Legume-Rhizobium-Symbiosis: Host’s Point of View

  • D. P. S. Verma
  • K. Nadler
Part of the Plant Gene Research book series (GENE)


The legume-Rhizobium endosymbiosis may be the most highly evolved and perhaps ultimate association between a microbe and a plant in which the two partners can still grow independently. Undoubtedly the strong selective pressure on this association is the resulting nutritional complementation: the plant can be considerd a carbon-rich, nitrogen-deficient phototroph and the Rhizobium a carbon-deficient, nitrogen-fixing heterotroph. The resulting symbiosis which occurs in a specialized organ, the root nodule, makes the plant autotrophic with respect to the availability of reduced nitrogen, a limiting factor in plant nutrition. This unique intracellular association contributes significantly towards the yield of the agriculturally important legume crops.


Nitrogen Fixation Root Nodule Root Hair Glutamine Synthetase Uninfected Cell 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allen, O. N., Allen E. K., 1981: The Leguminosae. Madison, Wisconsin: Univ. of Wiscons in Press.Google Scholar
  2. Appleby, C. A., 1974: Leghemoglobin. In: The Biology of Nitrogen Fixation. Quispel, A. (Ed.), New York: Elsevier Pub. Co. Inc, pp. 521–554.Google Scholar
  3. Appleby, C. A., Turner, G. L., MacNichol, P. K., 1975a: Involvement of oxyleghaemoglobin and cytochromome P-450 in an efficient oxidative phosphorylation pathway which support nitrogen fixation in Rhizobium. Biochim. Biophys. Acta 387, 461–475.PubMedGoogle Scholar
  4. Appleby, C. A., Nicola, N. A., Hurrell, J. G. R., Leach, S. J., 1975b: Characterization and improved separation of soybean leghaemoglobin. Biochemistry 14, 4444–4450.PubMedGoogle Scholar
  5. Appleby, C. A., Tjepkema, J. D., Trinick, M. J., 1983: Hemoglobin in a nonleguminous plant, Parasponia. Possible genetic origin and function in nitrogen fixation. Science 220, 951–953.PubMedGoogle Scholar
  6. Atkins, C. A., Rainbird, R. M., Pate, J. S., 1980: Evidence for a purine pathway of ureide synthesis in N2-fixing nodules of cowpea (Vigna unguiculata L. Walp.). Z. Pflanzenphysiol. 97, 249–260.Google Scholar
  7. Atkins, C. A., 1981: Metabolism of purine-nucleotides to form ureides in nitrogen-fixing nodules of cowpea (Vigna unguiculata L. Walp). FEBS Letts. 125, 89–93. Auger, S., 1981: Ph. D. Thesis McGill University, Montreal, Canada.Google Scholar
  8. Auger, S., Verma D. P. S., 1981: Induction and expression of nodule-specific host genes in effective and ineffective root nodules of soybean. Biochemistry 20, 1300–1306.PubMedGoogle Scholar
  9. Avissar, V. J., Nadler, K. D., 1978: Stimulation of tetrapyrrole formation in Rhizobium japonicum by restricted aeration. J. Bact. 135, 782–789.PubMedGoogle Scholar
  10. Badnenoch-Jones, Summons, R. E., Djordjevic, M. A., Shine, J., Letham, D. S., Rolfe, B. J., 1982: Mass-spectrometeric quantification of indole-3-acetic acid in culture supernatants; studies in relation to root hair curling and nodule initiation. Appl. Environ. Microbiol. 44, 275–280.Google Scholar
  11. Bal, A. K., Shantharam, S., Verma, D. P. S., 1980: Changes in the outer cell wall of Rhizobium during development of the root nodule symbiosis in soybean. Can. J. Microbiol. 26, 1096–1103.PubMedGoogle Scholar
  12. Bassett, B., Goodman, R. N., Novacky, A., 1977a: Ultrastructure of soybean nodules. I. Release of Rhizobia from the infection thread. Can. J. Microbiol. 23, 573–582.Google Scholar
  13. Bassett, B., Goodman, R. N., Novacky, A., 1977b: Ultrastructure of soybean nodules. II: deterioration of symbiosis in ineffective nodules. Can. J. Microbiol. 23, 873–883.PubMedGoogle Scholar
  14. Bauer, W. D., 1981: Infection of legumes by rhizobia. Ann. Rev. Plant Physiol. 32, 407–449.Google Scholar
  15. Baulcombe, D., Key, J., 1980: Polyadenylated RNA sequences which are reduced in concentration following auxin treatment of soybean hypocotyls. J. Biol. Chem. 225, 8907–8913.Google Scholar
  16. Bergersen, F. J., Goodchild, D. J., 1973: Aeration pathways in soybean root nodules. Anst. J. Biol. Sci. 26, 729–740.Google Scholar
