Plant and Soil

, Volume 186, Issue 1, pp 173–187 | Cite as

Host genetic control of symbiosis in soybean (Glycine max L.)

  • T. E. Devine
  • L. D. Kuykendall


Genes controlling nitrogen-fixing symbioses of legumes with specialized bacteria known as rhizobia are presumably the products of many millions of years of evolution. Different adaptative solutions evolved in response to the challenge of survival in highly divergent complexes of symbionts. Whereas efficiency of nitrogen fixation appears to be controlled by quantitative inheritance, genes controlling nodulation are qualitatively inherited. Genes controlling nodulation include those for non-nodulation, those that restrict certain microsymbionts, and those conditioning hypernodulation, or supernodulation. Some genes are naturally occurring polymorphisms, while others were induced or were the result of spontaneous mutations. The geographic patterns of particular alleles indicate the role of coevolution in determining symbiont specificites and compatibilities. For example, the Rj4 allele occurs with higher frequency (over 50%) among the soybean (G. max) from Southeast Asia. DNA homology studies of strains of Bradyrhizobium that nodulate soybean indicated two groups so distinct as to warrant classification as two species. Strains producing rhizobitoxine-induced chlorosis occur only in Group II, now classified as B. elkanii. Unlike B. japonicum, B. elkanii strains are characterized by (1) the ability to nodulate the rj1 genotype, (2) the formation of nodule-like structures on peanut, (3) a relatively high degree of ex planta nitrogenase activity, (4) distinct extracellular polysaccharide composition, (5) distinct fatty acid composition, (6) distinct antibiotic resistance profiles, and (7) low DNA homology with B. japonicum. Analysis with soybean lines near isogenic for the Rj4 versus rj4 alleles indicated that the Rj4 allele excludes a high proportion of B. elkanii strains and certain strains of B. japonicum such as strain USDA62 and three serogroup 123 strains. These groups, relatively inefficient in nitrogen fixation with soybean, tend to predominate in soybean nodules from many US soils. The Rj4 allele, the most common allelic form in the wild species, has a positive value for the host plants in protecting them from nodulation by rhizobia poorly adapted for symbiosis.

