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Biological nitrogen fixation in non-leguminous field crops: Recent advances

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Abstract

There is strong evidence that non-leguminous field crops sometimes benefit from associations with diazotrophs. Significantly, the potential benefit from N2 fixation is usually gained from spontaneous associations that can rarely be managed as part of agricultural practice. Particularly for dryland systems, these associations appear to be very unreliable as a means of raising the nitrogen status of plants. However, recent technical advances involving the induction of nodular structures on the roots of cereal crops, such as wheat and rice, offer the prospect that dependable symbioses with free-living diazotrophs, such as the azospirilla, or with rhizobia may eventually be achieved.

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References

  • Akao S, Nakata S and Yoneyama T 1991 Formation of nodules on non-nodulating soybean T201 after treatment with 2,4-dichlorophenoxyacetate. Plant and Soil 138, 207–212.

    Google Scholar 

  • Alexander D B and Zuberer D A 1989 Impact of soil environmental factors on rates of N2-fixation associated with roots of intact maize and sorghum plants. In Nitrogen Fixation with Non-Legumes. Eds. F A Skinner, R M Boddey and I Fendrik. pp 273–285. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  • Allen K A, Allen O N and Newman A S 1953 Pseudonodulation of leguminous plants induced by 2-bromo-3,5-dichlorobenzoic acid. Am. J. Bot. 40, 429–435.

    Google Scholar 

  • Al-Mallah MK, Davey MR and Cocking EC 1989 Formation of nodular structures on rice seedlings by rhizobia. J. Exp. Bot. 40, 473–478.

    Google Scholar 

  • Aloysius S K D and Paton A M 1984 Artificially induced symbiotic associations of L-form bacteria and plants. J. Appl. Bacteriol. 56, 465–477.

    Google Scholar 

  • App A A, Watanabe I, Alexander M, Ventura W, Daez C, Santiago T and DeDatta S K 1980 Nonsymbiotic nitrogen fixation associated with the rice plant in flooded soils. Soil Sci 130, 283–289.

    Google Scholar 

  • App A A, Santiago T, Daez C, Menguito C, Ventura W, Tirol A, Po J, Watanabe I, DeDatta S K and Roger P 1984 Estimation of the nitrogen balance for irrigated rice and the contribution of phototrophs. Field Crops Res 19, 17–27.

    Google Scholar 

  • Bani D C, Barberio M, Faviti F, Gallari E and Polsinelli M 1980 Isolation and characterization of glutamate synthetase mutants of Azospirillum brasilense. J. Gen. Microbiol. 118–9, 239–244.

    Google Scholar 

  • Barraquio W L, Ladha J K and Watanabe I 1983 Isolation and identification of N2-fixing Pseudomonas associated with wetland rice. Can. J. Microbiol. 29, 867–873.

    Google Scholar 

  • Bender G L, Goydych W, Rolfe B G and Nayudu M 1987 The role of Rhizobium conserved and host specific nodulation genes in the infection of the non-legume Parasponia andersonii Mol. Gen. Genet. 210, 299–306.

    Google Scholar 

  • Bender G L, Preston L, Barnard D and Rolfe B G 1990 Formation of nodule-like structures on the roots of the non-legumes rice and wheat. In Nitrogen Fixation: Achievements and Objectives. Eds. P M Gresshoff, L E Roth, G Stacey and W L Newton. Chapman and Hall, New York.

    Google Scholar 

  • Bergersen F J and Turner G L 1967 Nitrogen fixation by the bacteroid fraction of breis of soybean root nodules Biochim. Biophys. Acta 141, 507–520.

    Google Scholar 

  • Clara R W and Knowles R 1985 Superoxide dismutase, catalase and peroxidase in ammonium-grown and nitrogen-fixing Azospirillum brasilense. Can. J. Microbiol. 30, 1222–1228.

    Google Scholar 

  • Cocking E C, Al-Mallah M K, Benson E and Davey M R 1990 Nodulation of non-legumes by rhizobia. In Nitrogen Fixation: Achievements and Objectives. Eds. P M Gresshoff, L E Roth, G Stacey and W L Newton. Chapman and Hall, New York.