  17. Bergersen, F. J., Nutman, P. S., 1957: Symbiotic effectiveness in nodulated red clover. The influence of the host factor i, i. e. upon nodule structure and cytology. Heredity 11, 175–184.Google Scholar
  18. Bergersen, F. J., 1977: Physiological chemistry of dinitrogen fixation by legumes: In: A Treatise in Dinitrogen Fixation, Hardy, R. W. F., Silver, W. S. (eds.), New York: John Wiley, pp. 519–555Google Scholar
  19. Bergersen, F. J., 1965: Ammonia an early stable product of nitrogen fixation by soybean root nodules. Aust. J. Biol. Sci. 18, 1–9.Google Scholar
  20. Bergersen, F. J., 1974 ): Formation and function of bacteroids. In: The Biology of Nitrogen Fixation. Quispel, A. (ed.), Amsterdam: North-Holland, pp. 473–498.Google Scholar
  21. Bergmann H., Preddie, E., Verma, D. P. S., 1983: Nodulin ES: A subunit of specific uricase (uricase II) induced and localized in uninfected cells of nodules. The EMBO Jour. 2, 2333–2339.Google Scholar
  22. Beringer, J. E., Brewin, N., Johnston, A. W. B., Schulman, H. M., Hopwood, D. A., 1979: The Rhizobium-legume symbiosis. Proc. Roy. Soc. Lond. B 204, 219–223.Google Scholar
  23. Beringer, J. E., Brewin, N. J., Johnston, A. W. B., 1980: The genetic analysis of Rhi- zobium in relation to symbiotic nitrogen fixation. Heredity 45, 161–186.Google Scholar
  24. Bisseling, T., van den Bos, R. C., Weststrate, M. W., Hakkaart, M. J. J., van Kam-men, A., 1978: The effect of ammonium nitrate on the synthesis of nitrogenase and the concentration of leghemoglobin in pea root nodules induced by Rhizobium leguminosarum. Biochim. Biophys. Acta 539, 1–11.PubMedGoogle Scholar
  25. Bisseling, T., Been, C., Klugkist, J., van Kammen, A., Nadler, K., 1983: Nodule specific host proteins in effective and ineffective root nodules of Pisum sativum. The EMBO Jour. 2, 961–966.Google Scholar
  26. Boland, M. J., Hanks, J. F., Reynolds, P. H. S., Blevins, D. G., Tolbert, N. E., Schubert, K. R., 1982: Subcellular organization of ureide biogenesis from glycolytic intermediates and ammonium in nitrogen fixing soybean nodules. Planta 155, 45–51.Google Scholar
  27. Boland, M. J., Blevins, D. G., Randall, D. D., 1983: Soybean xanthine dehydrogenase: A kinetic study. Arch. Biochem. Biophys. 222, 2333–2339.Google Scholar
  28. Brill, W., 1980: Biochemical genetics of nitrogen fixation. Microbiol. Rev. 44, 449–467.PubMedGoogle Scholar
  29. Brisson, N., Verma D. P. S., 1982: Soybean leghemoglobin gene family: Normal, pseudo, and truncated genes. Proc. Nat. Acad. Sci. 79, 4055–4059.PubMedGoogle Scholar
  30. Burris, R. H., Orme-Johnson, W. H., 1974: Survey of nitrogenase and its EPR properties. In: Microbial Iron Metabolism. Neilands, J. B. (ed.), p. 597. New York: Academic Press.Google Scholar
  31. Caldwell, B. E., 1966: Inheritance of a strain-specific ineffective nodulation in soybeans. Crop. Sci 6, 427–428.Google Scholar
  32. Caldwell, B. E., Vest, H. G., 1977: Genetic aspects of nodulation and dinitrogen fixation by legumes: The macrosymbiont. In: A treatise on dinitrogen fixation. Sec. III, Hardy, R. W. F., Silver, W. S. (eds.) London: Wiley-Interscience, p. 557–575.Google Scholar
  33. Callaham, D., Torrey; J. G., 1977: Prenodule formation and primary nodule devel- opment in roots of Comptonia (Myricaceae). Can. J. Bot. 55, 2303–2318.Google Scholar
  34. Callaham, D., 1979: M. Sc. thesis. University of Massachusetts, Amherst.Google Scholar
  35. Callaham, D., Newcomb, W., Torrey, J. G., Peterson, R. L., 1979: Root hair infection in actinomycete-induced root nodule initiation in Casuarina, Myrica, and Comptonia. Botanical Gazette. 140 (Suppl.): Sl-S9.Google Scholar
  36. Callaham, D. A., Torrey, J. G., 1981: The structural basis for infection of root hairs of Trifolium repens by Rhizobium. Can. J. Bot. 59, 1647–1664Google Scholar
  37. Chakarvorty, A. K., Zurkowski W., Shine J., Rolfe, B. G., 1983: Symbiotic nitrogen fixation: molecular cloning of Rhizobium genes involved in exopolysaccharide synthesis and effective nodulation. J. Mol. Appl. Gen. 1, 585–596.Google Scholar
  38. Christeller, J. T., Laing, W. A., Sutton, W. D., 1977: Carbon dioxide fixation by lupine root nodules. 1. Characterization, association with phosphoenolpyruvate carboxylase, and correlation with nitrogen fixation during nodule development. Plant Physiol. 60, 47–50.PubMedGoogle Scholar