Key words

Bradyrhizobium legumes nitrogen fixation Nod Factors nodulation Rhizobium 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Akao S and Kouchi H 1992 A supernodulating mutant isolated from soybean cultivar Enrei. Soil Sci. Plant Nutr. 38, 183–187.Google Scholar
  2. An J, Carlson R W, Glushka J and Streeter J G 1995 The structure of a novel polysaccharide produced by Bradyrhizobium species within soybean nodules. Carbohydr. Res. 269, 303–317.Google Scholar
  3. Buzzell R I, Buttery B R and Ablett G R 1990 Supernodulation mutants in Elgin 87 soybean. In Nitrogen Fixation: achievements and objectives. Eds. P M Gresshoff, L E Roth, G Stacey and W E Newton. p. 726. Chapman and Hall, New York, USA.Google Scholar
  4. Caetano-Anolles G and Gresshoff P M 1990 Early induction of feedback regulatory responses governing nodulation in soybean. Plant Sci. 71, 69–81.Google Scholar
  5. Caetano-Anolles G and Gresshoff P M 1991 Efficiency of nodule initiation and autoregulatory responses in a supernodulating soybean mutant. Appl. Environ. Microbiol. 57, 2205–2210.Google Scholar
  6. Caldwell B E 1966 Inheritance of a strain specific ineffective nodulation in soybeans. Crop Sci. 6, 427–428.Google Scholar
  7. Carlson R W, Sanjuan J, Bhat U R, Glushka J, Spaink H P, Wijfjes A H M, van Brussel A A N, Stokkermans T J W, Peters N K and Stacey G 1993 The structures and biological activities of the lipo-oligosaccharide nodulation signals produced by type I and II strains of Brahyrhizobium japonicum. J. Biol. Chem. 268, 18372–18381.Google Scholar
  8. Carroll B J, McNeil D L and Gresshoff P M 1985 A supernodulation and nitrate-tolerant symbiotic (nts) soybean mutant. Plant Physiol. 78, 34–40.Google Scholar
  9. Cho M J and Harper J E 1991 Root isoflavanoid response to grafting between wild-type and nodulation-mutant soybean plants. Plant Physiol. 96, 1277–1282.Google Scholar
  10. Cregan P B and Keyser H H 1986 Host restriction of nodulation by Rhizobium japonicum strain USDA 123. Crop Sci. 26, 911–916.Google Scholar
  11. Delves A C, Carroll B J and Gresshoff P M 1988 Genetic analysis and complementation studies on a number of mutant supernodulatin soybean lines. J. Genet. 67, 1–8.Google Scholar
  12. Delves A C, Higgins A and Greshoff P M 1992 Shoot apex removal does not alter autoregulation of nodulation in soybean. Plant Cell Environ. 15, 249–254.Google Scholar
  13. Delves A C, Mathews A, Day D A, Carer A S, Carroll B T and Greshoff P M 1986 Regulation of soybean-Rhizobium symbiosis by shoot and root factors. Plant Physiol. 82, 588–590.Google Scholar
  14. Devine T E 1984 Genetics and breeding of nitrogen fixation. In Biological Nitrogen Fixation. Ed. M Alexander. pp 127–154. Plenum Press, New York, USA.Google Scholar
  15. Devine T E 1985 Nadulation of soybean (Glycine max L. Merr.) plant introduction lines with the fast-growing rhizobial strain USDA205. Crop Sci. 25, 354–356.Google Scholar
  16. Devine T E 1987 A comparison of rhizobial strain compatibilities of Glycine max and its progenitor species Glycine soja. Crop Sci. 27, 635–639.Google Scholar
  17. Devine T E 1989 The role of co-evolution in the soybean/microsymbiont interaction In World Soybean Research Conference IV Proceedings. Ed. A J Pascale. pp 1119–1124. Orientacion Grafica Editora S R L, Buenos Aires, Argentina.Google Scholar
  18. Devine T E and Breithaupt B H 1981 Frequencies of nodulation response alleles, Rj2 and Rj4, in soybean plant introductions and breeding lines. USDA Tech. Bull., No. 1628.Google Scholar
