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Molecular Biology of Stem Nodulation

  • R. P. Legocki
  • A. A. Szalay
Part of the Plant Gene Research book series (GENE)

Abstract

Due to the agricultural importance of legumes and their symbiosis with nitrogen-fixing rhizobia, the term “Rhizobium-legume symbiosis” has become almost synonymous with the term “root nodule symbiosis”. Recent studies, however, have shown that nodulation and symbiotic nitrogen fixation also occur on the stem of some legumes, including Aeschynomene and Sesbania. Upon association with specific Rhizobium strains, generally referred to as “stem rhizobia”, the Aeschynomene and Sesbania plants can form nodules on either roots or stems, or both (Yatazawa and Yoshida, 1979; Dreyfus and Ommergues, 1981; Eaglesham and Szalay, 1983). Unlike the formation of root nodules, stem nodulation in Aeschynomene is not significantly inhibited at increased concentrations of applied nitrogen, whereas the efficiency of nitrogen fixation in stem nodules is comparable to that of soybean root nodules (Legocki et al., 1983 a). These observations, along with the fact that repeated inoculations of Aeschynomene plants with stem Rhizobium result in an increased number of nodules (up to 450 per plant, Legocki et al., 1983 a), have recently led to an intensive research of the stem nodule symbiosis.

Keywords

Nitrogen Fixation Root Nodule Rhizobium Strain Symbiotic Nitrogen Fixation Infection Thread 
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.