  39. Cullimore, J. V., Lara, M., Lea, P. J., Miflin, B. J., 1983: Purification and properties of the two forms of glutamine synthetase from the plant fraction of Phaseolus root nodules. Planta 157, 245–253.Google Scholar
  40. Cutting, J. A., Schulman, H. M., 1969: The site of heme synthesis in soybean root nodules. Biochim Biophys. Acta. 192, 486–493.Google Scholar
  41. Dart, P. J., 1974: The infection process. In: The Biology of Nitrogen Fixation. Quispel, A. (ed.), Amsterdam: Elsevier-North-Holland, pp. 381–429.Google Scholar
  42. Dart, P. J., 1977: Infection and development of leguminous nodules. In: A treatise on dinitrogen fixation. Section III, biology, Hardy, R. W. F., Silver, W. S. (eds.), New York: John Wiley, pp. 367–472.Google Scholar
  43. Degenhardt, T. L., LaRue, T. A., Paul, E. A., 1976: Investigation of a non-nodulating cultivar of Pisum sativum. Can. J. Bot. 54, 1633–1636.Google Scholar
  44. Dénarié, J., Truchet, G., Bergeron, B., 1976: Effects of some mutations on symbiotic properties of Rhizobium. In: Symbiotic Nitrogen Fixation in Plants. Nut-man, P. S. (ed.), New York/London: Cambridge Univ. Press, pp. 47–61.Google Scholar
  45. Dilworth, M. J., 1980: Leghemoglobin. In: Methods in Enzymology, Vol. 69 c. San Pietro, A. (ed.), New York: Academic Press, pp. 812–823.Google Scholar
  46. Dilworth, M. J., 1980: Symbiotic Associations and Cyanobacteria. In: Nitrogen Fixation II. Newton, W. E., Orme-Johnson, W. H. (eds.), Baltimore: University Park Press, p. 325.Google Scholar
  47. Dullaart, J., 1967: Quantitative estimation of indoleacetic acid and indolecarboxylic acid in root nodules and roots of Lupinus luteus L. Acta Bot. Neerl. 16, 222–230.Google Scholar
  48. Ellfolk, N., Sievers, G., 1971: The primary stucture of soybean leghaemoglobin. Acta, Chem. Scand. 25, 3532–3534.Google Scholar
  49. Finan, T. M., Wood, J. M., Jordan, D. C., 1983: Symbiotic properties of C4-dicarboxylic acid transport mutants of Rhizobium leguminosarum. J. Bacteriol. 154, 1403–1413.PubMedGoogle Scholar
  50. Fuchsman, W., Appleby, C. A., 1979: Separation and determination of relative concentrations of the homogenous components of soybean leghemoglobins by isoelectric focusing. Biochim. Biophys. Acta, 579, 314–324.PubMedGoogle Scholar
  51. Francis, A. J., Alexander, M., 1972: Catalase activity and nitrogen fixation in legume nodules. Can. J. Microbiol. 18, 861–864.PubMedGoogle Scholar
  52. Fuller, F., Künstner, P., Nguyen, T., Verma, D. P. S., 1983: Nodulin genes of soybean: Analysis of cDNA clones reveals several abundant sequences in nitrogen fixing root nodules. Proc. Nat. Acad. Sci. 80, 2594–2599.PubMedGoogle Scholar
  53. Fuller, F., Künstner, P., Nguyen, T., Verma, D. P. S., 1983: Nodulin genes of soybean: Analysis of cDNA clones reveals several abundant sequences in nitrogen fixing root nodules. Proc. Nat. Acad. Sci. 80, 2594–2599.PubMedGoogle Scholar
  54. Gibson, A. M., 1964: Genetic control of strain-specific ineffective nodulation in Trifolium subterraneum L. Aust. J. Agric. Res. 15, 37–49.Google Scholar
  55. Glenn, A. R., Brewin, N. J., 1981: Succinate resistant mutants of Rhizobium leguminosarum. J. Gen. Microbiol. 126, 237–241.Google Scholar
  56. Groat, R. G., Vance, C. P., 1982: Root and nodule enzymes of ammonia assimilation in two plant conditioned symbiotically ineffective genotypes of alfalfa (Medicago sativa L.). Plant Physiol. 69, 614–618.PubMedGoogle Scholar
  57. Hanks, J. F., Schubert, K., Olbert, N. E., 1983: Isolation and characterization of infected and uninfected cells from soybean nodules. Role of uninfected cells in ureide synthesis. Plant Physiol. 71, 869–873.PubMedGoogle Scholar
  58. Hardy, R. W. F., Havelka, U. D., 1976: Photosynthate as a major factor limiting nitrogen fixation by field-grown legumes with emphasis on soybeans. In: Symbiotic Nitrogen Fixation in Plants. Nutman, P. S. (ed.), New York/London: Cambridge Univ. Press, pp. 421–439.Google Scholar
  59. Herridge, D. F., Atkin, C. A., Pate, J. S., Rainbird, R. M. 1978: Allantoin and allentoic acids in the nitrogen economy of the cowpea (Vigna unguiculata). Plant Physiol. 62, 459–498.Google Scholar
