Abstract
The importance of soybean as a source of oil and protein, and its ability to grow symbiotically on low-N soils, point to its continued status as the most valuable grain legume in the world. With limited new land on which to expand, and emphasis on sustainable systems, increases in soybean production will come mostly from increased yield per unit area. Improvements in biological nitrogen fixation can help achieve increased soybean production, and this chapter discusses research and production strategies for such improvement.
The soybean-Bradyrhizobium symbiosis can fix about 300 kg N ha-1 under good conditions. The factors which control the amount of N fixed include available soil N, genetic determinants of compatibility in both symbiotic partners and lack of other yield-limiting factors. Response to inoculation is controlled by the level of indigenous, competing bradyrhizobia, the N demand and yield potential of the host, and N availability in the soil.
Research efforts to improve BNF are being applied to both microbe and soybean. While selection continues for effective, naturally occurring bradyrhizobia for inoculants and the use of improved inoculation techniques, genetic research on bradyrhizobia to improve effectiveness and competitiveness is advancing. Selection, mutagenesis and breeding of the host have focused on supernodulation, restricted nodulation of indigenous B. japonicum, and promiscuous nodulation with strains of bradyrhizobia from the ‘cowpea’ cross-inoculation group. The research from the host side appears closer to being ready for practical use in the field.
Existing knowledge and technology still has much to offer in improving biological nitrogen fixation in soybean. The use of high-quality inoculants, and education about their benefits and use can still make a significant contribution in many countries. The importance of using the best adapted soybean genotype with a fully compatible inoculant cannot be overlooked, and we need to address other crop management factors which influence yield potential and N demand, indirectly influencing nitrogen fixation. The implementation of proven approaches for improving nitrogen fixation in existing soybean production demands equal attention as received by research endeavours to make future improvements.
Similar content being viewed by others
References
Abaidoo R C, George T, Bohlool B B and Singleton P W 1990 Influence of elevation and applied nitrogen on rhizosphere colonization and competition for nodule occupancy by different rhizobial strains on field-grown soybean and common bean. Can. J. Microbiol. 36, 93–96.
Al-Ithawi B, Deibert E J and Olson R A 1980 Applied N and moisture level effects on yield depth of root activity and nutrient uptake by soybeans. Agron. J. 72, 827–832.
Anonymous 1984 U. S. soybean production and utilization research. A report to the Senate Committee on Agriculture. Nutrition and Forestry and House Committee on Agriculture. Soybean Research Advisory Institute. Washington, DC. 69 p.
Amarger N 1981 Selection of Rhizobium strains on their competitive ability for nodulation. Soil Biol. Biochem. 13, 481–486.
Bergersen F S 1958 The bacterial component of soybean root nodule: Changes in respiratory activity, cell dry weight, and nucleic acid content with increasing nodule age. J. Gen. Microbiol. 19, 312–323.
Betts J H and Herridge D F 1987 Isolation of soybean lines capable of nodulation and nitrogen fixation under high levels of nitrate supply. Crop Sci. 27, 1156–1161.
Bezdicek D F, Evans D W, Adebe B and Witters R E 1978 Evaluation of peat and granular inoculum for soybean yield and N fixation under irrigation. Agron. J. 70, 865–868.
Boerma H R and Ashley D A 1988 Performance of three soybean mutants with increased nodulation. Agron. Abstracts. p 104.
Brevedan R E, Egli D B and Leggett J E 1978 Influence of N nutrition on flower and pod abortion and yield of soybeans. Agron. J. 70, 81–84.
Brockwell J, Diatloff A, Roughley R J and Date R A 1982 Selection of rhizobia for inoculants. In Nitrogen Fixation in Legumes. Ed. J M Vincent. pp 173–191. Academic Press, Sydney.
Bromfield E S P and Roughley R J 1980 Characterization of rhizobia isolated from nodules on locally-adapted Glycine max grown in Nigeria. Ann. Appl. Biol. 95, 185–190.
Burias N and Planchon C 1990 Increasing soybean productivity through selection for nitrogen fixation. Agron. J. 82, 1031–1034.
Burton J C 1980 Rhizobium inoculation and soybean production. In World Soybean Research Conference. part II: Proceedings. Ed. F T Corbin. pp 89–100. Westview Press, Boulder, CO.