    Google Scholar 

  • Dart P J 1986 Nitrogen fixation associated with non-legumes in agriculture. Plant and Soil 90, 303–334.

    Google Scholar 

  • Dart P J 1986 Infection of legumes by Rhizobium. In Microbiology in Action. Eds. W G Murrell and I R Kennedy. pp 35–52, Research Studies Pres Wiley, Chichester, UK.

    Google Scholar 

  • Darvey N 1972 Ph.D. thesis (A cytogenetic study of wheat), The University of New South Wales, Sydney, Australia.

  • DeConinck K, Horemans S, Randombage S and Vlassak K 1989 Occurrence and survival of Azospirillum spp in temperate regions. In Nitrogen Fixation With Non-Legumes. Eds. F A Skinner, R M Boddey and I Fendrik, pp 109–114. Kluwer Academic Publishers. Dordrecht, The Netherlands.

    Google Scholar 

  • Diem H G and Dommergues G M 1979. Significance and improvement of rhizospheric nitrogen fixation. In Recent Advances in Biological Nitrogen Fixation. Ed. N S SubbaRao. pp 190–226, Oxford Publishing, New Delhi.

    Google Scholar 

  • Dilworth M J and Parker C A 1969 Development of the nitrogen-fixing system in legumes. J. Theor. Biol. 25, 208–218.

    Google Scholar 

  • Döbereiner 1974 Nitrogen fixing bacteria in the rhizosphere. In The Biology of Nitrogen Fixation. Ed. A Quispel. pp 86–120, North-Holland, Amsterdam.

    Google Scholar 

  • Döbereiner J 1983 Ten years Azospirillum. In Azospirillum. II. Genetics, Physiology and Ecology. Ed. W. Klingmuller. pp 9–23, Birkhauser-Verlag, Basel.

    Google Scholar 

  • Döbereiner J 1989 Isolation and identification of root associated diazotrophs In Nitrogen Fixation With Non-Legumes. Eds. F A Skinner, R M Boddey and I Fendrik. pp 103–108. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  • Dreyfus B, Elmerich C and Dommergues Y R 1983 Freeliving Rhizobium strains able to grow on N2 as the soil nitrogen source. Appl. Environ. Microbiol. 45, 711–713.

    Google Scholar 

  • Elmerich C 1984 Molecular biology and ecology of diazotrophs associated with non-leguminous plants. Bio. Technology 2, 967–978.

    Google Scholar 

  • Foard D E, Haber A H and Fishman T N 1965 Initiation of lateral root primordia without completion of mitosis and without cytokinesis in uniserate pericycle. Am. J. Bot. 52, 580–590.

    Google Scholar 

  • Fujii T, Huang Y-D, Higashitani A, Nishimura Y, Iyama S, Hirota Y, Yoneyama T and Dixon R A 1987 Effect of inoculation with Klebsiella oxytoca and Enterobacter cloacae on dinitrogen fixation by rice-bacteria associations. Plant and Soil 103, 221–226.

    Google Scholar 

  • Gallani E and Bazzicapulo 1985 Effect of nitrogen compounds on nitrogenase activity in Azospirillum brasilense. FEMS Microbiol. Lett. 28, 35–38.

    Google Scholar 

  • Gauthier D and Elmerich C 1977 Relationship between glutamine synthetase and nitrogenase in Spirillum lipoferum. FEMS Microbiol. Lett. 2, 101–104.

    Google Scholar 

  • Gibson A H 1966 The carbohydrate requirements for symbiotic nitrogen fixation; A ‘whole plant’ growth analysis approach. Aust. J. Biol. Sci. 19, 499–515.

    Google Scholar 

  • Giles K L and Whitehead H C M 1977 Re-association of a modified mycorrhiza with the host plant roots (Pinus radiata) and the transfer of acetylene reduction activity. Plant and Soil 48, 143–152.

    Google Scholar 

  • Haack A 1961 Über den Ursprung der Wurzelknöllchen von Ornithopus sativus L. und Lupinus albus L. Z. Bakteriol. 114, 575–589.