  60. Holl, F. B., 1973a: Host-determined genetic control of nitrogen fixation with PisumRhizobium symbiosis. Can. J. Genet. Cytol. 15, 659.Google Scholar
  61. Holl, F. B., 1973b: A nodulatiog strain of Pisum unable to fix nitrogen. Plant Physiol. 51, suppl., p. 35.Google Scholar
  62. Holl, F. B., 1975: Host plant control of the inheritance of dinitrogen fixation with Pisum-Rhizobium symbiosis. Euphytica 24, 767–770.Google Scholar
  63. Holl, F. B., LaRue, T. A., 1976: Genetics of legume host plants. In: Proc. Ist International Symposium on Nitrogen Fixation. Vol. II. Newton, W. E., Nyman, C. J. (eds.), Pullman, Wash.: Washington State Univ. Press, pp. 391–399.Google Scholar
  64. Hunt, L. T., Hurst-Caldrone, S., Doughhof, M. O., 1978: Globins. In: Atlas of protein sequences and structure. 5 supp. 3, 229–251.Google Scholar
  65. Hurrell, J. G. R., Leach, S. J., 1977: The amino acid sequence of soybean leghaemoglobin c2. FEBS letters 80, 23–26.PubMedGoogle Scholar
  66. Hurrell, J. G. R., Nicola, N. A., Leach, S. J., 1979: Evolutionary and structural relationship of leghemoglobins. In: Soil Microbiology and Plant Nutrition. Broughton, W. J., John, C. K. (eds.), Kuala Lumpur: University of Malaya Press, pp. 253–281.Google Scholar
  67. Jensen, E. O., Palndon, K., Hyldig-Neilson, J. J., Jorgensen, P., Marker, K. A., 1981: The structure of a chromosomal gene from soybean. Nature 291, 677–679.Google Scholar
  68. Jochimsen, B., Rasmussen, O., 1982: Appearance of nodule-specific proteins in effective compared to ineffective nodules of soybean. In: Molecular Genetics of the Bacteria-Plant Interaction. Pühler, A. (ed.), ( Abs.). Symp., Univ. of Bielefeld.Google Scholar
  69. Koa, J. L., Perry, K. L., Kado, C. I., 1982: Indoacetic acid complementation and its relation to host range specifying genes on the Ti plasmid of Agrobacterium tumefaciens. Mol. Gen. Gen. 188, 425–432.Google Scholar
  70. Kefford, N. P., Brockwell, J., Zwar, J. A., 1960: The symbiotic synthesis of auxin by legumes and nodule bacteria and its role in nodule development. Aust. J. Biol. Sci. 13, 456–467.Google Scholar
  71. Kidby, D. K., Goodchild, D. J., 1966: Host influence in the ultrastructure of root nodules of Lupinus luteus and Ornithopus sativus. J. Gen. Microbiol. 45, 147–152.Google Scholar
  72. Kondorosi, A., Svab. Z., Kiss, G. B., Dixon, R. A., 1977: Ammonium assimilation and nitrogen fixation in Rhizobium meliloti. Mol. Gen. Genet. 151, 221–226.Google Scholar
  73. Kondorosi, A., Johnston. A. W. B., 1981: The Genetics of Rhizobium. In: International Rev. of Cytol. suppl. 13. Giles, K. L., Atherly, A. G. (eds.), New York: Academic Press, pp. 191–224.Google Scholar
  74. Kubo, H., 1939: Über das Hämoprotein aus den Wurzelknöllchen von Leguminosen. Acta. Phytochim 11, 195–200.Google Scholar
  75. Kuykendall, L. D., 1981: Mutants of Rhizobium that are altered in legume interaction and nitrogen fixation. In: Int. Rev. Cytol. Suppl. 13, Giles, K. L., Atherly, A. G. (eds.), New York: Academic Press, pp. 229–309.Google Scholar
  76. Lalonde, M., Knowles, R., 1975: Ultrastructure composition and biogenesis of the encapsulation material surrounding the endophyte in Alnus cripa var mollis root nodules. Can. J. Bot. 53, 1951–1971.Google Scholar
  77. Lara, N., Cullimore, J. V., Lea, P. J., Miflin, B. J., Johnston, A. W. B., Lamb, J. W., 1983: Appearance of a novel form of plant glutamine synthetase during nodule development in Phaseolus vulgaris L. Planta 157, 254–258.Google Scholar
  78. Lee, J., Brown, G. G., Verma, D. P. S., 1983: Arrangement of leghemoglobin genes in soybean chromosome. Nucl. Acid Res. 11, 5541–5553.Google Scholar
  79. Lee, J., Brown, G. G., Verma, D. P. S., 1983: Arrangement of leghemoglobin genes in soybean chromosome. Nucl. Acid Res. 11, 5541–5553.Google Scholar
  80. Legocki, R. P., Verma, D. P. S., 1979: A nodule-specific plant protein (Nodulin-35) from soybean. Science 205, 190–193.PubMedGoogle Scholar
  81. 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.PubMedGoogle Scholar
  82. Leong, S. A., Ditta, G. S., Helinski, D. R., 1982: Heme biosynthesis in Rhizobium. J. Biol. Chem. 257, 8724–8730.PubMedGoogle Scholar
