Plant and Soil

, Volume 141, Issue 1–2, pp 1–11 | Cite as

Biological nitrogen fixation for sustainable agriculture: A perspective

  • B. B. Bohlool
  • J. K. Ladha
  • D. P. Garrity
  • T. George


The economic and environmental costs of the heavy use of chemical N fertilizers in agriculture are a global concern. Sustainability considerations mandate that alternatives to N fertilizers must be urgently sought. Biological nitrogen fixation (BNF), a microbiological process which converts atmospheric nitrogen into a plant-usable form, offers this alternative. Nitrogen-fixing systems offer an economically attractive and ecologically sound means of reducing external inputs and improving internal resources. Symbiotic systems such as that of legumes and Rhizobium can be a major source of N in most cropping systems and that of Azolla and Anabaena can be of particular value to flooded rice crop. Nitrogen fixation by associative and free-living microorganisms can also be important. However, scientific and socio-cultural constraints limit the utilization of BNF systems in agriculture. While several environmental factors that affect BNF have been studied, uncertainties still remain on how organisms respond to a given situation. In the case of legumes, ecological models that predict the likelihood and the magnitude of response to rhizobial inoculation are now becoming available. Molecular biology has made it possible to introduce choice attributes into nitrogen-fixing organisms but limited knowledge on how they interact with the environment makes it difficult to tailor organisms to order. The difficulty in detecting introduced organisms in the field is still a major obstacle to assessing the success or failure of inoculation. Production-level problems and socio-cultural factors also limit the integration of BNF systems into actual farming situations. Maximum benefit can be realized only through analysis and resolution of major constraints to BNF performance in the field and adoption and use of the technology by farmers.

