 

  6. Denarié, J., Debelle, F., Truchet, G., and Promé, J.-C.,Rhizobium and legume nodulation: A molecular dialogue, in: New Horizons in Nitrogen Fixation, pp. 19–30. Eds R. Palacios, J. Mora and W. E. Newton. Kluwer Acad. Publ. Dordrecht 1993.

    Chapter  Google Scholar 

  7. Elliott, L. F., and Lynch, J. M., Potential uses for inocula in soils. OECD-Workshop, Maui, USA 1993.

  8. Görge, E., and Werner, D., Degradation of wyerone, the phytoalexin of faba beans byRhizobium leguminosarum. Curr. Microbiol.23 (1991) 153–157.

    Article  Google Scholar 

  9. Göttfert, M., Holzhäuser, D., Bäni, D., and Hennecke, H., Structural and functional analysis of two different nodD genes inBradyrhizobium japonicum USDA 110. Molec. Pl.-Microbe Interactions3 (1992) 257–265.

    Article  Google Scholar 

  10. Gresshoff, P. M., Plant function in nodulation and nitrogen fixation in legumes, in: New Horizons in Nitrogen Fixation, pp. 31–42. Eds R. Palacios, J. Mora and W. E. Newton. Kluwer Acad. Publ., Dordrecht 1993.

    Chapter  Google Scholar 

  11. Hilali, A., Aurag, J. Molina, J. A. E., and Schmidt, E. L., Competitiveness and persistence of strains ofRhizobium phaseoli introduced into Moroccan sandy soil. Biol. Fertil. Soils7 (1989) 213–218.

    Article  Google Scholar 

  12. Hirsch, A. M., Transley review no. 40. Developmental biology of legume nodulation. New Phytol.122 (1992) 211–237.

    Article  PubMed  Google Scholar 

  13. Hubac, C., Ferran, J., Guerrier, D., Trémolières, A., and Kondorosi, A., Luteolin absorption inRhizobium meliloti wild-type and mutant strains. J. gen. Microbiol.139 (1993) 1571–1578.

    Article  CAS  Google Scholar 

  14. Kannenberg, E. L., Rathbun, E. A., and Brewin, N. J., Molecular dissection of structure and function in the lipopolysaccharide ofRhizobium leguminosarum strain 3841 using monoclonal antibodies and genetic analysis. Molec. Microbiol.6 (1992) 2477–2487.

    Article  CAS  Google Scholar 

  15. Kape, R., Parniske, M., and Werner, D., Chemotaxis and nod gene activity ofBradyrhizobium japonicum in response to hydroxycinnamic acids and isoflavonoids. Appl. envir. Microbiol.57 (1991) 316–319.

    Article  CAS  Google Scholar 

  16. Kape, R., Parniske, M., Brandt, S., and Werner, D., Isoliquiritigenin, a strongnod gene- and glyceollin resistance-inducing flavonoid from soybean root exudate. Appl. envir. Microbiol.58 (1992) 1705–1710.

    Article  CAS  Google Scholar 

  17. Kape, R., Wex, K., Parniske, M., Görge, E., Wetzel, A., and Werner, D., Legume root metabolites and VA-mycorrhiza development. J. Pl. Physiol.141 (1992) 54–60.

    Article  Google Scholar 

  18. Kluepfel, D. A., The behavior and tracking of bacteria in the rhizosphere. A. Rev. Phytopath.31 (1993) 441–472.

    Article  Google Scholar 

  19. Martinez-Romero, E., Segovia, L., Mercante, F. M., Franco, A. A., Graham, P., and Pardo, M. A.,Rhizobium tropici, a novel species nodulatingPhaseolus vulgaris L. beans andLeucaena sp. trees. Int. J. syst. Bact.41 (1991) 417–426.

    Article  CAS  Google Scholar 

  20. Miller, K. J., Hadley, J. A., and Gustine, D. L., Cyclic β-1,6-1,3-glucans ofBradyrhizobium japonicum USDA 110 elicit isoflavonoid production in the soybean (Glycine max) host. Pl. Physiol.104 (1994) 917–923.

    Article  CAS  Google Scholar 

  21. Morandi, D., Phytoalexins, isoflavonoids, and flavonoids in the plant-VAM fungus interaction, in: The Role of VA-mycorrhizae in Transformation of Matter in the Soil and their Importance for Plant Nutrition and Plant Health. Abstracts of the First Conference of Cost Action 8.10, Einsiedeln 1990.