    Google Scholar 

  • Harari A, Kigel J and Okon Y 1989 Involvement of IAA in the interactions between Azospirillum brasilense and Panicum miliaceum In Nitrogen Fixation With Non-Legumes. Eds. F A Skinner, R M Boddey and I Fendrik. pp 227–234. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  • Hartmann A 1989 Ecophysiological aspects of growth and nitrogen fixation in Azospirillum spp. In Nitrogen Fixation With Non-Legumes. Eds. F A Skinner, R M Boddey and I Fendrik. pp 123–136. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  • Hartmann A, Fu H, Song S-D and Burris R H 1985 Comparison of nitrogenase regulation in A. brasilense, A. lipoferum and A. amazonense. In Azospirillum III: Genetics, Physiology, Ecology. Ed. W Klingmüller. pp 116–126, Springer-Verlag, Berlin.

    Google Scholar 

  • Hartmann A, Fu H and Burris R H 1986 Regulation of nitrogenase activity by ammonium chloride. J. Bacteriol. 165, 864–870.

    Google Scholar 

  • Hartmann A and Burris R H 1987 Regulation of nitrogenase activity by oxygen in Azospirillum brasilense and Azospirillum lipoferum. J. Bacteriol. 169, 944–948.

    Google Scholar 

  • Hegazi N A and Saleh H 1985 Possible contribution of Azospirillum spp. to the nutritional status of wheat plants grown in sandy soil. In Azospirillum. III. Genetics, Physiology, Ecology. Ed. W Klingmüller. pp 189–202. Springer-Verlag, Berlin.

    Google Scholar 

  • Hurek T, Reinhold B and Niemann E-G 1987 Effect of oxygen on NH4 +-grown continuous cultures of Azospirillum spp. and diazotrophic rods closely associated with Kallar grass. Can. J. Microbiol. 33, 919–922.

    Google Scholar 

  • Jackson R B 1985 Pesticide residues in soils. In Soils: An Australian Viewpoint. CSIRO publication, Division of Soils. pp 825–842. Canberra, Australia.

    Google Scholar 

  • Jagnow G 1990 Differences between cereal crop cultivars in root-associated nitrogen fixation, possible causes of variable yield responses to seed inoculation. Plant and Soil 123, 255–259.

    Google Scholar 

  • Jing Y, Zhang B T and Shan X Q 1990a Pseudonodules formation on barley roots induced by Rhizobium astragali. FEMS Microbiol. Lett. 69, 123–127.

    Google Scholar 

  • Jing Y X, Li G S, Shan X Q and Li J G 1990b Rice root nodules with nitrogenase and hemoglobin. Proc. Int. Symp. Nitrogen Fixation, H16. Knoxville, TN.

  • Kanemoto R H and Ludden P W 1984 Effect of ammonia, darkness and phenazine methosulfate on whole-cell nitrogenase activity and Fe protein modification in Rhodospirillum rubrum. J. Bacteriol. 158, 713–720.

    Google Scholar 

  • Kapulnik Y, Sarig S, Nur I and Okon Y 1983 Effect of Azospirillum inoculum on yield of field-grown wheat. Can. J. Microbiol. 29, 895–899.

    Google Scholar 

  • Kennedy I R 1979 Integration of nitrogenase in cellular metabolism. In A Treatise of Dinitrogen Fixation: Inorganic and Physical Chemistry and Biochemistry. Eds. R W F Hardy, R Bottomley and R C Burns. pp 653–90. Wiley, New York.

    Google Scholar 

  • Kennedy I R 1983 Action and entropy in a neurological disorder. In Molecular Aspects of Neurological Disorders. Eds. P L Jeffrey and L Austin. pp 147–50. Academic Press, Sydney.

    Google Scholar 

  • Kennedy I R 1986a Acid Soil and Acid Rain, Research Studies Press/Wiley, Chichester, UK.

    Google Scholar 

  • Kennedy I R 1986b Relative energy costs of dinitrogen and nitrate assimilation: Influence on cytoplasmic acidity. 8th Aust. Nitrogen Fixation Conf., Eds. W Wallace and S E Smith, AIAS Occasional Publn. 25, 121–122.

  • Kennedy IR 1988 The molecular basis of symbiotic nitrogen fixation. In Microbiology in Action. Eds. W G Murrell and I R Kennedy. pp 143–155. Research Studies Press/Wiley, Chichester, UK.