Key words

chemical fertilizer crop production developing countries environment inoculation legume pollution 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alexander M 1985 Ecological constraints on nitrogen fixation in agricultural ecosystems. Adv. Microb. Ecol. 8, 163–168.Google Scholar
  2. Almendras A S and Bottomley P J 1988 Cation and phosphate influences on the nodulating characteristics of indigenous serogroups of Rhizobium trifolii on soil grown Trifolium subteraneum L. Soil Biol. Biochem. 20, 345–352.Google Scholar
  3. Atkins C A 1986 The legume/Rhizobium symbiosis: Limitations to maximizing nitrogen fixation. Outl. Agric. 15, 128–134.Google Scholar
  4. Barker R and Chapman D 1988 The Economics of Sustainable Agricultural Systems in developing Countries. Mimeo, Cornell University, Ithaca, NY.Google Scholar
  5. Beck D P and Munns D N 1984 Phosphate nutrition of Rhizobium spp. Appl. Environ. Microbiol. 47, 278–282.Google Scholar
  6. Beck D P and Munns D N 1985 Effect of calcium on the phosphorus nutrition of Rhizobium meliloti. Soil. Sci. Soc. Am. J. 49, 334–337.Google Scholar
  7. Bohlool B B 1987 Fluorescence methods for study of Rhizobium in culture and in situ. In Symbiotic Nitrogen Fixation Technology. Ed. G H Elkan. pp. 127–147 Marcel Dekker, Inc. New York.Google Scholar
  8. Bohlool B B and Schmidt E L 1973 Persistence and competitive aspects of Rhizobium japonicum observed in soil by immunofluorescence microscopy. Soil Sci. Soc. Am. Proc. 37, 561–564.Google Scholar
  9. Bohlool B B and Schmidt E L 1980 The immunofluorescence approach in microbial ecology. In Advances in Ecology. Ed. M Alexander. pp203–235. Vol. 4. Plenum Press, New York, London.Google Scholar
  10. Bouldin D R 1986 The chemistry and biology of flooded soils in relation to the nitrogen economy in rice fields. In Nitrogen Economy of Flooded Rice Soils. Eds. S K DeDatta and W H Patrick pp1–14. Martinus Nijhoff Publishers. Dordrecht, The Netherlands.Google Scholar
  11. Byrlee D 1987 Mainmaining the momentum in post-green revolution agriculture: A micro-level perspective from Asia. MSU International Development Paper No. 10, Michigan State University, East Lansing, MI.Google Scholar
  12. Callaham D, DelTredici P and Torrey J G 1978 Isolation and cultivation in vitro of the actinomycete causing root nodulation in Comptonia. Science 199, 899–902.Google Scholar
  13. Cassman K G, Munns D N and Beck D P 1981 Growth of Rhizobium strains at low concentrations of phosphate. Soil Sci. Soc. Am. J. 45, 520–523.Google Scholar
  14. Danso S K A and Owiredu J D 1988 Competitiveness of introduced and indigenous cowpea Bradyrhizobium strains for nodule formation on cowpeas Vigna unguiculata (L.) (Walp.) in three soils. Soil Biol. Biochem. 20, 305–310.Google Scholar
  15. Danso S K, Bowen G D and Sanginga N 1992 Biological nitrogen fixation in trees in agroecosystems Plant and Soil 141, 177–196.Google Scholar
  16. Diem H G, Gauthier D and Dommergues Y R 1982 Isolation of Frankia from nodules of Casuarina equisetifolia. Can. J. Microbiol. 28, 526–530.Google Scholar
  17. Dowling D N and Broughton W J 1986 Competition for nodulation of legumes. Annu. Rev. Microbiol. 40, 131–157.Google Scholar
  18. Dunigan E P, Bollick P K, Huchinson R L, Hicks P M, Azubrecher F C, School S G and Mowers R P 1984 Introduction and survival of an inoculant strain of Rhizobium japonicum in soil. Agron. J. 76, 463–466.Google Scholar
  19. Ellis W R, Ham G E and Schmidt E L 1984 Persistence and recovery of Rhizobium japonicum in a field. Agron. J. 76, 573–576.Google Scholar
  20. Evans H J 1975 Enhancing Biological Nitrogen Fixation. National Science Foundation. Dir. Biological and Medical Sciences, Washington, DC 20550.Google Scholar
  21. Freire J R 1984 Important limiting factors in soil for the Rhizobium-legume symbiosis. In BNF Ecology, Technology and Physiology. Ed. M Alexander pp51–74. Plenum Press, New York, London.Google Scholar
  22. Fujita K, Ofosu-Budu K G and Ogata S 1992 Biological nitrogen fixation in mixed legume-cereal cropping systems. Plant and Soil 141, 155–176.Google Scholar
  23. Garrity D P 1990 Agronomic research on biofertilizers at IRRI: Overcoming systems-level constraints. In Proc. of the Nat. Symp. on Bio-and Organic Fertilizers. Univ. of the Philippines, Los Baños, Philippines. pp309–320.Google Scholar
  24. Garrity D P, Roberto T B, Crecensia C B, Pye Tin and Riaz M 1990 Indigofera tinctoria: Farmer-proven green manure for rainfed ricelands. In Proc. of the Nat. Symp. on Bio-and Organic Fertilizers. Univ. of the Philippines, Los Baños, Philippines. pp261–284.Google Scholar