Buttery B R and Dirks V A 1987 The effects of soybean cultivar, rhizobium strain and nitrate on plant growth, nodule mass and acetylene reduction rate. Plant and Soil 98, 285–293.
Caldwell B E 1966 Inheritance of a strain-specific ineffective nodulation in soybeans. Crop Sci. 6, 427–428.
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.
Carroll B J, Hartley R, Ashley D A, Boerma H R, Lawn R, Byth D and Greshoff P 1988 Field evaluation of supernodulating soybean mutants. In Nitrogen Fixation: Hundred Years After. Eds. H Bothe, F J de Bruijn and W E Newton. p 808. Gustav Fischer, Stuttgart, Germany.
Cassman K G, Whitney A S and Fox R L 1981 Phosphorus requirements of soybean and cowpea as affected by mode of N nutrition. Agron. J. 73, 17–22.
Cassman K C 1990 The role of soil fertility research in developing sustainable food production systems. Better Crops With Plant Food 74, 16–19.
Catlow H Y, Gleen A R and Dilworth M J 1990 Does rhizobial motility affect its ability to colonize along the legume root? Soil Biol. Biochem. 22 573–575.
Ciafardini G and Barbieri C 1987 Effects of cover inoculation of soybean on nodulation, nitrogen fixation, and yield. Agron. J. 79, 645–648.
Clark F E 1957 Nodulation responses of two near-isogenic lines of the soybean. Can J. Microbiol. 3, 113–123.
Cregan P B and Keyser H H 1986 Host restriction of nodulation by Bradyrhizobium japonicum strain USDA 123 in soybean. Crop Sci. 26, 911–916.
Cregan P B and Keyser H H 1988 Influence of Glycine spp. on competitiveness of Bradyrhizobium japonicum and Rhizobium fredii. Appl. Environ. Microbiol. 54, 803–808.
Cregan P B, Keyser H H and Sadowsky M J 1989a Soybean genotype restricting nodulation of a previously unrestricted serocluster 123 bradyrhizobia. Crop Sci. 29, 307–312.
Cregan P B, Leffel R C and A P Bolgiano 1989b Nitrogen metabolism of high and low seed protein soybean genotypes. Agron. Abstracts. p 110.
Danso S K A, Hera C and Douka C 1987 Nitrogen fixation in soybean as influenced by cultivar and Rhizobium strain. Plant and Soil 99, 163–174.
Danso S K A and Bowen G D 1989 Methods of inoculation and how they influence nodulation pattern and nitrogen fixation using two contrasting strains of Bradyrhizobium japonicum. Soil Biol. Biochem. 21, 1053–1058.
Dashiell K E, Kueneman E A, Root W R and Singh S R 1985 Breeding tropical soybean for superior seed longevity and for nodulation with indigenous rhizobia. In Soybean in Tropical and Subtropical Cropping Systems. Eds. S Shanmugasundaram and E W Sulzberger. pp 133–139. Asian Vegetable Research and Development Center, Shanhua, Taiwan.
Date R A 1976 Principles of Rhizobium strain selection. In Symbiotic Nitrogen Fixation in Plants, International Biological Programme 7. Ed. P S Nutman. pp 137–150. Cambridge University Press, Cambridge.
Devine T E and Weber D F 1977 Genetic specificity of nodulation. Euphytica 26, 527–535.
Devine T E 1984 Inheritance of soybean nodulation response with a fast-growing strain of rhizobia. J. Heredity 75, 359–361.
Dowling D N and Broughton W J 1986 Competition for nodulation of legumes. Annu. Rev. Microbiol. 40, 131–157.
Dreyfus B L, Diem H G and Dommergues Y R 1988 Future directions for biological nitrogen fixation research. Plant and Soil 108, 191–199.
Eaglesham A R J, Ayanaba A, Rao V and Eskew D L 1982 Mineral N effects on cowpea and soybean crop in a Nigerian Soil. II. Amount of N fixed and accrued in the soil. Plant and Soil 68, 183–192.
Eaglesham A R J, Hassouna S and Seeger R 1983 Fertilizer-N effects on N2 fixation by cowpea and soybean. Agron. J. 75, 61–66.