    Google Scholar 

  • Kennedy I R 1991 Acid Soil and Acid Rain. Research Studies Press/Wiley, Chichester, UK. 2nd edn. In press.

    Google Scholar 

  • Kennedy I R, Zeman A, Tchan Y T, New P B, Sriskandarajah S and Nie Y F 1990 Biological nitrogen fixation and prospects for yield increases in wheat. Trans. 14th Int. Contr. Soil Sci. III, 146–151.

    Google Scholar 

  • Kennedy I R, Sriskandarajah S, Yu D, Nie Y F and Tchan Y T 1991 C2H2 reducing para-nodules in wheat: Effects of growth regulators and colchicine. Proc. 9th Aust. Nitrogen Fixn. Conf. 9, 78–79.

    Google Scholar 

  • Kirkham M B 1990 Transit time for oxygen flow along streamlines in vertical and horizontal tillage: A model study. Trans. 14th Int. Congr. Soil Sci. I, 298–301.

    Google Scholar 

  • Kostychev S, Sheloumova A and Shul'gina 1926 Nitrogen content of soils of the southern coast of Crimea (Russian). Sonetskii Agron. 1, 1926.

    Google Scholar 

  • Ladha J K, Tirol A C, Laroy L G, Caldo G, Ventura W and Watanabe I 1986 N2 fixation (C2H2 reduction) by five rice varieties, and relationship with plant growth characters as affected by straw incorporation. Soil Sci. Plant Nutr. 32, 91–106.

    Google Scholar 

  • Ladha J K, Tirol-Padre A, Punzulan G C and Watanabe I 1987 Nitrogen-fixing (C2H2-reducing) activity and plant growth characters of 16 wetland rice varieties. Soil Sci. Plant Nutr. 33, 187–200.

    Google Scholar 

  • Ladha J K, Garcia M, Miyan S, Padre A T and Watanabe I 1989 Survival of Azorhizobium caulinodans in the soil and rhizosphere of wetland rice under Sesbania rostrata-rice rotation. Appl. Environ. Microbiol. 55, 454–460.

    Google Scholar 

  • Ladha J K, Pareek R P, So R and Becker M 1990 Stem nodules symbiosis and its unusual properties. In Nitrogen Fixation: Achievements and Objectives. Eds. P M Gresshoff, L E Roth, G Stacy and W L Newton. Chapman and Hall, New York.

    Google Scholar 

  • Li R P and MacRae I C 1991 Nitrogen fixing bacteria associated with sugarcane in Queensland. Proc. 9th Aust. Nitrogen Fixation Conf. 9, 9–10.

    Google Scholar 

  • Libbenga K R and Bogers R J 1974 Root-nodule morphogenesis. In The Biology of Nitrogen Fixation. Ed. A Quispel. pp 430–472. North-Holland, Amsterdam.

    Google Scholar 

  • Mertens T and Hess D 1984 Yield increases in spring wheat (Triticum aestivum L.) inoculated with Azospirillum lipoferum under greenhouse and field conditions of a temperate region. Plant and Soil 82, 87–99.

    Google Scholar 

  • Millbank J W 1974 Associations with blue-gree algae. In The Biology of Nitrogen Fixation. Ed. A Quispel. pp 238–264. North-Holland, Amsterdam.

    Google Scholar 

  • Millet E and Feldman M 1984 Yield response of a common spring wheat cultivar to inoculation with Azospirillum brasilense at various levels of nitrogen fertilization. Plant and Soil 80, 255–259.

    Google Scholar 

  • Millet E, Longeri L and Arbarzua M 1989 Ultrastructure of Frankia isolated from three Chilean shrubs (Rhamnaceae). In Nitrogen Fixation With Non-Legumes. Eds. F A Skinner, R M Boddey and I Fendrik. pp 47–56. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  • Mishustin E N and Shil'Nikova V K 1971 Biological Fixation of Atmospheric Nitrogen. MacMillan, London.

    Google Scholar 

  • Mulder E G and Brotonegoro S 1974 Free-living heterotrophic nitrogen-fixing bacteria. In The Biology of Nitrogen Fixation. Ed. A Quispel. pp 37–85. North-Holland Amsterdam.