  19. Devine T E, Kilen T C and O'Neill J J 1991 Genetic linkage of the phytophthora resistance gene Rps2 and the nodulation response gene Rj2 in soybean. Crop Sci. 713–715.Google Scholar
  20. Devine T E and Kuykendall L D 1994 Rfg1, a soybean gene controlling nodulation with fast growing Rhizobium fredii strain 205. Plant and Soil 158, 47–51.Google Scholar
  21. Devine T E, Kuykendall L D and Breithaupt B H 1983 Nodule-like structures induced on peanut by chloriosis producing strains of Rhizobium classified as R. japonicum. Crop Sci. 23, 394–397.Google Scholar
  22. Devine T E, Kuykendall L D and O'Neill J J 1988 DNA homology group and the identity of bradyrhizobial strains producing rhizobitoxine-induced foliar chlorosis on soybean. Crop Sci. 28, 939–941Google Scholar
  23. Devine T E, Kuykendall L D and O'Neill J J 1990 The Rj4 allele in soybean represses nodulation by chlorosis-inducing bradyrhizobia classified as DNA homology group II by antibiotic resistance profiles. Theor. Appl. Genet. 80, 33–37.Google Scholar
  24. Devine T E, Kuykendall L D and O'Neill J J 1991 Nodulation interaction of the soybean allele Rj2 with asiatic isolates of Bradyrhizobium japonicum. Crop Sci. 31, 1129–1131.Google Scholar
  25. Devine T E and O'Neill J J 1986 Registration of BARC-2 (Rj4) and BARC-3 (rj4) soybean germplasm. Crop Sci. 26, 1263–1264.Google Scholar
  26. Devine T E and O'Neill J J 1987 Registration of BARC-4 (Rj2) and BARC-5 (rj2) soybean germplasm. Crop Sci. 27, 1322–1323.Google Scholar
  27. Devine T E, O'Neill J J and Kuykendall L D 1993 Near isogenic lines of soybeans as tools to identify nodulation specific mutants of Bradyrhizobium elkanii. Plant and Soil 149, 205–209.Google Scholar
  28. Devine T E, Palmer R G and Buzzell R I 1983 Analysis of genetic linkage in the soybean. J. Heredity 74, 457–460.Google Scholar
  29. Devine T E and Weber D F 1977 Genetic specificity of nodulation. Euphytica 26, 527–535.Google Scholar
  30. Dobert R C, Breil B T and Triplett E W 1994 DNA sequence of the common nodulation genes of Bradyrhizobium elkanii and their phylogenetic relationship to those of other nodulating bacteria. Mol. Plant-Microbe Inter. 7, 564–572.Google Scholar
  31. Dockendorff T C, Sanjuan J, Grob P and Stacey G 1994 NolA represses nod gene expression in Bradyrhizobium japonicum. Mol Plant-Microbe Inter. 7, 596–602.Google Scholar
  32. Dowdle S F and Bohlool B B 1985 Predominance of fast-growing Rhizobium japonicum in a soybean field in the People's Republic of China. Appl. Environ. Microbiol. 50, 1171–1176.Google Scholar
  33. Erdman L W, Johnson H W and Clark F 1957 Varietal responses of soybeans to a bacterial-induced chlorosis. Agron. J. 49, 267–271.Google Scholar
  34. Fuhrmann J J 1990 Symbiotic effectiveness of indigenous soybean bradyrhizobia as related to serological, morphological, rhizobitoxin and hydrogenase phenotype. Appl. Environ. Microbiol. 56, 224–229.Google Scholar
  35. Fukuhara H, Minakawa Y, Akao S and Minamisawa K 1994 The involvement of indole-3-acetic acid produced by Bradyhizobium elkanii in nodule formation. Plant Cell Physiol. 35, 1261–1265.Google Scholar
  36. Gremaud M F and Harper J E 1989 Selection and initial characterization of partially nitrate tolerant nodulation mutants of soybean. Plant Physiol. 89, 169–173.Google Scholar
  37. Gresshoff P M 1993 Molecular genetic analysis of nodulation genes in soybean. In Plant Breeding Reviews. Ed. J Janick. Vol. 11. pp 275–318. John Wiley and Sons Publishers, New York, NY, USA.Google Scholar
