Plant and Soil

, Volume 108, Issue 1, pp 93–110 | Cite as

Mineral constraints to nitrogen fixation

  • Graham W. O'hara
  • Nantakorn Boonkerd
  • Michael J. Dilworth


Mineral nturient defiencies are a major constraint limiting legume nitrogen fixation and yield. In this review general techniques for assessing nutrient involvement in symbiotic nitrogen fixation are described and specific methods are outlined for determining which developmental phase of the symbiosis is most sensitive to nutrient deficiency.

The mineral nutrition of the Rhizobium component of the symbiosis is considered both as the free living organism in the soil and as bacteroids in root nodules. Rhizobial growth and survival in soils is not usually limited by nutrient availability. Multiplication of rhizobia in the legume rhizosphere is limited by low Ca availability. Nodule initiation is affected by severe Co deficiency through effects on rhizobia. Nodule development is limited by severe B deficiency via an effect on plant cell growth. Fe deficiency limits nodule development by affecting rhizobia and strains of rhizobia differ widely in their ability to acquire sufficient Fe for their symbiotic development. Nodule function requires more Mo than does the host plant, and in some symbioses nitrogen fixation may be specifically limited by low availability of Ca, Co, Cu and Fe. The importance of the peribacteriod membrane in determining nutrient availability to bacteroids is considered.

It is concluded that the whole legume-Rhizobium symbiosis should be considered when improving legume growth and yield under nutrient stress conditions. Differences among rhizobial strains in their ability to obtain mineral nutrients from their environment may be agronomically important.

Key words

bacteroid (Brady) Rhizobium legume nodulation nutrient deficiency symbiosis 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ahmed S and Evans H J 1960 Cobalt: a micronutrient element for the growth of soybean plants under symbiotic conditions. Soil Sci. 90, 205–10.Google Scholar
  2. Anderson A J 1956 Effects of fertilizer treatments on pasture growth. Proc. 7th Internat. Grassl. Congr. 323–33.Google Scholar
  3. Anderson A J and Spencer D 1950a Molybdenum in nitrogen metabolism of legumes and non-legumes. Aust. J. Sci. Res. B. 3, 414–30.Google Scholar
  4. Anderson A J and Spencer D 1950b Sulphur in nitrogen metabolism of legumes and non-legumes. Aust. J. Sci. Res. B. 3, 431–49.Google Scholar
  5. Andrew, C S 1976 Effect of calcium, pH and nitrogen on the growth and chemical composition of some tropical and temperate pasture legumes. I Nodulation and Growth. Aust. J. Agric. Res. 27, 611–623.Google Scholar
  6. Andrew C S 1977a Nutritional restraints on legume—symbiosis.In Exploiting the Legume—Rhizobium Symbioses in Tropical Agriculture Eds. J M Vincentet al. pp 253–274. Univ. Hawaii, College of Trop. Agric. Misc. Pub. 145.Google Scholar
  7. Andrew C S 1977b The effect of sulphur on the growth, sulphur and nitrogen concentrations, and critical sulphur concentrations of some tropical and temperate pasture legumes. Aust. J. Agric. Res. 28, 807–20.CrossRefGoogle Scholar
  8. Andrew C S, Kippo E A and Barford H 1952 Plant responses to nitrogen and sulphur on a heavy clay soil from the Darling Downs, South-east Queensland. Aust. J. Agric. Res. 3, 111–24.CrossRefGoogle Scholar