  83. Lepo, J. E., Hanus, F. J., Evans, H. J., 1980: Chemoautotrophic growth of hydrogen-uptake-positive strains of Rhizobium japonicum. J. Bact. 141, 664–670.PubMedGoogle Scholar
  84. Libbenga, K. R., Bogers, R. J., 1974: Root-nodule morphogenesis. In: The biology of nitrogen fixation. Quispel, A. (ed.), Amsterdam: North-Holland, pp. 430–472.Google Scholar
  85. Libbenga, K. R., vanlren, F., Bogers, R. J. Shraag-Lamers, M. F., 1973: The role of hormones and gradients in the initiation of Cotex proliferation and nodule formation in Pisum sativum L. Planta 114, 29–39.Google Scholar
  86. Libbenga, K. R., Torrey, J. G., 1973: Hormone-induced endoreduplication prior to mitosis in cultured pea nodule cortex cells. Am. J. Bot. 60, 293–299.Google Scholar
  87. Lie, T. A., 1971: Symbiotic nitrogen fixation under stress conditions. Plant and Soil spec. vol. 117–127.Google Scholar
  88. Liu, S.-T., Perry, K. L., Schardl, C. L., Kado, C. I., 1982: Agrobacterium Ti-plasmid indoleacetic acid genes is required for crown gall oncogenesis. Proc. Nat. Acad. Sci (U. S. A.) 79, 2812–2816.Google Scholar
  89. Margulis, L., 1981: Symbiosis in Cell Evolution, San Francisco: W. H. Freeman and Co.Google Scholar
  90. Meade, H, Long, S. R., Ruvkun, G. B., Brown, S. E., Ausubel, F. M., 1982: Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon mutagenesis. J. Bact. 149, 114–122.PubMedGoogle Scholar
  91. Nadler, K. D., 1981: A mutant strain of Rhizobium leguminosarum with an abnormality in heme synthesis. In: Current perspectives in nitrogen fixation, Gibson, A. H., Newton, W. E. (eds.), p. 414 ( Abs.), Canberra: Aust. Acad. Science.Google Scholar
  92. Nash, D., Schulman, H., 1976: Leghemoglobin and nitrogenase activity during soybean root nodule development. Can. J. Bot. 54, 2790–2797.Google Scholar
  93. Newcomb, W., 1981: Nodule morphogenesis and differentiation. In: Int. Rev. Cytol. Supp. 13. Giles K. L., Atherly, A. G., (eds.), New York: Academic Press, pp. 247–298.Google Scholar
  94. Newcomb, W., Peterson, R. L., Callaham, D., Torrey, J. G., 1978: Structure and host-actinomycete interactions in developing root nodules of Comptonia peregrine. Can. J. Bot. 56, 502–531.Google Scholar
  95. Newcomb, W., 1976: A correlated light and electron microscope study of symbiotic growth and differentiation in Pisum sativum root nodules. Can. J. Bot. 54, 2163–2186.Google Scholar
  96. Newcomb, W., Sippel, D., Peterson, R. L., 1979a: The early morphogenesis of Glycine max and Pisum sativum root nodules. Can. J. Bot. 57, 2603–2616.Google Scholar
  97. Newcomb, W., Peterson, R. L., 1979b: The occurrence and ontogeny of transfer cells associated with lateral roots and root nodules in Leguminoseae. Can. J. Bot. 57, 2583–2602.Google Scholar
  98. Newcomb, E. H., Tandon, S. R., 1981: Uninfected cells of soybean root nodules: Ultrastructure suggest key role in ureide production. Science 21, 1394–1396.Google Scholar
  99. Noel, K. D., Stacey, G., Tandon, S. R., Silver, L. E., Brill, W. J., 1982: Rhizobium japonicum mutants defective in symbiotic nitrogen fixation. J. Bact. 152, 485–494.PubMedGoogle Scholar
  100. Nutman, P. S., 1952: Studies on the physiology of nodule formation. III Experiments on the excision of root-tips and nodules. Annals of Botany (N. S.) 16, 79–101.Google Scholar
  101. Nutman, P. S., 1954: Symbiotic effectiveness in nodulated red clover. A major gene for ineffectiveness in the host. Heredity 8, 47–60.Google Scholar
  102. Nutman, P. S., 1956: The influence of the legume in root nodule symbiosis. A comparative study of host determinants and functions. Biol. Rev. Camb. Philos. Soc. 31, 109–151.Google Scholar
  103. Nutman, P. S., 1957: Symbiotic effectiveness in nodulated red clover. III. Further studies on inheritance of ineffectiveness in the host. Heredity 11, 157–173.Google Scholar
  104. Nutman, P. S., 1969: Genetics of symbiosis and nitrogen fixation in legumes. Proc. Roy. Soc. B. 172, 417–437.Google Scholar
  105. Nutman, P. S., 1981: Hereditary host factors affecting nodulation and nitrogen fixation. In: Current Perspectives in Nitrogen Fixation. Gibson, A. H., Newton, W. E. (eds.), Canberra: Aust. Academy of Science, pp. 194–204.Google Scholar