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References

  1. Allen, E. K., Allen, O. N., 1950: Biochemical and symbiotic properties of the rhizobia. Bacteriol. Rev. 14, 273–330.PubMedGoogle Scholar
  2. Allen, O. N., Allen, E. K., 1981: In: The Leguminosae, A Source Book of Characteristics, Uses, and Nodulation. Madison: The University of Wisconsin Press, 812 pp.Google Scholar
  3. Appleby, C. A., Nicola, N. A., Hurrell, J. G. R., Leach, S. J., 1975: Characterization and improved separation of soybean leghemoglobins. Biochemistry 14, 4444–4450.PubMedCrossRefGoogle Scholar
  4. Baulcombe, D., Verma, D. P. S., 1978: Preparation of a complementary DNA for leghemoglobin and direct demonstration that leghemoglobin is encoded by the soybean genome. Nucl. Acids Res. 5, 4141–4153.PubMedCrossRefGoogle Scholar
  5. Bogusz, D., Delajudie, P., Dreyfus, B., 1983: Transposons, plasmids and bacteriophages as tools in genetic analysis of Rhizobium from Sesbania rostrata. In: Proceedings of the First Internat. Symp. Molec. Genetics of the Bacteria-Plant Interaction, Pühler, A. (ed.). Berlin - Heidelberg - New York - Tokyo: Springer (in press).Google Scholar
  6. Burns, R. C., Hardy, R. W. F., 1975: Description and classification of diazotrophs. In: Nitrogen Fixation in Bacteria and Higher Plants, Kleinzeller, A., Whitmann, H. G. (eds.), 14–38, Berlin — Heidelberg – New York: Springer.CrossRefGoogle Scholar
  7. Davis, B. J., 1964: Disc electrophoresis, method and application to human serum proteins. Annals New York Acad. Sci. 121, 404–427.CrossRefGoogle Scholar
  8. Dreyfus, B. L., Dommergues, Y. R., 1981: Stem nodules on the tropical legume Sesbania rostrata. In: Current Perspectives in Nitrogen Fixation, Gibson, A. H., Newton, W. E. (eds.), p. 471, Canberra: Australian Academy of Sciences.Google Scholar
  9. Dreyfus, B. L., Elmerich, C., Dommergues, Y. R., 1983: Free-living Rhizobium strain able to grow on N2 as the sole nitrogen source. Appl. Environmental Microbiol. 45, 711–713.Google Scholar
  10. Eaglesham, A. R. J., Szalay, A. A., 1983: Aerial stem nodules on Aeschynomene spp. Plant Sci. Lett. 29, 265–272.Google Scholar
  11. Eckhardt, T., 1978: A rapid method for the identification of plasmid deoxyribonucleic acid in bacteria. Plasmid 1, 584–588.PubMedCrossRefGoogle Scholar
  12. Ellfolk, N., 1972: Leghaemoglobin, a plant haemoglobin. Endeavour 31, 139–142.Google Scholar
  13. Elmerich, C., Dreyfus, B. L., Reysset, G., Aubert, J.-P., 1982: Genetic analysis of nitrogen fixation in a tropical fast-growing Rhizobium. EMBO J. 1, 449–503.Google Scholar
  14. Elmerich, C., Dreyfus, B., Aubert, J.-P., 1983: Submitted (FEMS).Google Scholar
  15. Fuchsman, W. H., Appleby, C. A., 1979: Separation and determination of the relative concentrations of the homogeneous components of soybean leghemoglobin by isoelectric focusing. Biochim. Biophys. Acta 579, 314–324.PubMedGoogle Scholar
  16. Graham, P. H., Parker, C. A., 1964: Diagnostic features in the characterization of the root-nodule bacteria of legumes. Plant and Soil 20, 383–396.CrossRefGoogle Scholar
  17. Hagerup, O., 1982: En hygrofil baelgplante (Aeschynomene aspera L.) med bakterieknolde paa staengelen. Dan. Bot. Ark. 15, 1–9.Google Scholar
  18. Johnson, M. D., Allen, O. N., 1952: Cultural reactions of rhizobia with special reference to strains isolated from Sesbania species. Antonie van Leeuwenhoek J. Microbiol. Serol. 18, 1–12.Google Scholar
  19. Jordan, D. C., Allen, O. N., 1974: Rhizobiaceae. In: Bergey’s Manual of Determinative Bacteriology, Buchanan, R. E., Gibbons, N. E. (eds.), 261–267, Baltimore: The Williams and Wilkins Co.Google Scholar
  20. Kado, C. I., Liu, S. T., 1981: Rapid procedure for determination and isolation of large and small plasmids. J. Bacteriol. 145, 1365–1373.PubMedGoogle Scholar
  21. Keister, D. L., 1975: Acetylene reduction by pure cultures of rhizobia. J. Bacteriol. 123, 1265–1268.PubMedGoogle Scholar
  22. Kingsbury, J. M., 1964: In: Poisonous Plants of the United States and Canada. Englewood Cliffs, N. J.: Prentice-Hall. 626 pp.Google Scholar
  23. Kiss, G. B., Dobo, K., Dusha, I., Breznovits, A., Orosz, L., Vincze E., Kondorosi, A., 1980: Isolation and characterization of an R-prime plasmid from Rhizobium meliloti. J. Bacteriol. 141, 121–128.PubMedGoogle Scholar
  24. Kurz, W. G. W., LaRue, T. A., 1975: Nitrogenase activity in rhizobia in absence of plant host. Nature (London) 256, 407–408.CrossRefGoogle Scholar
  25. Laemmli, U. K., 1970: Cleavage of structural proteins during the assembly of the head of bacteriophasity. Nature New Biol. 227, 680–685.CrossRefGoogle Scholar