  9. Anon 1979 Iron. Subcommittee on Iron. Committee on Medical and Biologic effects of Environmental Pollutants. National Research Council, University Park Press, Baltimore.Google Scholar
  10. Arnon D I and Stout P R 1939 The essentiality of certain elements in minute quantity for plants with special reference to copper. Plant Physiol. 14, 371–375.Google Scholar
  11. Banath C L, Greenwood E A N and Loneragan J F 1966 Effects of calcium deficiency on symbiotic nitrogen fixation. Plant Physiol. 41, 760–3.Google Scholar
  12. Beck D P and Munns D N 1984 Phosphate nutrition ofRhizobium spp. J. Appl. Env. Microbiol. 47, 278–82.Google Scholar
  13. Beck D P and Munns D N 1985 Effect of calcium on the phosphorus nutrition ofRhizobium meliloti. Soil Sci. Soc. Am. J. 49, 334–337.Google Scholar
  14. Bell R W 1985 Effects of Calcium on Growth, Nodulation, and Nutrient Uptake by Tropical Grain Legumes. Ph. D. thesis. University of Queensland, Brisbane.Google Scholar
  15. Bergersen F J 1961 The growth of Rhizobium in synthetic media. Aust. J. Biol. Sci. 14, 349–360.Google Scholar
  16. Bergersen F J 1974 The effects of phosphate concentrations on N2 and NH4+-grownKlebsiella pneumonia. J. Gen. Microbiol. 4, 412–4.Google Scholar
  17. Bieleski R L 1973 Phosphate pools, phosphate transport, and phosphate availability. Annu. Rev. Plant Physiol. 24, 225–252.CrossRefGoogle Scholar
  18. Blevins D G, Barnett N M and Bottino P J 1977. The effects of calcium deficiency and the ionophore A23187 on nodulation, nitrogen fixation and growth of soybeans. Physiol. Plant. 41, 235–38.Google Scholar
  19. Brenchley W E and Thornton H G 1925 The relation between the development, structure and functioning of the nodules onVicia faba, as influenced by the presence or absence of boron on the nutrient medium. Proc. Roy. Soc. B. 98, 373–9.Google Scholar
  20. Brown C M and Dilworth M J 1975 Ammonia assimilation by Rhizobium cultures and bacteroids. J. Gen. Microbiol. 86, 39–48.PubMedGoogle Scholar
  21. Cartwright B and Hallsworth E G 1970 Effects of copper deficiency on root nodules of subterraneum clover. Plant and Soil 33, 685–98.CrossRefGoogle Scholar
  22. Cassman K G, Munns D N and Beck D P 1981a Phosphorus nutrition ofRhizobium japonicum: strain differences in phosphate storage and utilization. Soil Sci. Soc. Am. J. 45, 517–520.Google Scholar
  23. Cassman K G, Munns D N and Beck D P 1981b Growth of Rhizobium strains at low concentrations of phosphate. Soil. Sci. Soc. Am. J. 45, 520–523.Google Scholar
  24. Chandler M R 1978 Some observations on infection ofArachis hypogaea by Rhizobium. J. Exp. Bot 29, 749–55.Google Scholar
  25. Chandler M R, Date R A and Roughley R J 1982 Infection and root nodule development inStylosanthes sp. byRhizobium. J. Exp. Bot. 33, 45–57.Google Scholar
  26. Chatel D L, Robson A D Gartrell J W and Dilworth, M J 1978 The effect of inoculation and cobalt application on the growth of and nitrogen fixation by sweet lupins. New Phytol. 83, 63–79.Google Scholar
  27. Clark D G 1936 Physiological studies onRhizobium species. New York Agr. Exp. Sta. Ithaca Mem. 196.Google Scholar
  28. Cowles J R and Evans H J 1968 Some properties of the ribonucleotide reductase fromRhizobium meliloti. Arch. Biochem. Biophys. 127, 770–778.CrossRefPubMedGoogle Scholar
  29. Craswell E T, Loneragan J F and Keerati-Kasikorn P 1987 Mineral constraints to food legume crop production in Asia. Paper presented to ACIAR WORKSHOP on Food Legume Improvement for Asian Farming Systems, Khon Kaen. Thailand. pp 99–111.Google Scholar