Eaglesham A R J 1985 Comparison of nodulation promiscuity of US- and Asian-type soya beans. Trop. Agric. (Trinidad) 62, 105–109.
Eaglesham A R J 1989a Global importance of Rhizobium as an inoculant. In Microbial Inoculation of Crop Plants. Eds. R Cambell and R M MacDonald. pp 29–48. Oxford University Press, Oxford.
Eaglesham A R J 1989b Nitrate inhibition of root-nodule symbiosis in doubly rooted soybean plants. Crop Sci. 29, 115–119.
Eisbreinner G and Evans H J 1983 Aspects of hydrogenase metabolism in nitrogen-fixing legumes and other plant-microbe associations. Annu. Rev. Plant Physiol. 34, 103–136.
Ellis W R, Ham G E and Schmidt E L 1984 Persistence and recovery of Rhizobium japonicum inoculum in a field soil. Agron. J. 76, 573–576.
Evans H J, Emerich D W, Ruiz-Argueso T, Maier R J and Albrecht S L 1980 Hydrogen metabolism in the legume-Rhizobium symbiosis. In Nitrogen Fixation, Vol. 2. Eds. W H Orme-Johnson and W ENewton. pp 67–86. University Park Press, Baltimore, MD.
Evans H J, Hanus F J, Haugland R A, Cantrell M A, Xu L, Russell S A, Lamber G A and Harker A R 1985 Hydrogen recycling in nodules affects nitrogen fixation and growth of soybeans. In World Soybean Research Conference III: Proceedings. Ed. R Schibles. pp 935–942. Westview Press Boulder, CO.
Fehr W R, Caviness C E, Burmood D T and Pennington J S 1971 Stages of development descriptions for soybean, Glycine max (L.) Merr. Crop Sci. 11, 929–930.
Fehr W R 1987 Breeding methods for cultivar development. In Soybeans: Improvement, Production and Uses, Second Edition. Ed. J R Wilcox. pp 249–293. American Society of Agronomy, Madison, WI.
Gao J, Wang Q, Hao Z, Zhang H, Zhao G, Zhang G, Wang X and Xue B 1987 Study on the symbiotic nitrogen fixation of soybean by 15N. Soybean Sci. 6, 55–61.
Ge C and Xu L 1982 Observation of the infection behaviour of indigenous Rhizobium japonicum and its distribution in different varieties of soybean in the fields. Chinese Oil Crops 3, 56–58 (In Chinese).
George T, Bohlool B B and Singleton P W 1987 Bradyrhizobium japonicum-environment interactions: Nodulation and interstrain competition in soils along an elevational transect. Appl. Environ. Microbiol. 53, 1113–1117.
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, 563–567.
Gibson A H and Harper J E 1985 Nitrate effect on nodulation of soybean by Bradyrhizobium japonicum. Crop Sci. 25, 497–501.
Greder R R, Orf J H and Lambert J W 1986 Heritabilities and associations of nodule mass and recovery of Bradyrhizobium japonicum serogroup USDA 110 in soybean. Crop Sci. 26, 33–37.
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.
Guffy R D, Heuvel R M V, Vasilas B L, Nelson R L, Frobish M A and Hesketh J D 1989 Evaluation of the N2 fixation capacity of four genotypes by several methods. Soil Biol. Biochem. 21, 339–342.
Ham G E 1976 Competition among strains of rhizobia. In World Soybean Research. Ed. L DHill. pp 144–150. Interstate Printers and Publishers, Danville, IL.
Ham G E 1980 Inoculation of legumes with Rhizobium in competition with naturalized strains. In Nitrogen Fixation, Vol. 2. Eds. W E Newton and W H Orme-Johnson. pp 131–138. University Park Press, Baltimore, MD.
Hardarson G, Golbs M and Danso S K A 1989 Nitrogen fixation in soybean (Glycine max L. Merrill) as affected by nodulation patterns. Soil Biol. Biochem. 21, 783–787.
Hardy R W F, Burns R C and Holsten R D 1973 Applications of the acetylen: ethylene assay for measurement of nitrogen fixation. Soil Biol. Biochem. 5, 47–81.