  106. O’Gara, F., Shanmugam, K. T., 1976; Regulation of nitrogen fixation by rhizobia: Export of fixed N2 as NH4+. Biochim Biophys. Acta. 437, 313–321.Google Scholar
  107. Orme-Johnson, W. H., 1977: Biochemistry of Nitrogenase. In: Genetic Engineering for Nitrogen Fixation. Hollaender, A., Burris, R. H., Day, P. R., Hardy, R. W., Helinski, D. R, Lamborg, M. R., Owens, L., Vallentine, R. C. (eds.), New York/London: Plenum Press, p. 317–333.Google Scholar
  108. Pankhurst, C. E., Schwinghamer, E., 1974: Adenine requirement for nodulation of pea by an auxotrophic mutant of Rhizobium leguminosarum. Arch. Microbiol. 100, 219–238.Google Scholar
  109. Pate, J. S., Layzell, D. B., McNeil, D. L., 1979a: Modeling the transport and utilization of carbon and nitrogen in a nodulated legume. Plant Physiol. 63, 730–737.PubMedGoogle Scholar
  110. Pate, J. S., Layzell, D. B., Atkins, C. A., 1979b: Economy of carbon and nitrogen in a nodulated and nonnodulated (NO3-grown) legume. Plant Physiol. 64, 1083–1088.PubMedGoogle Scholar
  111. Peters, G. A., Ray, T. B., Mayne, B. C., Toia, R. E., 1980: Azolla-Anabaena association: Morphological and physiological strains. In: Nitrogen Fixation. Newton, W. E., Orme-Johnson, W. M., (eds.), Vol. 2, Baltimore: Univ. Park Press, pp. 293–309.Google Scholar
  112. Peterson, M. A., Barns, D. K., 1981: Inheritance of ineffective nodulation and onnodulation trait in alfalfa. Crop. Sci. 21, 611–616.Google Scholar
  113. Postgate, J. R., 1982: The Fundamentals of Nitrogen Fixation. London/New York: Cambridge University Press.Google Scholar
  114. Puppo. A., Rigaud, J., Job, D., 1980: Leghemoglobin reduction by a nodule reductase. Plant Sci. Let. 20, 1–6.Google Scholar
  115. Puppo, A., Rigaud, J., 1975: Indole 3 acetic acid oxidation by leghemoglobin from soybean nodules. Physiol. Plant. 35, 181–185.Google Scholar
  116. Rawsthorne, S., Minchin, F. R., Summerfields, R. J., Cookson, C., Combes, J., 1980: Carbon and nitrogen metabolism in legume root nodules. Phytochem. 19, 341–355.Google Scholar
  117. Reisert, P. S., 1981: Plant cell surface structure and recognition phenomena with reference to symbiosis. In: Int. Rev. Cytol. Supp. 12. pp. 71–112.Google Scholar
  118. Reynolds, P. H. S., Farnden, K. J. F., 1979: The involvement of aspartate amonotransferases in ammonium assimilation in lupine nodules. Phytochemistry 18, 1625–1630.Google Scholar
  119. Reynolds, P. H. S., Blevins, D. G., Boland, M. J., Schubert, K. R., Randal, D. D., 1982: Enzymes of ammonia assimilation in legume nodules: A comparison between ureide-and amide-transporting plants. Physiol. Plant. 55, 255–260.Google Scholar
  120. Robertson, J. G., Lyttleton, P., Bullivant, S., Graston, G. F., 1978a: Membranes in lupine root nodules I. The role of Golgi bodies in the biogenesis of infection threads and peribacteroid membranes. J. Cell Sci. 30, 129–149.PubMedGoogle Scholar
  121. Robertson, J. G., Warburton, M. P., Lyttleton, P., Fordyce, A. M., Bullivant, S., 1978b: Membranes in lupine root nodules II. Preparation and properties of peribacteroid membranes and bacteroid envelope inner membranes from developing root nodules. Ibiol. 30, 151–174.Google Scholar
  122. Robertson, J. G., Lyttleton, P., 1982: Coated and smoot vesicles in the biogenesis of cell walls, plasma membranes, infection threads and peribacteroid membranes in root hairs and nodules of white clover. J. Cell. Sci. 58, 63–78.PubMedGoogle Scholar
  123. Robertson, J. G., Warburton, M. P., Farnden, K. J. F., 1975b: Induction of gluta- mate synthase during nodule development in lupin: FEBS Letts. 55, 33–37.Google Scholar
  124. Roessler, P. G., Nadler, K. D., 1982: Effects of iron deficiency on heure biosynthesis in Rhizobium japonicum. J. Bacteriol. 149, 1021–1026.PubMedGoogle Scholar
  125. Rolfe, B. G., Gresshoff, P. M., 1980: Rhizobium trifolii mutant interactions during establishment of nodulation in white clover. Aust. J. Biol. Sci. 33, 491–504.Google Scholar
  126. Ronson, C. W., Lyttleton, P., Robertson, J. G., 1981: C4-dicarboxylate transport mutants of Rhizobium trifolii from ineffective nodules of Trifolium repens. Proc. Nat. Acad. Sci. (U. S. A.) 78, 4284–4288.Google Scholar