  30. Damirgi S M, Frederick L R and Anderson I C 1967 Serogroups ofRhizobium japonicum in soybean nodules as affected by soil types. Agron J. 59, 10–12.Google Scholar
  31. Danso S K A 1977 The ecology of Rhizobium and recent advances in the study of the ecology of Rhizobium.In Biological Nitrogen Fixation in Farming Systems of the Tropics. Eds. A Ayanaba and P J Dart, pp 115–126, Wiley, New York.Google Scholar
  32. Dart P J 1977 Infection and development of leguminous nodules.In A Treatise on Dinitrogen Fixation, Section III, Biology, Eds. R W F Hardy and W S Silver. pp 367–472. John Wiley and Sons, Inc., New York.Google Scholar
  33. Date R A and Halliday J 1980 Relationships betweenRhizobium and tropical forage legumes.In Advances in Legume Science. Eds. R J Summerfield and A H Bunting, pp 597–601, HMSO, London.Google Scholar
  34. Date R A and Norris D O 1979 Rhizobium screening ofStylozanthes species for effectiveness in nitrogen fixation. Aust. J. Agric. Res. 30, 85–104.CrossRefGoogle Scholar
  35. De Hertogh A A, Mayeux P A and Evans H J 1964 The relationship of cobalt requirements to propionate metabolism in Rhizobium. J. Biol. Chem. 239, 2446–2455.Google Scholar
  36. Delwiche C C, Johnson C M and Reisenauer H M 1961 Influence of cobalt on nitrogen fixation by Medicago. Plant Physiol. 36, 73–8.Google Scholar
  37. Dilworth M J 1974 Dinitrogen fixation. Annu. Rev. Plant Physiol. 25, 81–114.CrossRefGoogle Scholar
  38. Dilworth M J 1985 The mineral nutrition of Rhizobium as a factor in considering the mineral nutrition of legumes. Tropical Legume Improvement. ACIAR Proceedings Series No. 8, 71–73.Google Scholar
  39. Dilworth M J and Bisseling T 1984 Cobalt and nitrogen fixation inLupinus angustifolius L. III DNA and methionine in bacteroids. New Phytol. 98, 311–316.Google Scholar
  40. Dilworth M J and Glenn A R 1984 How does a legume nodule work? Trends Biochem. Sci. 9, 519–522.CrossRefGoogle Scholar
  41. Dilworth M J and Glenn A R 1985 Transport in Rhizobium and its significance to the legume symbiosis.In Nitrogen Fixation and CO2 Metabolism, Eds. P W Ludden and J E Burris. Elsevier Science Publishing Co., Inc.Google Scholar
  42. Dilworth M J, Robson A D and Chatel D L 1979 Cobalt and nitrogen fixation inLupinus angustifolius L. 11 Nodule formation and function. New Phytol. 83, 63–79.Google Scholar
  43. Eady R R and Robson R L 1984 Characteristics of N2 fixation in Mo-limited batch and continuous cultures ofAzotobacter vinelandii. Bochem. J. 224, 853–862.Google Scholar
  44. Eady R R, Robson R L, Richardson T H, Miller R W and Hawkins M 1987 The Vanadium initrogenase ofAzotobacter chroococcum. Biochem J. 244, 197–207.PubMedGoogle Scholar
  45. Edwards D G 1977 Nutritional factors limiting nitrogen fixed by rhizobia.In Biological Nitrogen Fixation in Farming systems of The Tropics. Eds. A Ayanaba and P J Dart, pp 189–204, Wiley, New York.Google Scholar
  46. Gates C T and Wilson J R 1974 The interaction of nitrogen and phosphorus on the growth, nutrient status and nodulation ofStylosanthes humilis H.B.K. (Townsville Stylo). Plant and Soil 41, 325–33.CrossRefGoogle Scholar
  47. Gates C T, Wilson J R and Shaw N H 1966 Growth and chemical composition of Townsville lucerne (Stylosanthes humilis). 2. Chemical composition with special reference to cations, as affected by the principal constituent elements of molybdenised super phosphate. Aust. J. Exp. Agric. Anim. Husb. 6, 266–76.Google Scholar