Hardy R W F and Havelka U D 1976 Phytosynthate as a major factor limiting nitrogen fixation by field-grown legumes with emphasis on soybean. In Symbiotic Nitrogen Fixation In Plants. Ed. P S Nutman. pp 421–439. Cambridge University Press, Cambridge.
Harper J E 1987 Nitrogen metabolism. In Soybeans: Improvement, Production, and Uses. 2nd edition. Ed. J R Wilcox. pp 497–533. Am. Soc. Agron., Madison, WI.
Havelka U D, Boyle M G and Hardy R W F 1982 Biological nitrogen fixation. In Nitrogen in Agricultural Soils. Ed. J Stevenson. pp 365–422. American Society of Agronomy, Madison, WI.
Hennecke H, Meyer L, Gottfert M and Fischer H 1988 Genetics of the Bradyrhizobium iaponicum-soybean symbiosis: Recent developments on genes for nodulation, bacteroid respiration, and regulation of nitrogen fixation. In Molecular Genetics of Plant-Microbe Interactions. Eds. R Palacios and D P S Verma. pp 118–123. American Phytopathological Society, St. Paul, MN.
Herridge D F and Holland J F 1987 Effects of tillage on plant available nitrogen and N2 fixation by soybean. In Nitrogen Cycling in Agricultural Systems of Temperate Australia. Eds. P E Bacon, J Evans, P R Storrier and A R Taylor. pp 390–396. Aust. Soc. Soil Sci. Inc., Wagga Wagga, Australia.
Herridge D F and Bergersen F J 1988 Symbiotic nitrogen fixation. In Advances in Nitrogen Cycling in Agricultural Ecosystems. Ed. J R Wilson. pp 46–65. C.A.B. International. Wallingford, UK.
Herridge D F, Betts J H and Rose I A 1988 Breeding for improved nodulation and nitrogen fixation by soybean. In Proc. 5th Austr. Soybean Research Workshop. pp 75–77. NSW Agriculture & Fisheries, Agricultural Research Centre, Tamworth, Australia.
Hinson K 1975 Nodulation responses from nitrogen applied to soybean half-root systems. Agron. J. 67, 799–804.
Hodgson A L M, Roberts W P and Waid J S 1985 Regulated nodulation of Trifolium subterraneum inoculated with bacteriocin producing strains of Rhizobium trifolii. Soil Biol. Biochem. 17, 475–478.
Hubbell D H 1988 Extension/transfer of BNF technology. In Nitrogen Fixation by Legumes in Mediterranean Agriculture. Eds. D P Beck and L A Materon. pp 367–370. Kluwer Academic Publishers, Dordrecht. The Netherlands.
Hume D J, Shanmugasundaram S and Beversdorf W D 1985 Soybean (Glycine max L. Merrill). In Grain Legume Crops. Eds. R J Summerfield and E H Roberts. pp 391–432. Collins Professional and Technical Books, London.
Hume D J and Shelp B J 1990 Superior performance of the Hup Bradyrhizobium japonicum strain 532C in Ontario soybean field trials. Can. J. Plant Sci. 70, 661–666.
Hymowitz T 1970 On the domestication of the soybean. Econ. Bot. 24, 408–421.
Imsande J 1986 Inhibition of nodule development in soybean by nitrate or reduced nitrogen. J. Exp. Bot. 37, 348–355.
Imsande J 1989 Rapid dinitrogen fixation during soybean pod fill enhances net photosynthetic output and seed yield: A new perspective. Agron. J. 81, 549–556.
Jackobs J A, Smyth C A and Erickson D 1985 International Soybean Variety Experiment. Tenth Report of Results 1983. INTSOY Series Number 16, Univ. of Illinois, Urbana-Champaign. 113 p.
Johnson H W and Clark F E 1958 Role of the root nodule in the bacterial-induced chlorosis of soybeans. Soil Sci. Soc. Am. Proc. 22, 527–528.
Johnston A W B, Downie J A, Rossed L, Shearman C A, Firmin J L, Borthakur D, Wood E A, Bradley D and Brewin N J 1987 Molecular analysis of the Rhizobium genes involved in the induction of nitrogen-fixing nodules on legumes. Phil. Trans. R. Soc. Lond. B317, 193–207.
