Plant and Soil

, Volume 186, Issue 1, pp 151–159 | Cite as

Toward a new concept of the evolution of symbiotic nitrogen fixation in the Leguminosae

  • James A. Bryan
  • Graeme P. Berlyn
  • John C. Gordon


It is generally believed that only the nodulating species of the Leguminosae fix atmospheric nitrogen; however, anatomical, ecological and taxonomic considerations indicate that non-nodulating legume species may also fix nitrogen. To test whether nitrogen-fixing symbioses in the Leguminosae might extend to the non-nodulating species, a survey of the Leguminosae was conducted: living plants of non-nodulating species were assayed using acetylene reduction. Ethylene evolution, indicating apparent nitrogenase activity, was detected in non-nodulating species representing the major taxonomic groups of Caesalpinioideae as well as in non-nodulating species of the Papilionoideae and Mimosoideae. Non-nodules nitrogen fixation appears to have provided evolutionary precursors for the nodular symbiosis in the Leguminosae.

Key words

Caesalpinioideae nitrogenase activity nodulation root cortex taxonomy 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allen O N and Allen E K 1981 The Leguminosae: A Source Book of Characteristics, Uses, and Nodulation. Univ. Wisc. Press, Madison, WI, USA. 812 p.Google Scholar
  2. Barclay A S and Earle F R 1974 Chemical analysis of seeds III: Oil and protein content of 1253 species. Econ. Bot. 28, 178–236.Google Scholar
  3. Barnet Y M, Catt P C and Hearne D H 1985 Biological nitrogen fixation and root-nodule bacteria (Rhizobium sp. and Bradyrhizobium sp.) in two rehabilitating sand dune areas planted with Acacia spp. Aust. J. Bot. 33, 595–610.Google Scholar
  4. Bonnier C 1957 Symbiose Rhizobium-Légumineuses en Région Équatoriale. Publicatians de l'Institut National pour l'Étude Agronomique du Congo Belge. Séries Scientifique, No 72. 67 p.Google Scholar
  5. Bonnier C 1958 Discussion following Chapter 13 by G B Masefield, Some factors affecting nodulation in the tropics. In Nutrition of the Legumes. Ed. E G Hallsworth. p 212. Academic Press, New York, USA.Google Scholar
  6. Bower N, Hertel K, Oh J and Storey R 1988 Nutritional evaluation of marama bean (Tylosema esculentum, Fabaceae): Analysis of the seed. Econ. Bot. 42, 533–540.Google Scholar
  7. Bryan J A 1995 Leguminous trees with edible beans, with indications of a rhizobial symbiosis in non-nodulating legumes. Ph.D. thesis, Yale University, New Haven, Connecticut, USA. 310 p.Google Scholar
  8. Ding M, Yi Wei-min and Liao Lan-yu 1986 A survey on the N2-ase activities of nodules of tree legumes, including Tamarindus indica, a species not widely known to nodulate, in artificial forests in Dainbai, Guangdong, China. NFTRR 4, 9–10.Google Scholar
  9. Domingo I L 1983 Nitrogen fixation in Southeast Asian forestry: research and practice. In Biological Nitrogen Fixation in Forest Ecosystems: Foundations and Applications. Eds. J C Gordon and C T Wheeler. pp 295–315. Martinus Nijhoff/Dr W Junk Publishers, The Hague, the Netherlands.Google Scholar
  10. Doyle J J 1994 Phylogeny of the legume family: an approach to understanding the origins of nodulation. Annu. Rev. Ecol. Syst. 25, 325–349.Google Scholar
  11. Dreyfus B L and Dommergues Y R 1981 Nodulation of Acacia species by fast- and slow-growing tropical strains of Rhizobium. Appl. Environ. Microbiol. 41, 97–99.Google Scholar