  38. Gresshoff P M 1993 Plant function in nodulation and nitrogen fixation in legumes. In New Horizons in Nitrogen Fixation. Eds. R Palacios, J Mora and W E Newton. pp 31–54. Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
  39. Hadley H H and Hymowitz T 1973 Speciation and cytogenetics. In Soybeans: Improvement, Production, and Uses. Ed. B E Caldwell. Agronomy 16, 97–116.Google Scholar
  40. Harper J E and Nickell C D 1995 Genetic analysis of nonnodulating soybean mutants in a hypernodulated background. Soybean Genet. Newsl. 22, 185–190.Google Scholar
  41. Hedges B R, Sellner J M, Devine T E and Palmer R G 1990 Assigning isocitrate dehydrogenase to linkage group 11 in soybean. Crop Sci. 30, 940–942.Google Scholar
  42. Hollis A B, Kloos W E and Elkan G H 1981 DNA: DNA hybridization studies of Rhizobium japonicum and related Rhizobiaceae. J. Genet. Microbiol. 123, 215–222.Google Scholar
  43. Hubbell D H and Elkan G H 1967 Correlation of physiological characteristics with nodulating abilty in Rhizobium japonicum. Can. J. Microbiol. 13, 235–241.Google Scholar
  44. Huber T A, Agarwal A K and Keister D L 1984 Extracellular polysaccharide composition, ex planta nitrogenase activity, and DNA homology in Rhizobium japonicum. J. Bacteriol. 158, 1168–1171.Google Scholar
  45. Hunter W J and Kuykendall L D 1990 Enhanced nodulation and nitrogen fixation by a revertant of a nodulation-defective Bradyrhizobium japonicum tryptophan auxotroph. Appl. Environ. Microbiol. 56, 2399–2403.Google Scholar
  46. Hunter W J and Kuykendall L D 1995 Symbiotic properties of 5-methyltryptophan-resistant mutants of Bradyrhizobium japonicum. Plant and Soil 173, 293–298.Google Scholar
  47. Jordan D C 1982 Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow-growing, root nodule bacteria from leguminous plants. Int. J. System. Bacteriol. 32, 136–139.Google Scholar
  48. Keister D L and Marsh S S 1990 Hemoproteins of Bradyrhizobium japonicum cultured cells and bacteroids. Appl. Environ. Microbiol. 56, 2736–2741.Google Scholar
  49. Keyser H H and Cregan P B 1987 Nodulation and competition for nodulation of selected soybean genotypes among Bradyrhizobium japonicum serogroup 123 isolates. Appl. Environ. Microbiol. 53, 2631–2635.Google Scholar
  50. Keyser H H, Weber D F and Uratsu S L 1984 Rhizobium: japonicum serogroup and hydrogenase phenotype distribution in 12 states. Appl. Environ. Microbiol. 47, 613–615.Google Scholar
  51. Kokubun M and Akao S 1994 Inheritance of supernodulation in soybean mutant En6500. Soil Sci. Plant Nutr. 40, 715–718.Google Scholar
  52. Krishnan H B and Pueppke S G 1992 Inactivation of nolC conditions developmental abnormalities in nodulation of Peking soybean by Rhizobium fredii USDA257. Mol Plant-Microbe Inter. 5 14–21.Google Scholar
  53. Krishnan H B and Pueppke S G 1994 Cultivar-specific genes of the nitrogen-fixing soybean symbiont, Rhizobium fredii USA257, also regulate nodulation of Erythrina spp. Am. J. Bot. 8, 38–45.Google Scholar
  54. Kummer R M and Kuykendall L D 1989 Symbiotic properties of amino acid auxotrophs of Bradyrhizobium japonicum. Soil Biol. Biochem. 21, 779–782.Google Scholar
  55. Kuykendall L D 1989 Influence of Glycine max nodulation on the persistence in soil of a genetically marked strain of Bradyrhizobium japonicum. Plant and Soil 116, 275–277.Google Scholar
  56. Kuykendall L D, Devine T E and Cregan P B 1982 Positive role of nodulation on the establishment of Rhizobium japonicum in subsequent crops of soybean. Current Microbiol. 7, 79–81.Google Scholar