  22. Morandi, D., Bailey, J.A., and Gianinazzi-Pearson, V., Isoflavonoid accumulation in soybean roots infected with vesicular-arbuscular mycorrhizal fungi. Physiol. Pl. Path.24 (1984) 357–364.

    Article  CAS  Google Scholar 

  23. Olivares, J., Amarger, N., Brom, S., Broughton, B., Martinez, E., Paau, A., Sadowsky, M., Simarov, B., Tikhonovich, I., Triplett E., and Werner, D., Competitiveness ofRhizobium strains for nodule occupancy, in: New Horizons in Nitrogen Fixation, pp. 773–775. Eds R. Palacios, J. Mora and W. E. Newton. Kluwer Acad. Publ., Dordrecht 1993.

    Chapter  Google Scholar 

  24. Parniske, M., Ahlborn, B., and Werner, D., Isoflavonoid-inducible resistance to the phytoalexin glyceollin in soybean rhizobia. J. Bact.173 (1991) 3432–3439.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Parniske, M., Kosch, K., Werner, D., and Müller, P., Exoß mutants ofBradyrhizobium japonicum with reduced competitiveness for nodulation ofGlycine max. MPMI6 (1992) 99–106.

    Article  Google Scholar 

  26. Peters, N. K., Forst, J. W., and Long, S. R., A plant flavone, luteolin, induces expression ofRhizobium meliloti nodulation genes. Science233 (1986) 977–980.

    Article  CAS  PubMed  Google Scholar 

  27. Phillips, D. A., Flavonoids: Plant signals to soil microbes, in: Recent Advances in Phytochemistry 26, Phenolic Metabolism in Plants, pp. 201–231. Eds H. A. Stafford and R. K. Ibrahim. Plenum Press, New York 1992.

    Chapter  Google Scholar 

  28. Pühler, A., Arnold, W., Buendia-Claveria, A., Kapp, D., Keller, M., Niehaus, K., Quandt, J., Roxlau, A., and Weng, W. M., The role of theRhizobium meliloti exopolysaccharides EPSI and EPSII in the infection process of alfalfa nodules, in: Advances in Molecular Genetics of Plant-Microbe Interactions vol. 1, pp. 189–194. Eds H. Hennecke and D. P. S. Verma. Kluwer Acad. Publ., Dordrecht 1991.

    Chapter  Google Scholar 

  29. Rao, J. R., Sharma, N. D., Hamilton, J. T. G., Boyd, D. R., and Cooper, J. E., Biotransformation of the pentahydroxy flavone quercetin byRhizobium loti andBradyrhizobium strains (Lotus). Appl. envir. Microbiol.57 (1991) 1563–1565.

    Article  CAS  Google Scholar 

  30. Recourt, K., Tunen, A. J. van, Mur, L. A., Brussel, A. A. N. van, Lugtenberg, B. J. J., and Kijne, J. W., Activation of flavonoid biosynthesis in roots ofVicia sativa subsp.nigra plants by inoculation withRhizobium leguminosarum biovarviciae. Pl. molec. Biol.19 (1992) 411–420.

    Article  CAS  Google Scholar 

  31. Rovira, A. D., Elliott, L. F., and Cook, R. J., The impact of cropping systems on rhizosphere organisms affecting plant health, in: The Rhizosphere, pp. 389–436. Ed. J. M. Lynch. J. Wiley & Sons, Chichester-New York 1991.

    Google Scholar 

  32. Savoure, A., Magyar, Z., Pierre, M., Brown, S., Schultze, M., Dudits, D., Kondorosi, A., and Kondorosi, E., Activation of the cell cycle machinery and the isoflavonoid biosynthesis pathway by activeRhizobium meliloti Nod signal molecules inMedicago microcallus suspensions. EMBO J.13 (1994) 1093–1102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Schenk, S. U., Lambein, F., and Werner, D., Broad antifungal activity of β-isoxazolinonyl-alanine, a non-protein amino acid from roots of pea (Pisum sativum L.) seedlings. Biol. Fertil. Soils11 (1991) 203–209.

    Article  CAS  Google Scholar 

  34. Schenk, S. U., and Werner, D., β-(3-Isoxazolin-5-on-2-yl)-alanine fromPisum: Allelopathic properties and antimycotic bioassay. Phytochemistry30 (1991) 467–470.

    Article  CAS  Google Scholar 

  35. Schmidt, P. E., Parniske, M., and Werner, D., Production of the phytoalexin glyceollin I by soybean roots in response to symbiotic and pathogenic infection. Bot. Acta105 (1992) 18–25.