    Google Scholar 

  • New P B and Kennedy I R 1989 Regional distribution and pH sensitivity of Azospirillum associated with wheat roots in eastern Australia. Microbial Ecol. 17, 299–309.

    Google Scholar 

  • New P B, Sukiman H I and Kennedy I R 1991 Host plant-bacterial strain specificity in Azospirillum. Proc. 9th Aust. Nitrogen Fixation Conf. 9, 76–77.

    Google Scholar 

  • Nye P H and Tinker P B 1977 Solute Movement in the Soil-root system. p 207. Blackwell, Oxford.

    Google Scholar 

  • Okon Y, Kapulnik Y and Sarig S 1988 Field inoculation studies with Azospirillum in Israel. In Biological Nitrogen Fixation. Ed. N S SubbaRao. pp 175–196. Oxford and IBH Publishing, New Delhi.

    Google Scholar 

  • Pacovsky R S 1989 Influence of inoculation with Azospirillum brasilense and Glomus fasciculatum on sorghum nutrition. In Nitrogen Fixation With Non-Legumes. Eds. F A Skinner, R M Boddey and I Fendrik. pp 235–240. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  • Pedrosa F O, DeSouza E M, Machado H B, Rigo L U and Funayama S (1989) Regulation of nif genes expression in Azospirillum brasilense and Herbaspirillum seropedicae. In Nitrogen Fixation With Non-Legumes. Eds. F A Skinner, R M Boddey and I Fendrik. pp 155–163. Kluwer Academic Publishers. Dordrecht, the Netherlands.

    Google Scholar 

  • Pereira J A R, Cavalcante V A, Baldini V I and Döbereiner J 1989 Field inoculation of sorghum and rice with Azospirillum spp. and Herbaspirillum seropedicae In Nitrogen Fixation With Non-legumes. Eds. F A Skinner, R M Boddey and I Fendrik. pp 219–226. Kluwer Academic Publishers. Dordrecht, The Netherlands.

    Google Scholar 

  • Piana L, Delledone M, Antonelli M N and Fogher C 1988 Root hair deformation induced on maize and medicago by an Azospirillum transconjugant containing a Rhizobium meliloti nodulation region. In Azospirillum IV. Genetics. Physiology, Ecology. Ed. W Klingmüller. pp 83–91. Springer Verlag, Berlin.

    Google Scholar 

  • Plazinski J, Innes R W and Rolfe B G 1985 Expression of Rhizobium trifolii early nodulation genes on maize and rice plants. J. Bacteriol. 163, 812–815.

    Google Scholar 

  • Postgate J 1972 Biological Nitrogen Fixation. Merrow Publn. Co. Watford.

    Google Scholar 

  • Postgate J R 1974 Prerequisites for biological nitrogen fixation in free-living heterotrophic bacteria. In The Biology of Nitrogen Fixation. Ed. A Quispel. pp 663–686. North-Holland. Amsterdam.

    Google Scholar 

  • Quispel A 1974 The endophytes of the root nodules in non-leguminous plants. In The Biology of Nitrogen Fixation. Ed. A Quispel. pp 499–520. North-Holland Amsterdam.

    Google Scholar 

  • Rai S N and Gaur A C 1982 Nitrogen fixation by Azospirillum spp. and effect of Azospirillum lipoferum on the yield and N-uptake of wheat crop. Plant and Soil 69, 233–238.

    Google Scholar 

  • Ravishankar H N, Kennedy I R and New P B 1986 Autotrophic growth and nitrogen fixation in Derxia gummosa. J. Gen. Microbiol. 132, 1797–1803.

    Google Scholar 

  • Reinhold B and Hurek T 1989 Location of diazotrophs in the root interior with special attention to the kallar grass association. In Nitrogen Fixation With Non-Legumes. Eds. F A Skinner, R M Boddey and I Fendrik. pp 199–208. Kluwer Academic Publishers. Dordrecht, The Netherlands.