  12. Earle F R and Jones Q 1962 Analyses of seed samples from 113 plant families. Econ. Bot. 16, 221–250.Google Scholar
  13. Faria S M de, Lewis G P, Sprent J I and Sutherland J M 1989 Occurrence of nodulation in the Leguminosae. New Phytol. 111, 607–619.Google Scholar
  14. Faria S M de, Cavalcante de Lima H, Carvalho A M, Conçalves V F and Sprent J I 1994 Occurrence of nodulation in legume species from Bahia, Minas Gerais and Espirito Santo states of Brazil. In Advances in Legume Systematics 5: The Nitrogen Factor. Eds. J I Sprent and D McKey. pp 17–23. Royal Botanic Gardens, Kew, UK.Google Scholar
  15. Faria S M de and Sprent J I 1994 Legume nodule development: an evolutionary hypothesis. In Advances in Legume Systematics 5: The Nitrogen Factor. Eds. J I Sprent and D McKey. pp 33–39. Royal Botanic Gardens, Kew, UK.Google Scholar
  16. Fehér D and Bolcor R 1926 Untersuchungen über die bakterielle Wurzelsymbiose einiger Leguminosenhölzer. Planta (Berlin) 2, 406–413.Google Scholar
  17. Felker P and Clark P R 1981 Nodulation and nitrogen fixation (acetylene reduction) in desert ironwood (Olneya tesota). Oecologia (Berlin) 48, 292–293.Google Scholar
  18. Fred E B, Baldwin I L and McCoy E 1932 Root Nodule Bacteria and Leguminous Plants. Univ. Wisc. Press, Madison, WI, USA. 343 p.Google Scholar
  19. Friesner G M 1926 Bacteria in the roots of Gleditsia triacanthos L. Proc. Indiana Acad. Sci. 34, 215–224.Google Scholar
  20. Hellriegel H and Wilfarth H 1888 Untersuchungen über die Stickstoffnahrung 071 der Gramineen und Leguminosen. Beilageheft zu der Zeitschrift des Vereins für die Rübenzücker-Industrie des deutschen Reiches. Kayssler and Co., Berlin, Germany.Google Scholar
  21. Jenkins M B, Virginia R A and Jarrell W M 1989 Ecology of fastgrowing and slow-growing mesquite-nodulating rhizobia in Chihuahuan and Sonoron desert ecosystems. Soil Sci. Soc. Am. J. 53, 543–549.Google Scholar
  22. Jones Q and Earle F R 1966 Chemical analyses of seeds II: Oil and protein content of 759 species. Econ. Bot. 20, 127–156.Google Scholar
  23. Lachmann J 1858 Über Knollen an den Wurzeln der Leguminosen. 071 Landwirthschaftliche Mitteilungen. Zeitschrift der Königlichen höheren landwirthschaftlichen Lehranstalt und der damit vereinigten landwirthschaftlichen Versuchsstation zu Poppelsdorf. Adolph Marcus, Bonn, Germany. pp 34–52.Google Scholar
  24. Lechtova-Trnka M 1931 Étude sur les bactéries des légumineuses et observations sur quelques champignons parasites des nodosités. Botaniste 23, 301–531.Google Scholar
  25. Leonard L T 19:25 Lack of nodule-formation in a subfamily of the Leguminuosae. Soil Sci. 20, 165–167.Google Scholar
  26. Lim G 1977 Nodulation of tropical legumes in Singapore. Trop. Agric. (Trinidad) 54, 135–141.Google Scholar
  27. Martínez-Romero E 1994 Recent developments in Rhizobium taxonomy. Plant and Soil 161, 11–20.Google Scholar
  28. McKey D 1994 Legumes and nitrogen: the evolutionary ecology of a nitrogen-demanding lifestyle. In Advances in Legume Systematics 5: The Nitrogen Factor. Eds. J I Sprent and D McKey. pp 211–228. Royal Botanic Gardens, Kew, UK.Google Scholar
  29. Moreira F M S and Franco A A 1994 Rhizobia-host interactions in tropical ecosystems in Brazil. In Advances in Legume Systematics 5: The Nitrogen Factor. Eds. J I Sprent and D McKey. pp 63–74. Royal Botanic Gardens, Kew, UK.Google Scholar
  30. Moreira F M S, Gillis M, Pot B, Kersters K and Franco A A 1993 Characterizatian of rhizobia isolated from different divergence groups of tropical Leguminosae by comparative polyacrylamide gel electrophoresis of their total proteins. Syst. Appl. Microbiol. 16, 135–146.Google Scholar