  48. Greenwood E A N and Hallsworth E G 1960 Studies on the nutrition of forage legumes. II. Some interactions of calcium, phosphorus, copper and molybdenum on the growth and chemical composition ofTrifolium subterraneaum L. Plant and Soil 12, 97–127.Google Scholar
  49. Ham G E, Frederick L R and Anderson I C 1971 Serogroups ofRhizobium japonicum in soybean nodules sampled in Iowa. Agron. J. 63, 69–72.Google Scholar
  50. Hardy R W F and Holsten R D 1977 Methods for measurement of dinitrogen fixation.In A Treatise on Dinitrogen Fixation. Eds. R W F Hardy and A H Gibson. John Wiley and Sons, New York.Google Scholar
  51. Hohenberg J S and Munns D N 1984 Effect of soil acidity factors on nodulation and growth ofVigna unguiculata in solution culture. Agron. J. 76, 477–481.Google Scholar
  52. Humphrey B A and Vincent J M 1962 Calcium in cell walls ofRhizobium trifolii. J. Gen. Microbiol. 19, 557–562.Google Scholar
  53. Jha K K 1966 Effect of molybdenum, vanadium, tungsten, and cobalt on the growth of Rhizobium. Ind. J. Microbiol. 6, 29–34.Google Scholar
  54. Johansen C, Kerridge P C, Luck P E, Cook B G Lowe K F and Ostrowski H 1977 The residual effect of molybdenum fertilizers on growth of tropical pasture legumes in a subtropical environment. Aust. J. Exp. Agric. Anim. Husb. 17, 961–68.CrossRefGoogle Scholar
  55. Jones R K, Robinson P J, Haydock K P and Megarrity R G 1971 Sulphur-nitrogen relationships in the tropical legumeStylosanthes humilis. Aust. J. Agric. Res. 22, 885–94.CrossRefGoogle Scholar
  56. Jordan J V and Anderson G R 1950 The effect of boron on nitrogen fixation by Azotobacter. Soil Sci. 69, 311–19.Google Scholar
  57. Keyser H H, Munns D N and Hohenberg J S 1979 Acid tolerance of rhizobia in culture and in symbiosis with cowpea. Soil Sci. Soc. Am. J. 43, 719–722.Google Scholar
  58. Lo S Y and Reisenauer H M 1968 Zinc nutrition of alfalfa. Agron. J. 60, 464–66.Google Scholar
  59. Loneragan J F 1959 Calcium in the nitrogen metabolism of subterraneum clover. Aust. J. Biol. Sci. 12, 26–39.Google Scholar
  60. Loneragan J F 1972 The soil chemical environment in relation to symbiotic nitrogen fixation.In Use of Isotopes for Study of Fertilizer Utilization by Legume Crops. Tech. Rep. No 149. FAO/IAEA, Vienna.Google Scholar
  61. Loneragan J F and Dowling E J 1958 The interaction of calcium and hydrogen ions in the nodulation of subterranean clover. Aust. J. Agric. Res. 9, 464–472.CrossRefGoogle Scholar
  62. Lowe R H and Evans H J 1962 Cobalt requirement for the growth of rhizobia. J. Bacteriol. 83, 210–211.PubMedGoogle Scholar
  63. Lowe R H, Evans H J and Ahmed S 1960 The effect of cobalt on the growth ofRhizoboium japonicum. Biochem. Biophys. Res. Commun. 3, 675–678.PubMedGoogle Scholar
  64. Lowther W L 1970 Calcium in the nodulation and growth of legumes. PhD Thesis. University of Western Australia.Google Scholar
  65. Lowther W L and Loneragan J F 1968 Calcium and nodulation of subterraneum clover. Plant Physiol. 43, 1362–1366.Google Scholar
  66. Lowther W L and Loneragan J F 1970 Calcium in the nodulation of legumes. Ed. M J T Norman. Proc. of the XIthe Int. Grassl. Congr. Surfers Paradise. pp446–450.Google Scholar
  67. McCalla T M 1937 Behaviour of legume bacteria (Rhizobium) in relation to exchangeable calcium and hydrogen ion concentration of the colloidal fraction of the soil. Res. Bull. Miss. Agric. Exp. Sta. No. 256.Google Scholar