  26. Legocki, R. P., Verma, D. P. S., 1979: A nodule-specific plant protein (nodulin-35) from soybean. Science 205, 190–193.PubMedCrossRefGoogle Scholar
  27. Legocki, R. P., Verma, D. P. S., 1980: Identification of “nodule-specific” host proteins (nodulins) involved in the development of Rhizobium-legume symbiosis. Cell 20, 153–163.PubMedCrossRefGoogle Scholar
  28. Legocki, R. P., Eaglesham, A. R. J., Szalay, A. A., 1983 a: Stem nodulation in Aeschynomene: a model system for bacterium-plant interactions. In: Proceedings of the First Internat. Symp. Molec. Genetics of the Bacteria-Plant Interaction, Pühler, A. (ed.), 210–219, Berlin — Heidelberg — New York — Tokyo: Springer.CrossRefGoogle Scholar
  29. Legocki, R. P., Yun, A., Szalay, A. A., 1984: Manuscript in preparation.Google Scholar
  30. Legocki, R. P., Szalay, A. A., 1984: Expression of Beta-galactosidase controlled by a nitrogenase promotor in stem nodules of Aeschynomene scabra. Manuscript submitted (PNAS).Google Scholar
  31. Marsh, C. D., Clawson, A. B., 1920: Daubentonia longifolia (coffee bean), a poisonous plant. J. Agric. Res. 20, 507–513.Google Scholar
  32. Martinez-De Drets, G., Arias, A., 1972: Enzymatic basis for differentiation of Rhizobium into fast-and slow-growing groups. J. Bacteriol. 109, 467–470.Google Scholar
  33. McComb, J. A., Elliott, J., Dilworth, M. J., 1975: Acetylene reduction by Rhizobium in pure culture. Nature (London) 256, 409–410.CrossRefGoogle Scholar
  34. Muenscher, W. C., 1939: In: Poisonous Plants of the United States. Rural Science Series. New York: Macmillan, 266 pp.Google Scholar
  35. O’Farrell, P. H., 1975: High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250, 4007–4021.Google Scholar
  36. Quinto, C., de la Vega, H., Flores, M., Fernandez, L., Ballado, T., Soberon, G., Palacios, R., 1982: Reiteration of nitrogen fixation gene sequences in Rhizobium phaseoli. Nature 299, 724–726.Google Scholar
  37. Rosenberg, M., Court, D., 1979: Regulatory sequences involved in the promotion and termination of RNA transcription. Ann. Rev. Genet. 13, 319–353.PubMedCrossRefGoogle Scholar
  38. Ruvkun, G. B., Ausubel, F. M., 1980: Interspecies homology of nitrogenase genes. Proc. Natl. Acad. Sci. U. S. A. 77, 191–195.PubMedCrossRefGoogle Scholar
  39. Ruvkun, G. B., Ausubel, F. M., 1981: A general method for site-directed mutagenesis in procaryotes. Nature 289, 85–88.PubMedCrossRefGoogle Scholar
  40. Ruvkun, G. B., Sundaresan, V., Ausubel, F. M., 1982: Directed transposon Tn 5 mutagenesis and complementation analysis of Rhizobium meliloti symbiotic nitrogen fixation genes. Cell 28, 551–559.CrossRefGoogle Scholar
  41. Schaede, R., 1940: Die Knöllchen der adventiven Wasserwurzeln von Neptunia oleracea und ihre Bakteriensymbiose. Planta 31, 1–21.CrossRefGoogle Scholar
  42. Stowers, M. D., Eaglesham, A. R. J., 1983: A stem-nodulating Rhizobium with physiological characteristics of both fast and slow growers. J. Gen. Microbiol. (in press).Google Scholar
  43. Sullivan, D., Brisson, N., Goodchild, B., Verma, D. P. S., Thomas, D. Y., 1981: Molecular cloning and organization of two leghaemoglobin genomic sequences of soybean. Nature 289, 516–518.CrossRefGoogle Scholar
  44. Teale, F. W. J., 1959: Cleavage of the haem-protein link by acid methylethylketone. Biochim. Biophys. Acta 35, 543.PubMedCrossRefGoogle Scholar
  45. Tsien, H. C., Dreyfus, B. L., Schmidt, E. L., 1983: Morphogenesis of stem nodules of Sesbania rostrata. In: Abstracts of the 9th North American Rhizobium Conference, Ithaca, N. Y., P6.Google Scholar
  46. Verboom, W. C., 1966: The grassland communities of Barotseland. Trop. Agric. (Trinidad) 43, 107–115.Google Scholar
  47. Vincent, J. M., 1977: Rhizobium: a general microbiology. In: A Treatise on Dinitrogen Fixation, Sect. III: Biology, Hardy, R. W. F., Silver, W. S. (eds.), 277–366, New York: Wiley.Google Scholar
  48. Whittaker, R. G., Lennox, S., Appleby, C. A., 1981: Relationship of the minor soybean leghemoglobins d1, d2, d3 to the major leghemoglobins c1, c2 and c3. Biochem. Int. 3, 117–124.Google Scholar
  49. Yatazawa, M., Yoshida, S., 1979: Stem nodules in Aeschynomene indica and their capacity of nitrogen fixation. Physiol. Plant. 45, 293–295.CrossRefGoogle Scholar
  50. Zurkowski, W., Lorkiewicz, Z., 1978: Effective method for the isolation of non-nodulating mutants of Rhizobium trifoiii. Genet. Res. (Camb.) 32, 311–314.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag/Wien 1984

Authors and Affiliations

  • R. P. Legocki
    • 1
  • A. A. Szalay
    • 1
  1. 1.Boyce Thompson Institute for Plant ResearchCornell UniversityIthacaUSA

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