  25. Gauthier D, Diem H G, Dommergues Y R and Ganry F 1985 Assessment of N2 fixation by Casuarina equisetifolia inoculated with Frankia ORS021001 using 15N methods. Soil Biol. Biochem. 17, 375–379.Google Scholar
  26. George T, Ladha J K, Buresh R J and Garrity D P 1992 Managing native and legume-fixed nitrogen in lowland rice-based cropping systems. Plant and Soil 141, 69–91.Google Scholar
  27. George T, Singleton P W and Bohlool B B 1988 Yield, soil nitrogen uptake, and nitrogen fixation by soybean from four maturity groups grown at three elevations. Agron. J. 80, 63–567.Google Scholar
  28. Gibson A H 1977 The influence of environmental and managerial practices in the legume-Rhizobium symbiosis. In A Treatise on Dinitrogen Fixation. Section IV: Agronomy and Ecology. Eds. R W FHardy and A H Gibson. pp 393–450. Wiley, New York.Google Scholar
  29. Helyar K R and Munns D N 1975 Phosphate fluxes in the soil-plant system. Hilgardia 43, 103–130.Google Scholar
  30. Holben W E, Jansson J K, Chelm B K and Tiedje J M 1988 DNA probe method for the detection of specific micro-organisms in the soil bacterial community. Appl. Environ. Microbiol. 54, 703–711.Google Scholar
  31. Ishizuka J 1992 Trends in biological nitrogen fixation research and application. Plant and Soil 141, 197–209.Google Scholar
  32. Kang B T 1990 Alley farming. Adv. Agron. 43, 315–359.Google Scholar
  33. Keeney D 1982 Nitrogen management for maximum efficiency and minimum pollution. In Nitrogen in Agricultural Soils. Ed. F J Stevenson. Agronomy Monograph 22, pp 605–649, ASA, Madison, WI.Google Scholar
  34. Keyser H H and Munns D N 1979 Effects of calcium, manganese, and aluminum on growth of rhizobia in acid media. Soil Sci. Soc. Am. J. 43, 500–503.Google Scholar
  35. Keyser H H and Li F 1992 Potential for increasing biological nitrogen fixation in soybean. Plant and Soil 141, 119–135.Google Scholar
  36. Khanna-Chopra R and Sinha R 1989 Impact of climate variation on production of pulses. In Climate and Food Security. pp219–236. The Int. Rice Research Inst., Los Baños, Philippines.Google Scholar
  37. King F H 1911 Farmers of Forty Centuries. Rodale Press, Inc., Emmaus, PA. 441 pGoogle Scholar
  38. Koyama T and App A 1979 Nitrogen balance in flooded rice soils. In Nitrogen and Rice, The Int. Rice Research Inst. pp95–104. Los Baños, Philippines.Google Scholar
  39. Ladha J K, Pareek R P and Becker M 1992 Stem-nodulating legume-Rhizobium-symbiosis and its agronomic use in lowland rice. Adv. Soil Sci. In press.Google Scholar
  40. Ladha J K, Pareek R P, So R and Becker M 1990 Stem nodule symbiosis and its unusual properties. In Nitrogen Fixation: Achievements and Objectives, Eds. P M Gresshoff, L E Roth, G Stacey and W L Newton pp633–640. Chapman and Hall, New York, London.Google Scholar
  41. Ledgard S F and Steele K W 1992 Biological nitrogen fixation in mixed legume/grass pastures. Plant and Soil 141, 137–153.Google Scholar
  42. Leung K and Bottomley P J 1987 Influence of phosphate on the growth and nodulation characteristics of Rhizobium trifolii. Appl. Environ. Microbiol. 53, 2098–2105.Google Scholar
  43. Lumpkin T A and Plucknett D L 1982 Azolla as a green manure: Use and management in crop production. Westview Tropical Agriculture Series No.5, Westview Press, Boulder. CO. 225 p.Google Scholar
  44. Munns D N 1977 Soil acidity and related matters. In Exploiting the Legume-Rhizobium Symbiosis in Tropical Agriculture. Eds. J M Vincent, A S Whitney and J Bose. pp 211–236. Univ. Hawaii Coll. Trop. Agr. Misc. Publ. 145.Google Scholar
  45. Munns D N and Franco A A 1982 Soil constraints to legume production. In Biological Nitrogen Fixation Technology for Tropical Agriculture. Eds. P H Graham and S C Harris. pp 133–152. CIAT Workshop 1981, Cali, Columbia.Google Scholar
  46. National Academy of Sciences 1979 Tropical Legumes: Resources for the Future. Washington, DC. 331 p.Google Scholar
  47. National Research Council (US) 1984 Casuarinas: Nitrogen-fixing Trees for Adverse Sites. National Academy Press, Washington, DC. 118 p.Google Scholar
  48. Odum E P 1989 Input management of production system. Science 243, 177–182.Google Scholar
  49. Peoples M B and Crasswell E T 1992 Biological nitrogen fixation: Investiments, expectations and actual contributions to agriculture. Plant and Soil 141, 13–39.Google Scholar
  50. Pingali P L, Moya P F and Velasco L E 1990 The post-green revolution blues in asian rice production—The diminished gap between experiment station and farmer yields. IRRI Social Science Division paper No 90–01.Google Scholar