  127. Ronson, C. W., Primrose, S. B., 1979: Carbohydrate metabolism in Rhizobium trifolii: identification and symbiotic properties of mutants. J. Gen. Microbiol. 112, 77–88.Google Scholar
  128. Ryan, E., Bodley, F., Fottrell, P. F., 1972: Purification and characterization of aspartate aminostransferases from soybean rot nodules and Rhizobium japonicum. Phytochem. 11, 957–963.Google Scholar
  129. Sahlmman, K., Fahraeus, G., 1963: An electron microscope study of root hair infection by Rhizobium. J. Gen Microbiol. 33, 425–427.Google Scholar
  130. Schwinghamer, E. A., 1970: Requriement for riboflavin for effective symbiosis on clover by an auxotrophic mutant strain of Rhizobium trifolii. Aust. J. Biol. Sci. 23, 1187–1196.Google Scholar
  131. Scott, D. B., Robertson, J. G., Farnden, K. J. F., 1976: Ammonia assimilation in lupine nodules. Nature 263, 703–708.Google Scholar
  132. Scott, K. F., Hughes, J. E., Gresshoff, P. M., Beringer, J. E., Rolfe, G. G., Shine, J., 1982: Molecular cloning of Rhizobium trifolii genes involved in symbiotic nitrogen fixation. J. Mol. App. Gen. 1, 315–326.Google Scholar
  133. Schwinghamer, E. A., 1977: Genetic aspects of nodulation and dinitrogen fixation by legumes: The microsymbiont. In: A Treatise on Dinitrogen Fixation III. Biology. Hardy, R. W. F., Silver, W. S. (eds.), p. 675, London: Wiley-Interscience.Google Scholar
  134. Sequeira, 1980: Defenses triggered by the invader: Recognition and compatibility phenomena. In: Plant Disease, vol. V, New York: Acadmic Press.Google Scholar
  135. Shubert, K. R., 1981: Enzymes of purine biosynthesis and catabolism in Glycine max. I. Comparison of activities with N2 fixation and composition of xylem exudate during nodule development. Plant Physiol. 68, 1115–1122.Google Scholar
  136. Streeter, J. G., 1977: Asparaginase and asparagine transaminase in soybean leaves and root nodules. Plant Physiol. 60, 235–239.PubMedGoogle Scholar
  137. Sullivan, D., Brisson, N., Goodchild, B., Verma, D. P. S., Thomas, D., 1981: Molecular cloning and organization of two leghemoglobin genomic sequences of soybean. Nature 289, 516–518.Google Scholar
  138. Sutton, W. D., Pankhurst, C. E., Craig, A. S., 1981: The Rhizobium bacteroid state. In: Int. Rev. Cytol., Suppl. 13, Giles, K. L., Atherly, A. G. (eds.), New York: Academic Press, pp. 149–177.Google Scholar
  139. Tajima, S., Yamamoto, Y., 1975: Enzymes of purine catabolism in soybean plants. Plant and Cell Physiol. 16, 271–282.Google Scholar
  140. Thimann, K. V., 1936: On The physiology of formation of nodules in legume roots. Proc. Nat. Acad. Sci. (U. S. A.) 22, 511–514.Google Scholar
  141. Trinchant, J. C., Birot A. M., Rigaud, J., 1981: Oxygen supply and energy-yielding substrates for nitrogen fixation (acetylene reduction) by bacteroid preparations. J. Gen. Microbiol. 125, 159–165.Google Scholar
  142. Triplett, E. W., Blevins, D. G., Randal, D. D., 1982: Purification and properties of soybean xanthine dehydrogenase. Arch. Biochem. Biophys. 219, 39–46.PubMedGoogle Scholar
  143. Truchet, G., 1978: Sur l’état diploide des cellules du méristème des nodules radiculaires des légumineruses. Ann. Sc. Nat. Bot. Biol. rég. 19, 3–38.Google Scholar
  144. Truchet, G., Michel M., Dénarié, J., 1980: Sequential analysis of the organogenesis of lucerne (Medicago sativa) root nodules using symbiotically-defective mutants of Rhizobium meliloti. Differentiation 16, 163–172.Google Scholar
  145. Verma, D. P. S., Bewley, J. D., Auger, S., Fuller, F., Purohit, J., Künstner, P., 1983a: Host genes involved in symbiosis with Rhizobium. In: Genetic Engineering. Application to Agriculture, Owens, L. D. (ed.), London/New Jersey: Granada Pub./Romman and Allanhead Pub, pp. 236–245.Google Scholar
  146. Verma, D. P. S., Bewley, J. D., Auger, S., Fuller, F., Purohit, J., Künstner, P., 1983a: Host genes involved in symbiosis with Rhizobium. In: Genetic Engineering. Application to Agriculture, Owens, L. D. (ed.), London/New Jersey: Granada Pub./Romman and Allanhead Pub, pp. 236–245.Google Scholar