Jones M B, Burton J C and Vaughn C E 1978 Role of inoculation in establishing subclover on California annual grasslands. Agron. J. 70, 1081–1085.
Judy W H and D KWhigham 1978 International Soybean Variety Experiment. Fourth Report of Results 1976. INTSOY Series Number 16, Univ. of Illinois, Urbana-Champaign. 401 p.
Kamicker B J and Brill W J 1987 Methods to alter the recovery and nodule location of Bradyrhizobium japonicum inoculant strains on field-grown soybeans. Appl. Environ. Microbiol. 53, 1737–1742.
Kapusta G and Rouwenhorst D L 1973 Influence of inoculum size on Rhizobium japonicum serogroup distribution frequency in soybean nodules. Agron. J. 65, 916–919.
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.
Kosslak R M and Bohlool B B 1984 Suppressions of nodule development of one side of a split-root system of soybeans caused by prior inoculation of the other side. Plant Physiol. 75, 125–130.
Kvien C S, Ham G E and Lambert J W 1981 Recovery of introduced Rhizobium japonicum strains by soybean genotypes. Agron. J. 73, 900–905.
LaFavre J S and Eaglesham A R J 1986 Rhizobitoxine: A phytotoxin of unknown function which is commonly produced by bradyrhizobia. Plant and Soil 92, 443–452.
Larson W E 1986 Presidential Address: The adequacy of world soil resources. Agron. J. 78, 221–225.
LaRue T A and Patterson T G 1981 How much nitrogen do legumes fix? Adv. Agron. 34, 15–38.
Latimore M J, Giddens J and Ashley D A 1977 Effect of ammonium and nitrate nitrogen upon photosynthate supply and nitrogen fixation by soybeans. Crop Sci. 17, 399–404.
Lawn R J and Burn W A 1974 Symbiotic nitrogen fixation in soybeans. I. Effect of photosynthetic source-sink manipulations. Crop Sci. 14, 11–16.
Lawn R J and Byth D E 1989 Saturated soil culture—a technology to expand the adaptation of soybean. In Proceedings World Soybean Res. Conf. IV. Ed. A J Pascale. pp 576–581. Asociación Argentina de la Soja, Buenos Aires, Argentina.
Leffel R C 1989 Breeding soybean for enhanced nitrogen metabolism. In Proceedings World Soybean Res. Conf. IV. Ed. A J Pascale. pp 1125–1130. Asociación Argentina de la Soja, Buenos Ahes, Argentina.
Li F, Chen H and Wang F 1986 Rhizobium numbers and their distribution in soil in relation to nodule occupancy. In Trans. 13th. Congr. ISSS, Vol. 2. pp 602–603.
Lim S T, Andersen K, Tait R and Valentine R C 1980 Genetic engineering in agriculture: Hydrogen uptake (hup) genes. Trends Biochem. Sci. 5, 167–170.
Maier R J and Brill W J 1978 Mutant strains of Rhizobium japonicum with increased ability to fix nitrogen for soybean. Science 201, 448–450.
Malik N S A, Calvert H E and Bauer W D 1987 Nitrate induced regulation of nodule formation in soybean. Plant Physiol. 84, 266–271.
McDermott T R and Graham P H 1989 Bradyrhizobium japonicum inoculant mobility, nodule occupancy, and acetylene reduction in the soybean root system. Appl. Environ. Microbiol. 55, 2493–2498.
Mellor H Y, Glenn A R, Arwas R and Dilworth M 1987 Symbiotic and competitive properties of motility mutants of Rhizobium trifolii TA1. Arch. Microbiol. 148, 34–39.
Mengel D B, Segars W, and Rehm G W 1987 Soil fertility and liming. In Soybeans: Improvement, Production and Uses. Second Edition. Ed. J R Wilcox. pp 461–496. American Society of Agronomy, Madison, WI.
Millhollon E P and Williams L E 1986 Carbohydrate partitioning and the capacity of apparent nitrogen fixation of soybean plants grown outdoor. Plant Physiol. 81, 280–284.
Moawad H A, Ellis W R and Schmidt E L 1984 Rhizosphere response as a factor in competition among three serogroups of indigenous Rhizobium japonicum for nodulation of field-grown soybeans. Appl. Environ. Microbiol. 47, 607–612.