  51. Plucknett D L and Smith N J H 1986 Sustaining agricultural yields. Bioscience 36, 40–45.Google Scholar
  52. Pradhan P 1988 The establishment requirements of Sesbania rostrata as a pre-rice green manure. M. Sc. Thesis. Univ. of the Philippines, Los Baños, Philippines. 189 p.Google Scholar
  53. Roger P A and Ladha J K 1992 Biological N2 fixation in wetland rice fields: Estimation and contribution to nitrogen balance. Plant and Soil 141, 41–55.Google Scholar
  54. Russell J P, Beech D F and Jone P N 1989 Grain legume productivity in subsistence agriculture. Food Policy 14, 129–142.Google Scholar
  55. Sanchez P A 1980 Management considerations for acid soils with high phosphorus fixation capacity. In The Role of Phosphorus in Agriculture. pp471–514. American Society of Agronomy. Madison, WI.Google Scholar
  56. Shanmugasundaram S 1988 Seed production and management of mungbean and soybean. In Sustainable Agriculture: Green Manure in Rice Farming. pp359–376. The Int. Rice Research Inst., Los Baños, Philippines.Google Scholar
  57. Singer M J and Munns D N 1987 Soils, an Introduction. Macmillan, New York 492 p.Google Scholar
  58. Singleton P W, Abdel-Magid H M and Tavares J W 1985 The effect of phosphorus on the effectiveness of strains of Rhizobium japonicum. Soil Sci. Soc. Am. J. 49, 613–616.Google Scholar
  59. Singleton P W and Bohlool B B 1983 Effect of salinity on the functional components of the soybean-Rhizobium japonicum symbiosis. Crop Sci. 23, 259–262.Google Scholar
  60. Singleton P W, Bohlool B B and Nakao P 1992 Legume response to rhizobial inoculation in the tropics: Myths and realities. In Myths and Science of the Soils of the Tropics. Eds. R Lal and P Sanchez. Soil Sci. Soc. Am. Spec. Publ. No. 29. Madison, WI. In press.Google Scholar
  61. Singleton P W and Tavares J W 1986 Inoculation response of legumes in relation to the number and effectiveness of indigenous Rhizobium populations. Appl. Environ. Microbiol. 51, 1013–1018.Google Scholar
  62. TAC CGIAR 1988 Sustainable agricultural production: Implications for international agricultural research. CGIAR (Consultative Group on International Agricultural Research) Meeting, Berlin, Germany.Google Scholar
  63. Thies J E, Singleton P W and Bohlool B B 1991a Influence of the size of indigenous rhizobial populations on establishment and symbiotic performance of introduced rhizobia on field-grown legumes. Appl. Environ. Microbiol. 57, 19–28.Google Scholar
  64. Thies J E, Singleton P W and Bohlool B B 1991b Modeling symbiotic performance of introduced rhizobia in the field by use of indices of indigenous population size and nitrogen status of the soil. Appl. Environ. Microbiol. 57, 29–37.Google Scholar
  65. Tiepkema J D, Schwintzer C R and Bensen D R 1986 Physiology of actinorhizal nodules. Annu. Rev. Plant Physiol. 36, 209–232.Google Scholar
  66. Torrey J G 1978 Nitrogen fixation by actinomycete-nodulated angiosperms. Bioscience 28, 586–592.Google Scholar
  67. Urquiaga S, Botteon P B L and Boddey R M 1989 Selection of sugarcane cultivars for associated biological nitrogen fixation using 15N labelled soil. In Nitrogen Fixation with Non-Legumes. Eds. F A Skinner R M Boddey and I Fendrik pp311–319. Kluwer Academic Publisher, Dordrecht, The Netherlands.Google Scholar
  68. Watanabe I and Liu C C 1992 Improving nitrogenfixing systems and integrating them into sustainable rice farming. Plant and Soil 141, 57–67.Google Scholar
  69. Weaver R W and Frederick L R 1974a Effect of inoculum rate on competitive nodulation of Glycine max L. Merrill. I. Greenhouse studies. Agron. J. 66, 229–232.Google Scholar
  70. Weaver R W and Frederick L R 1974b Effect of inoculum rate on competitive nodulation of Glycine max L. Merrill. II. Field studies. Agron. J. 66, 233–236.Google Scholar
  71. Weber D F and Miller V L 1972 Effect of soil temperature on Rhizobium japonicum serogroup distribution in soybean nodules. Agron. J. 64, 796–798.Google Scholar
  72. Willey R W 1979 Intercropping—its importance and research needs. Part 2: Agronomy and research approaches. Field Crops Abstr. 32, 73–85.Google Scholar

Copyright information

© Kluwer Academic Publishers 1992

Authors and Affiliations

  • B. B. Bohlool
    • 1
  • J. K. Ladha
    • 2
  • D. P. Garrity
    • 2
  • T. George
    • 1
  1. 1.Nif TAL ProjectUniversity of HawaiiPaiaUSA
  2. 2.International Rice Research Institute (IRRI)ManilaPhilippines

Personalised recommendations