  31. Naisbitt T, James E K and Sprent J I 1992 The evolutionary significance of the legume genus Chamaecrista, as determined by nodule structure. New Phytol. 122, 437–492.Google Scholar
  32. Nobbe F, Schmid E, Hiltner L and Hotter E 1891 Versuche über die Stickstoff-Assimilation der Leguminosen. Landwirtsch. Vers. Stn. [Tharand] 39, 327–359.Google Scholar
  33. Polhill R M and Raven P H 1981 Advances in Legume Systematics. Royal Botanic Gardens, Kew, UK. 1049p.Google Scholar
  34. Polhill R M, Raven P H and Stirton C H 1981 Evolution and systematics of the Leguminosae. In Advances in Legume Systematics, Part 1. Eds. R M Polhill and P H Raven. pp 1–26. Royal Botanic Gardens, Kew, UK.Google Scholar
  35. Rothschild D I de 1967 Estudio preliminar sobre la presencia de bacterias en la raiz de Gleditsia amorphoides (Gris.) Taub. y G. triacanthos L. (Leguminosae). Comunicaciones del Museo Argentino de Ciencias Naturales “Bernardino Rivadivia” e Instituto Nacional de Investigacion de las Ciencias Naturales. Botánica 2, 9–14.Google Scholar
  36. Rothschild D I de 1970 Nodulación en leguminosas subtropicales de la flora Argentina. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadivia” e Instituto Nacional de Investigacion de las Ciencias Naturales. Botánica 3, 267–286.Google Scholar
  37. Sprent J I 1994 Evolution and diversity in the legume-rhizobium symbiosis: chaos theory? Plant and Soil 161, 1–10.Google Scholar
  38. Sutherland J M, McInroy S G, James E K and Naisbitt T 1994 Nodule structure with special reference to the tribes Sophoreae, Genisteae and Thermopsideae. In Advances in Legume Systematics 5: The Nitrogen Factor. Eds. J I Sprent and D McKey. pp 41–55. Royal Botanic Gardens, Kew, UK.Google Scholar
  39. Szott L T, Palm C A and Sanchez P A 1991 Agroforestry in acid soils of the humid tropics. Adv. Agron. 45, 275–301.Google Scholar
  40. Turk D and Keyser H H 1992 Rhizobia that nodulate tree legumes: specificity of the host for nodulation and effectiveness. Can. J. Microbiol. 38, 451–460.Google Scholar
  41. Turner G L and Gibson A H 1980 Measurement of nitrogen fixation by indirect means. In Methods for Evaluating Biological Nitrogen Fixation. Ed. F J Bergersen. pp 111–184. John Wiley and Sons, Ltd., New York, USA.Google Scholar
  42. Upchurch R G 1987 Estimation of bacterial nitrogen fixation using acetylene reduction. In Symbiotic Nitrogen Fixation Technology. Ed. G H Elkan pp 289–305. Marcel Dekker, Inc., New York, USA.Google Scholar
  43. Young J P W 1993 Molecular phylogeny of rhizobia and their relatives. In New Horizons in Nitrogen Fixation. Eds. R Palacios, J Mora and W W Newton. pp 587–592. Kluwer Academic Publishers, Dordrecht, the Netherlands.Google Scholar
  44. Young J P W and Johnston A W B 1989 The evolution of specificity in the legume-Rhizobium symbiosis. TREE 4, 341–349.Google Scholar
  45. Zhang X, Harper R, Karsisto M and Lindström K 1991 Diversity of Rhizobium bacteria isolated from the root nodules of leguminous trees. Int. J. Syst. Bacteriol. 41, 104–113.Google Scholar

Copyright information

© Kluwer Academic Publishers 1996

Authors and Affiliations

  • James A. Bryan
    • 1
  • Graeme P. Berlyn
    • 1
  • John C. Gordon
    • 1
  1. 1.School of Forestry and Environmental StudiesYale UniversityNew HavenUSA

Personalised recommendations