    Google Scholar 

  • Rodriquez-Barrueco C, Sevillano F and Nebrada T M 1989 Effective nodulation of Coriaria myrtifolia L. induced by Frankia strains from Alnus glutinosa. In Nitrogen Fixation With Non-Legumes. Eds. F A Skinner, R M Boddey and I Fendrik. pp 15–24. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  • Roger P A and Ladha J K 1990 Estimation of biological N2 fixation and its contibution to nitrogen balance in wetland rice field. Trans. 14th Int. Congr. Soil Sci. III, 128–133.

    Google Scholar 

  • Rolfe B G and Bender G L 1990 Evolving a Rhizobium for non-legume nodulation. In Nitrogen Fixation: Achievements and Objectives. Eds. P M Gresshoff, L E Roth, G Stacey and W L Newton. Chapman and Hall, New York.

    Google Scholar 

  • Roughley R J 1988 Principles of inoculant strain selection, inoculant production and quality control. In Microbiology in Action. Eds. W J Murrell and I R Kennedy. pp 53–66. Research Studies Press/Wiley, Chichester, UK.

    Google Scholar 

  • Schubert K R 1982 The energetics of biological nitrogen fixation, Workshop Summaries, I, 1, Am. Soc. Plant Physiol. pp 4–20.

  • Schubert K R 1986 Products of biological nitrogen fixation in higher plants: Synthesis, transport and metabolism. Annu. Rev. Plant Physiol. 37, 539–556.

    Google Scholar 

  • Silsbury J H 1977 Energy requirement for symbiotic nitrogen fixation. Nature, London 267, 149–150.

    Google Scholar 

  • Skinner F A, Boddey R M and Fendrik I (Eds.) 1989 Nitrogen Fixation with Non-Legumes. Kluwer Academic Publishers. Dordrecht, The Netherlands.

    Google Scholar 

  • Smith R L, Bouton J H, Schank S C, Quesenberry K H, Tyler M E, Milam J R, Gaskins M H and Litell R C 1976 Nitrogen fixation in grasses inoculated with Spirillum lipoferum. Science 193, 1003–1005.

    Google Scholar 

  • Smith R L, Schank S C, Bouton J H and Quesenberry K H 1978 Yield increases of tropical grasses after inoculation with Spirillum lipoferum. Ecol. Bull. Stockholm 26, 380–35.

    Google Scholar 

  • Smith R L, Schank S C, Milam J R and Baltensperger A 1984 Response of Sorghum and Pennisetum species to the N2-fixing bacterium Azospirillum brasilense. Appl. Environ. Microbiol. 47, 1331–1336.

    Google Scholar 

  • Sprent J and deFaria M 1989 Mechanisms of infection of plants by nitrogen fixing organisms In Nitrogen Fixation With Non-Legumes. Eds. F A Skinner, R M Boddey and I Fendrik. pp 3–14. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  • Tchan Y T 1988 Some aspects of non-rhizobial diazotrophs: their past and their future. In Microbiology in Action. Eds. W G Murrell and I R Kennedy. pp 193–207. Research Studies Press/Wiley, Chichester, UK.

    Google Scholar 

  • Tchan Y T and Kennedy I R 1988 Asymbiotic nitrogen fixation. In Nitrogen Cycling in Temperate Agricultural Systems. Eds. P E Bacon, J Evans, R R Storrier and A C Taylor. pp 120–142. Riverina Branch: Australian Society of Soil Science.

  • Tchan Y T and Kennedy I R 1989 Possible N2-fixing root nodules induced in non-legumes. Agric. Sci. (AIAS, Melbourne) 2, 57–59.

    Google Scholar 

  • Tchan Y T, Zeman A and Kennedy I R 1991 Nitrogen fixation in para-nodules of wheat roots by introduced free-living diazotrophs. Plant and Soil 137, 43–47.

    Google Scholar 

  • Terzachi B E and Christensen M J 1986 Should the transfer of nitrogen-fixing ability to an eukaryotic cell be reconsidered? J. Plant Physiol. 122, 275–283.

    Google Scholar 

  • Tien T M, Gaskins M H, and Hubbell D H 1979 Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.). Appl. Environ. Microbiol. 37, 1016–1024.

    Google Scholar 

  • Trinick M J 1973 Symbiosis between Rhizobium and the non-legume Trema aspera. Nature, London 144, 459.