Nangju D 1980 Soybean response to indigenous rhizobia as influenced by cultivar origin. Agron. J. 72, 403–406.
Nutman P S 1987 Centenary lecture. Phil. Trans. R. Soc. Lond. B317, 69–106.
Olsen S R 1982 Presidential Address: Removing barriers to crop productivity. Agron. J. 74, 1–4.
Paau A S 1989 Improvement of Rhizobium inoculants. Appl. Environ. Microbiol. 55, 762–865.
Pal U R 1989 Comparative contributions of native rhizobia vs. strains of Rhizobium japonicum to nitrogen uptake of promiscuous soybeans in Nigerian savanna. In Proceedings World Soybean Res. Conf. IV. Ed. A J Pascale. pp 494–499. Asociación Argentina de la Soja, Buenos Aires, Argentina.
Patterson T G and LaRue T A 1983 N2 fixation (C2H2) and ureide content of soybeans: Environmental effects and source-sink manipulations. Crop Sci. 23, 819–824.
Peoples M B, Faizah A W, Rerkasem B and Herridge D F 1989 Methods for Evaluating Nitrogen Fixation by Nodulated Legumes in the Field. Australian Centre for International Agricultural Research, Canberra. 76 p.
Phillips D A and DeJong T M 1984 Dinitrogen fixation in leguminous crop plants. In Nitrogen in Crop Production. Ed. R D Hauck. pp 121–132. American Society of Agronomy, Madison, WI.
Pulver E L, Brockman F and Wien H C 1982 Nodulation of soybean cultivars with Rhizobium spp. and their response to inoculation with R. japonicum. Crop Sci. 22, 1065–1070.
Pulver E L, Kueneman E A and Ranga-Rao V 1985 Identification of promiscuous nodulating soybean efficient in N2 fixation. Crop Sci. 25, 660–663.
Quispel A 1988 Hellriegel and Wilfarth's discovery of (symbiotic) nitrogen fixation hundred years ago. In Nitrogen Fixation: Hundred Years After. Eds. H Bothe F J de Bruijn and W E Newton. pp 3–12. Gustav Fisher, Stuttgart, Germany.
Rennie R J 1984 Comparisons of N balance and 15N isotope dilution to quantify N2 fixation in field-grown legumes. Agron. J. 76, 785–790.
Roughley R J 1976 The production of high quality inoculants and their contribution to legume yield. In Symbiotic Nitrogen Fixation in Plants, International Biological Programme 7. Ed. P S Nutman. pp 125–136. Cambridge University Press, Cambridge.
Roughley R J and Pulsford D J 1982 Production and control of legume inoculants. In Nitrogen Fixation in Legumes. Ed. J M Vincent. pp 193–209. Academic Press, Sydney.
Russell J S, Beech D F and Jones P N 1989 Grain legume productivity in subsistence agriculture. Food Policy May, 1989, 129–141.
Sadowsky M J, Tully R E, Cregan P B and Keyser H H 1987 Genetic diversity in Bradyrhizobium japonicum serogroup 123 and its relation to genotype-specific nodulation of soybean. Appl. Environ. Microbiol. 53, 2624–2630.
Schwinghamer E A and Brockwell J 1978 Competitive advantage of bacteriocin- and phage-producing strains of Rhizobium trifolii in mixed culture. Soil Biol. Biochem. 10, 383–387.
Scott W O and Aldrich S R 1983 Modern Soybean Production. S & A Publication, Champaign, IL. 209 p.
Scudder W T 1974 Rhizobium inoculation of soybeans for sub-tropical and tropical soils. I. Initial field trials. Soil Crop Sci. Soc. Fla. Proc. 34, 79–82.
Shanmugasundaram S 1989 Global cooperation for the improvement of soybean research and development. In Proceedings World Soybean Res. Conf. IV. Ed. A J Pascale. pp 1939–1947. Asociación Argentina de la Soja, Buenos Aires, Argentina.
Sinclair T R and Wit C Tde 1975 Photosynthate and nitrogen requirements for seed production by various crops. Science 189, 565–567.