  57. Kuykendall L D, Hahn M, Hennecke H and Hunter W J 1992 Genetically improved rhizobia and their use in agriculture. In Biological Nitrogen Fixation and Sustainability of Tropical Agriculture. Eds. K Mulongoy, M Gueye and D S C Spencer. pp 211–210. John Wiley and Sons, London, UK.Google Scholar
  58. Kuykendall L D and Hunter W J 1991 Enhancement of nitrogen fixation with Bradyrhizobium japonicum mutants. US Patent 5,021,076.Google Scholar
  59. Kuykendall L D and Hunter W J 1995 Symbiotic ineffectiveness of trpCD deletion mutants of Bradyrhizobium japonicum. Soil Biol. Biochem. 27, 1035–1039.Google Scholar
  60. Kuykendall L D, Roy M A, O'Neill J J and Devine T E 1988 Fatty acids, multiple antibiotic resistance, and DNA homology among Bradyrhizobium japanicum strains. Int. J. Syst. Bacteriol. 37, 358–361.Google Scholar
  61. Kuykendall L D, Saxena B, Devine T E and Udell S E 1992 Genetic diversity in Rhizobium japonicum and a proposal for Bradyrhizobium elkanii sp. nov. Can. J. Microbiol. 38, 501–505.Google Scholar
  62. Lohrke S M, Orf J H, Martinez-Romero E and Sadowsky M J 1995 Host-controlled restriction of nodulation of Bradyrhizobium japonicum strains in Serogroup 110. Appl. Environ. Microbiol. 61, 2378–2383.Google Scholar
  63. Mathews A, Carroll B J and Gresshoff P M 1989 A new nonnodulation gene in soybean. J. Heredity 80, 357–360.Google Scholar
  64. Mathews A, Carroll B J and Gresshoff P M 1990 The genetic interaction between non-nodulation and supernodulation in soybean: an example of developmental epistasis. Theor. Appl. Genet. 79, 125–130.Google Scholar
  65. Meinhardt L W, Krishnan H B, Balatti P A and Pueppke S G 1993 Molecular cloning and characterization of a sym plasmid locus that regulates cultivar-specific nodulation of soybean by Rhizobium fredii USA257. Mol. Microbiol. 9, 17–29.Google Scholar
  66. Minamisawa K 1989 Extracellular polysaccharide composition, rhizobitoxine production, and hydrogenase phenotype in Bradyrhizobium japonicum. Plant Cell Physiol. 30, 877–884.Google Scholar
  67. Minamisawa K and Fukai K 1991 Production of indole-3-acetic acid by Bradyrhizobium japonicum. A correlation with genotype grouping and rhizobitoxine production. Plant Cell Physiol. 32, 1–9.Google Scholar
  68. Murphy S G and Elkan G H 1965 Nitrogen metabolism of some strains of Rhizobium japonicum having different nodulating capacities. Can. J. Microbiol. 11, 1039–1041.Google Scholar
  69. Nangju D 1980 Soybean response to indigenous rhizobia as influenced by cultivar origin. Agron. J. 72, 403–406.Google Scholar
  70. Palmer R G and Kilen T C 1987 Qualitative genetics and cytogenetics. In Soybeans: Improvement, Production and Uses. Ed. J R Wilcox. Agronomy 16, 135–209.Google Scholar
  71. Polhill R M, Raven P H and Stirton C H 1981 Evolution and Systematics of the Leguminosae. In Advances in Legume Systematics. Part I. Eds. R M Polhill and R H Raven. pp 1–26. Royal Botanic Gardens, Kew, UK.Google Scholar
  72. Pracht J E, Nickell C D and Harper J E 1993 Genes controlling nodulation in soybean: Rj5 and Rj6. Crop Sci. 33, 711–713.Google Scholar
  73. Pracht J E, Nickell C D, Harper J E and Bullock D G 1994 Agronomic evaluation of non-nodulating and hypernodulating mutants of soybean. Crop Sci. 34, 738–740.Google Scholar
  74. Pueppke S G and Payne J H 1987 Responses of Rj1 and rj1 soybean isolines to inoculation with Bradyrhizobium japonicum. Plant Physiol. 84, 1291–1295.Google Scholar