    Google Scholar 

  • Trinick M J 1988 Bradyrhizobium of the non-legume Parasponia. In Microbiology in Action. Eds. W G Murrell and I R Kennedy. pp 107–118. Research Studies Press/Wiley, Chichester, UK.

    Google Scholar 

  • Urquiaga S, Botteon P B L and Boddey R M 1989 Selection of sugarcane cultures for associated biological nitrogen fixation using 15N soil. In Nitrogen Fixation with Non-legumes. Eds. F A Skinner, R M Boddey and I. Fendrik pp 311–319. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  • Vieille C and Elmerich C 1990 Characterization of two Azospirillum brasilense Sp7 plasmid genes homologous to Rhizobium meliloti Nodpq. Mol. Plant-Microbe Inter. 3, 389–400.

    Google Scholar 

  • Vincent J M 1980 Factors controlling the legume-Rhizobium symbiosis. In Nitrogen Fixation, Volume II. Eds. W E Newton and W H Orme-Johnson. pp 103–129. University Park Press, Baltimore, MD.

    Google Scholar 

  • Vincent J M 1984 Potential for enhancing biological nitrogen fixation. In Crop Breeding: A Contemporay Basis. Eds. P B Jose and S C Blixt. pp 185–215. Pergamon Press, Oxford.

    Google Scholar 

  • Volpon A G T, De-Polli H and Podenier J 1981 Physiology of nitrogen fixation in Azospirillum lipoferum BR17. Arch. Microbiol. 128, 371–375.

    Google Scholar 

  • Wani S P, Chandrapalaiah, Zanbre M A, and Lee K K 1989 Association between N2-fixing bacteria and pearl millet plants: Responses, mechanisms and persistence. In Nitrogen Fixation with Non-Legumes. Eds. F A Skinner, R M Boddey and I Fendrik. pp 249–262. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  • Watanabe I, Yoneyama T, Padre B and Ladha J K 1987a Difference in natural abundance of 15N in several rice (Oryza sativa L.) varieties: Application for evaluating N2 fixation. Soil Sci. Plant Nutr. 33, 407–415.

    Google Scholar 

  • Watanabe I, So R, Ladha J K, Katayama-Fujimura Y and Kuraishi H 1987b A new nitrogen-fixing species of pseudomonad: Pseudomonas diazotrophicus sp. nov. isolated from the root of wetland rice. Can. J. Microbiol. 33, 670–678.

    Google Scholar 

  • Whipps J M and Lynch J M 1983 Substrate flow and utilization in the rhizosphere of cereals. New Phytol. 95, 605–623.

    Google Scholar 

  • Wilde M H 1951 Anatomical modifications of bean roots following treatment with 2,4-D. Am. J. Bot. 38, 79–91.

    Google Scholar 

  • Yoo I D, Fujii T, Sano Y, Komagata K, Yoneyama T, Iyama S and Hirota Y 1986 Dinitrogen fixation of rice-Klebsiella associations. Crop Sci. 26, 297–301.

    Google Scholar 

  • You C and Zhou F 19, 89 Non-nodular endorhizospheric nitrogen fixation in wetland rice. Can. J. Microbiol. 35, 403–408.

    Google Scholar 

  • Yu D G 1988 Studies on 2,4-D induction of wheat nodules and the introduction of Rhizobium into nodules. M.Sc. thesis supervised by T W Chen (CAAS, Beijing).

  • Zeman A, Tchan Y T and Kennedy I R 1991 The para-nodule on wheat as a model of a N2-fixing symbiosis on a non-legume. Proc. 9th Aust. Nitrogen Fixation Conf. 9, 80–81.

    Google Scholar 

  • Zhu Z 1989 Dynamics of soil nitrogen and its management. In Progress in Irrigated Rice Research. pp 151–164. International Rice Research Conf., IRRI, Manila.

  • Zimmer W and Bothe H 1989 The phytohormonal interactions between Azospirillum and wheat. In Nitrogen Fixation With Non-Legumes. Eds. F A Skinner, R M Boddey and I Fendrik. pp 137–146. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

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Kennedy, I.R., Tchan, YT. Biological nitrogen fixation in non-leguminous field crops: Recent advances. Plant Soil 141, 93–118 (1992). https://doi.org/10.1007/BF00011312

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