  147. Verma, D. P. S., Bergmann, H., Fuller, F., Preddie, E., 1983c: The role of plant genes in soybean-Rhizobium interactions. In: Molecular genetics of the bacteria plant interaction, Pühler, A. (ed.), Berlin–Heidelberg–New York: Springer, pp. 156–163.Google Scholar
  148. Verma, D. P. S., 1982: Host-Rhizobium interactions during symbiotic nitrogen fixation, In: The molecular biology of plant development. Smith, H., Grierson, D., (eds.), Oxford: Blackwell Pub, pp. 437–466.Google Scholar
  149. Verma, D. P. S., Bal, A. K., 1976: Intracellular site of synthesis and localization of leghaemoglobin in soybean root nodules. Proc. Nat. Acad. Sci. (U. S. A.) 73, 3843–3847.Google Scholar
  150. Verma, D. P. S., Hunter, N., Bal, A. K., 1978a: Asymbiotic association of Rhizobium with pea epicotyls treated with plant hormone. Planta 138, 107–110.Google Scholar
  151. Verma, D. P. S., Kazazian, V., Zogbi, V., Bal, A. K., 1978b: Isolation and characterization of the membrane envelope enclosing the bacteroids in soybean root nodules. J. Cell Biol. 78, 919–936.PubMedGoogle Scholar
  152. Verma, D. P. S., Legocki, R., Auger, S., 198 lb: Expression of nodule specific genes of soybean. In: Current perspectives in nitrogen fixation. Gibson, A. H., Newton, W. E., (eds.), Canberra: Aust. Acad. Sci, pp. 205–208.Google Scholar
  153. Verma, D. P. S., Ball, S., Guérin, C., Wanamaker, L., 1979: Leghemoglobin biosynthesis in soybean root nodules. Characterization of nascent and released peptides and the relative rate of synthesis of major leghemoglobins. Biochem. 18, 476–483.Google Scholar
  154. Verma, D. P. S., Haugland, R., Brisson, N., Legocki, R., Lacroix, L., 1981: Regulation of the expression of leghemoglobin genes in effective and ineffective root nodules of soybean. Biochim. Biophys. Acta, 653, 98–107.PubMedGoogle Scholar
  155. Verma, D. P. S., Long, S., 1983: The molecular biology of Rhizobium-legume symbiosis. Int. Rev. Cytol. Suppl. 14, Jeon, K. (ed.), p. 211–245, New York: Academic Press.Google Scholar
  156. Vest, G., 1970: Rj3 — A gene conditioning ineffective nodulation in soybean. Crop Sci. 10, 34–35.Google Scholar
  157. Vest, G., Caldwell, B. F., 1972: Rj4 — a gene conditioning ineffective nodulation in soybean. Crop. Sci. 12, 692–693.Google Scholar
  158. Vincent, 1980: Factors controlling the legume-Rhizobium symbiosis. In: Nitrogen Fixation Vol. II, Newton, W. E., Orme-Johnson, H. H. (eds.), Baltimore: Univ. Park Press, pp. 103–129.Google Scholar
  159. Vose, P. B., Ruschel, A. P., 1981: Associative nitrogen fixation. Cleveland: CRC Press.Google Scholar
  160. Wang, T. L., Wood, E. A., Brewin, N. J., 1982: Growth regulators, Rhizobium and nodulation in peas. Indole-3-acetic acid from the culture medium of nodulating and non-nodulating strains of R. leguminosarum. Planta 155, 345–349.Google Scholar
  161. Werner, D., Morschel, E., Striplf, R., Winchenbach, B., 1980: Development of nodules of Glycine max infected with an ineffective strain of Rhizobium japonicum. Planta 147, 320–329.Google Scholar
  162. Whittaker, R. G., Lennox, S., Appleby, C. A., 1981: Relationship of the minor soybean leghemoglobins dl, d2 and d3 to the major leghemoglobins cl, c2 and c3. Biochem. Int. 3, 117–124.Google Scholar
  163. Wiborg, O., Hyldig-Nielsen, J. J., Jensen, E. O., Palndan, K., Marcker, K. A., 1982: The nucleotide sequences of two leghemoglobin genes from soybean. Nucl. Acid. Res. 10, 3487–3494.Google Scholar
  164. Williams, L. F., Lynch, D. L., 1954: Inheritance of a non-nodulating character in soybean. Agronomy 46, 28–29.Google Scholar
  165. Wittenberg, J. B., Bergersen, F. J., Appleby, C. A., Turner, G. L., 1974: Facilitated oxygen diffusion. The role of leghemoglobin in nitrogen fixation by bacteroids isolated from soybean root nodules. J. Biot Chem. 249, 4057–4066.Google Scholar
  166. Yao, P. Y., Vincent, J. M., 1976: Factors responsible for the curling and branching of clover root hairs by Rhizobium. Plant Soil 45, 1–16.Google Scholar

Copyright information

© Springer-Verlag/Wien 1984

Authors and Affiliations

  • D. P. S. Verma
    • 1
  • K. Nadler
    • 1
    • 2
  1. 1.Department of BiologyMcGill UniversityMontrealCanada
  2. 2.Department of Botany and Plant PathologyMichigan State UniversityEast LansingUSA

Personalised recommendations