  75. Sadowsky M J and Cregan P B 1992 The soybean Rj4 allele restricts nodulation by Bradyrhizobium japonicum serogroup 123 strains. Appl. Environ. Microbiol. 58, 720–723.Google Scholar
  76. Scholla M H and Elkan G H 1984 Rhizobium fredii sp. nov., a fast growing bacterium that effectively nodulates soybeans. Int. J. Syst. Bacteriol. 34, 484–486.Google Scholar
  77. Shoemaker R, Polzin K, Lorenzen L and Specht J 1995 Molecular genetic mapping of soybean: Map utilization. Crop Sci. 32, 1091–1098Google Scholar
  78. Song L, Carroll B J, Gresshoff P M and Herridge D F 1995 Field assessment of supernodulating genotypes of soybean for yield. N2 fixation and benefit to subsequent crops. Soil Biol. Biochem. 27, 563–569.Google Scholar
  79. Sprent J I 1994 Evolution and diversity in the legume-Rhizobium symbiosis: chaos theory? Plant and Soil 161, 1–10.Google Scholar
  80. Stacey G, Sanjuan S, Luka S, Dockendorff T and Carlson R W 1995 Signal exchange in the Bradyrhizobium-soybean symbiosis. Soil Biol. Biochem. 27, 473–483.Google Scholar
  81. Streeter J G 1994 Failure of inoculant rhizobia to overcome the dominance of indigenous strains for nodule formation. Can. J. Microbiol. 40, 513–522.Google Scholar
  82. Streeter J G and Salminen S O 1993 Distribution of the two types of polysaccharide formed by Bradyrhizobium japonicum bacteroids in nodules on field-grown soybean plants (Glycine max (L,.) Merr.) Soil Biol. Biochem. 25, 1027–1032.Google Scholar
  83. Streeter J G, Salminen S O, Whitmoyer R E and Carlson R W 1992 Formation of novel polysaccharides by Bradyrhizobium japonicum bacteroids in soybean nodules. Appl. Environ. Microbiol. 58, 607–613.Google Scholar
  84. Trese A T 1995 A single dominant gene in McCall soybean prevents effective nodulation with Rhizobium fredii USDA257. Euphytica 81, 279–282.Google Scholar
  85. Van Berkum P and Keyser H H 1985 Anaerobic growth and denitrification among different serogroups of soybean rhizobia. Appl. Environ. Microbiol. 49, 772–777.Google Scholar
  86. Vest G and Caldwell B E 1972 Rj4 a gene conditioning ineffective nodulation in soybeans. Crop Sci. 12, 692–694.Google Scholar
  87. Vest G, Weber D F and Sloger C 1973 Nodulation and nitrogen fixation. In Soybeans: Improvement, Production, and Uses. Ed. B E Caldwell. Agronomy 16, 363–390.Google Scholar
  88. Vuong T D, Nickell C D and Harper J E 1996 Genetic and allelism analyses of hypernodulating soybean (Glycine max (L.) Merr.) mutants from two genetic backgrounds. Crop Sci. (In press).Google Scholar
  89. Weber D F, Keyser H H and Uratsu S L 1989 Serological distribution of Bradyrhizobium japonicum from US soybean production areas. Agron. J. 81, 786–789.Google Scholar
  90. Wells S E and Kuykendall L D 1983 Tryptophan auxotrophs of Rhizobium japonicum. J. Bacteriol. 156, 1356–1358.Google Scholar
  91. Williams L F and Lynch D L 1954 Inheritance of a nonnodulating character in the soybean. Agron. J. 46, 28–29.Google Scholar
  92. Wilson A C, Ochman H and Prager E M 1987 Molecular time scale for evolution. Trends Genet. 3, 241–247.Google Scholar
  93. Young J P W, Downer H L and Eardly B D 1991 Phylogeny of the phototrophic Rhizobium strain BTAil by polymerase chain reaction-based sequencing of a 16S rRNA gene segment. J. Bacteriol. 173, 2271–2277.Google Scholar

Copyright information

© Kluwer Academic Publishers 1996

Authors and Affiliations

  • T. E. Devine
    • 1
    • 2
  • L. D. Kuykendall
    • 1
    • 2
  1. 1.Plant Molecular Biology LaboratoryUSDA, ARSBeltsvilleUSA
  2. 2.Soybean and Alfalfa Research LaboratoryUSDA, ARSBeltsvilleUSA

Personalised recommendations