    Article  CAS  Google Scholar 

  36. Schmidt, P. E., Broughton, W. J., and Werner, D., Nod factors ofBradyrhizobium japonicum andRhizobium sp. NGR234 induce flavonoid accumulation in soybean root exudate. MPMI7 (1994) 384–390.

    Article  CAS  Google Scholar 

  37. Somasegaran, P., and Bohlool, B. B., Single-strain versus multistrain inoculation: Effect of soil mineral N available on rhizobial strain effectiveness and competition for nodulation on chick-pea, soybean and dry bean. Appl. envir. Microbiol.56 (1990) 3298–3303.

    Article  CAS  Google Scholar 

  38. Spaink, H. P., Rhizobial lipo-oligosaccharides: Answers and questions. Pl. molec. Biol.20 (1992) 977–986.

    Article  CAS  Google Scholar 

  39. Streit, W., Kosch, K. and Werner, D., Nodulation competitiveness ofRhizobium leguminosarum bv.phaseoli andRhizobium tropici strains measured by glucuronidase (gus) gene fusion. Biol. Fertil. Soils14 (1992) 140–144.

    Article  CAS  Google Scholar 

  40. Streit, W., Bjourson, A. J., Cooper, J. E., and Werner, D., Application of subtraction hybridization for the development of aRhizobium leguminosarum biovarphaseoli andRhizobium tropici group-specific DNA probe. FEMS Microbiol. Ecol.13 (1993) 59–68.

    Article  CAS  Google Scholar 

  41. Thies, J., Singleton, P. W., and Bohlool, B. B., Influence of size of indigenous rhizobial populations on establishment and symbiotic performance of introduced rhizobia on field-grown legumes. Appl. envir. Microbiol.57 (1991) 19–28.

    Article  CAS  Google Scholar 

  42. Vargas, A. A. T., and Graham, P. A., Cultivar and pH effect on competition for nodule sites between isolates ofRhizobium in beans. Pl. Soil117 (1989) 195–200.

    Article  Google Scholar 

  43. Werner, D., Symbiosis of Plants and Microbes. Chapman & Hall, London-New York 1992.

    Google Scholar 

  44. Werner, D., Ahlborn, B., Antoun, H., Bernard, S., Bolanos, C., Cooper, J. E., Görge, E., Jacobi, A., Kalliopi, P., Kape, R., Katinakis, P., Kosch, K., Müller, P., Parniske, M., Schmidt, P., Streit, W., and Wetzel, A., Communication and signal exchange in theRhizobium/Bradyrhizobium-legume system. Endocytobiosis Cell Res.10 (1993) 5–15.

    Google Scholar 

  45. Wolff, A. B., Streit, W., Kipe-Nolt, J. A., Vargas, H., and Werner, D., Competitiveness ofRhizobium leguminosarum bv.phaseoli strains in relation to environmental stress and plant defense mechanisms. Biol. Fertil. Soils12 (1991) 170–176.

    Article  Google Scholar 

  46. Wolff, A. B., Singleton, P. W., Sidirelli, M., and Bohlool, B. B., Influence of acid soil on nodulation and interstrain competitiveness in relation to tannin concentrations in seeds and roots ofPhaseolus vulgaris. Soil Biol. Biochem.25 (1993) 715–721.

    Article  Google Scholar 

  47. Zhang, X., Harper, R., Karsisto, M., and Lindström, K., Diversity ofRhizobium bacteria isolated from the root nodules of leguminous trees. int. J. syst. Bact.41 (1991) 104–113.

    Article  Google Scholar 

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Authors and Affiliations

  1. Fachbereich Biologie der Philipps-Universität, Karl-von-Frischstrasse, D-35032, Marburg, Germany

    D. Werner, S. Bernard, E. Görge, A. Jacobi, R. Kape, K. Kosch, P. Müller, M. Parniske, S. Schenk, P. Schmidt & W. Streit

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  1. D. Werner
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  2. S. Bernard
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  3. E. Görge
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  4. A. Jacobi
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  5. R. Kape
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  7. P. Müller
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  8. M. Parniske
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Werner, D., Bernard, S., Görge, E. et al. Competitiveness and communication for effective inoculation byRhizobium, Bradyrhizobium and vesicular-arbuscular mycorrhiza fungi. Experientia 50, 884–889 (1994). https://doi.org/10.1007/BF01923474

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