Sinclair T R 1989 Simultaneous limitation to soybean yield increase by carbon and nitrogen. In Proceedings World Soybean Res. Conf. IV. Ed. A J Pascale. pp 183–188. Asociación Argentina de la Soja, Buenos Aires, Argentina.
Singleton P W and Stockinger K R 1983 Compensation against ineffective nodulation in soybean. Crop Sci. 23, 69–72.
Smith K J and Huyser W 1987 World distribution and significance of soybean. In Soybean: Improvement, Production and Use. 2nd edition. Ed. J R Wilcox. pp 1–22. Am. Soc. Agron., Madison, WI.
Sprent J I and Minchin F R 1983 Environmental factors on the physiology of nodulation and nitrogen fixation. In Temperate Legumes: Physiology, Genetics and Nodulation. Eds. D G Jones and D R Davies. pp 269–317. Pitman Advance Publishing Program, Boston.
Tang S 1979 Study on the nodulation and nitrogen fixation of soybean in lessive soils. Acta Pediologica Sinica 16, 9–16.
Thibodeau P S and Jaworski E G 1975 Patterns of nitrogen utilization in the soybean. Planta 127, 133–147.
Thies J E, Singleton P W and Bohlool B B 1991 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.
Thompson J A 1984 Production and Quality Control of Carrier-based Legume Inoculants. ICRISAT, Andhra Pradesh, India. 37 p.
Triplett E W 1990a Construction of a symbiotically effective strain of Rhizobium leguminosarum bv. trifolii with increased nodulation competitiveness. Appl. Environ. Microbiol. 56, 98–103.
Triplett E W 1990b The molecular genetics of nodulation competitiveness in Rhizobium and Bradyrhizobium. Molecular Plant-Microbe Interactions 3, 199–206.
Troedson R J 1988 Physiological aspects of the acclimation and growth of soybean (Glycine max (L.) Merrill) in saturated soil culture. PhD thesis, Univ. of Queensland.
Vance C P, Egli M A, Griffith S M and Miller S S 1988 Plant regulated aspects of nodulation and N2 fixation. Plant. Cell Environ. 11, 413–427.
Vest G 1970 Rj3—A gene conditioning ineffective nodulation in soybean. Crop Sci. 10, 34–35.
Vest G and Caldwell B E 1972 Rj4—A gene conditioning ineffective nodulation in soybean. Crop Sci. 12, 692–693.
Vest G, Weber D F and Sloger C 1973 Nodulation and nitrogen fixation. In Soybean: Improvement, Production, and Uses. Eds. B E Caldwell, R W Howell, R W Judd and H W Johnson. pp 353–390. American Society of Agronomy, Madison, WI.
Vincent J M 1980 Factors controlling the legume-Rhizobium symbiosis. In Nitrogen Fixation. Vol. 2. Eds. W E Newton and W H Orme-Johnson. pp 103–129. University Park Press, Baltimore, MD.
Wadisirisuk P, Danso S K A, Hardarson G and Bowen G D 1989 Influence of Bradyrhizobium japonicum location and movement on nodulation and nitrogen fixation in soybeans. Appl. Environ. Microbiol. 55, 1711–1716.
Weaver R W and Frederick L R 1974 Effect of inoculum rate on competitive nodulation of Glycine max L. Merrill. II Field studies. Agron. J. 66, 233–236.
Williams L E and Phillips D A 1983 Increased soybean productivity with a Rhizobium japonicum mutant. Crop Sci. 23, 246–250.
Williams L F and Lynch D L 1954 Inheritance of a nonnodulating character in the soybean. Agron. J. 46, 28–29.
Zapata F, Danso S K A, Hardarson G and Fried M 1987 Time course of nitrogen fixation in field-grown soybean using nitrogen-15 methodology. Agron. J. 79, 172–176.
Zhang H, Zhang G, Zhao G, Wang X, Xu B and Zhao F 1986 Nitrogenase activity, nodulation and the N2 fixation of the indigenous Rhizobium japonicum. Soybean Sci. 5, 47–56.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Keyser, H.H., Li, F. Potential for increasing biological nitrogen fixation in soybean. Plant Soil 141, 119–135 (1992). https://doi.org/10.1007/BF00011313
Issue Date:
DOI: https://doi.org/10.1007/BF00011313