  68. McLachlan K D and Norman B W 1961 Phosphorus and symbiotic nitrogen fixation in subterranean clover. J. Aust. Inst. Agric. Sci. 27, 244–5.Google Scholar
  69. Miller R W and Sirois J C 1983 Calcium and magnesium effects on symbiotic nitrogen fixation in the alfalfa (M. sativa)—Rhizobium meliloti system. Physiol. Plant. 58, 464–470.Google Scholar
  70. Modi M, Shah K S and Modi V V 1985 Isolation and characterisation of catechol-like siderophore from cowpea Rhizobium RA-1. Arch. Microbiol. 141, 156–158.CrossRefGoogle Scholar
  71. Mulder E G 1948 Investigations on the nitrogen nutrition of pea plants. Plant and Soi 1, 179–212.Google Scholar
  72. Munns D N 1970 Nodulation ofMedicago sativa in solution culture. V. Calcium and pH requirements during infection. Plant and Soil. 32, 90–102.CrossRefGoogle Scholar
  73. Munns D N 1977 Mineral nutrition and the legume symbiosis.In A Treatise on Dinitrogen Fixation. Section IV. Agronomy and Ecology. Eds. R W F Hardy and A H Gibson John Wiley and Sons, New York.Google Scholar
  74. Munns D N 1978 Soil acidity and nodulation.In Mineral Nutrition of Legumes in Tropical and Subtropical soils. Eds. C S Andrew and E J Kamprath, pp 247–264 Melbourne, Australia. CSIRO.Google Scholar
  75. Munns D N 1979 Mineral nutrition and nodulation.In Proc. of the World Soybean Research Conf. 11. Ed. FT Corbin, pp 47–56, Westview Press, Boulder, Colorado.Google Scholar
  76. Munns D N 1986 Acid soil tolerance in legumes and rhizobia.In Advances in Plant Nutrition Volume 2. Eds. B Tinker and A Lauchli, pp 63–92. Praeger, New York.Google Scholar
  77. Munns D N and Mosse B 1980 Mineral nutrition of legume crops.In Advances in Legume Science. Eds. R J Summerfield and A H Bunting, pp 115–125 H M S O London.Google Scholar
  78. Nambiar P T C and Sivaramakrishnan S 1987 Detection and assay of siderophores in cowpea rhizobia (Bradyrhizobium) using radioactive Fe (59Fe). Lett. Appl. Microbiol 4, 37–40.Google Scholar
  79. Neilands J B 1981 Microbial iron compounds. Annu. Rev. Biochem. 50, 715–31.CrossRefPubMedGoogle Scholar
  80. Neilands J B 1982 Microbial envelope proteins related to iron. Annu. Rev. Microbiol. 36, 285–309.CrossRefPubMedGoogle Scholar
  81. Norris D O 1956 Legumes and the Rhizobium symbiosis. Emp. J. Exp. Agric. 24, 247–70.Google Scholar
  82. Norris D O 1958 Rhizobium need magnesium, not calcium. Nature 182, 734–5.Google Scholar
  83. Norris D O 1959 The role of calcium and magnesium in the nutrition ofRhizobium. Aust. J. Agric. Res. 10, 651–98.CrossRefGoogle Scholar
  84. O'Hara G W, Riley I T, Glenn A R and Dilworth M J 1985. The ammonium permease ofRhizobium leguminosarum MNF 3841. J. Gen. Microbiol. 131, 757–764.Google Scholar
  85. O'Hara G W, Franklin M and Dilworth M J 1987a Sulphur nutrition of bradyrhizobia.In UNESCO Regional Symposium and Workshop on Biotechnology of Nitrogen Fixation in the Tropics, 25–29 Aug. 1986, UPM, Serdang, Malaysia (In press).Google Scholar
  86. O'Hara G W, Franklin M and Dilworth M J 1987b Sulfur nutrition of free living and symbioticBradyrhizobium japonicum andBradyrhizobium sp. (Arachis).In Proc. Int. Symposium on Food Legume Improvement for Asian Farming Systems 1–5 Sept. 1986. Khon Kaen, Thailand no 18, p 275.Google Scholar
  87. O'Hara G W, Franklin M and Dilworth M J 1987c Effect of sulfur supply on sulfate uptake, and alkaline sulfatase activity in free-living and symbiotic bradyrhizobia. Arch. Microb. 149, 163–167.Google Scholar
  88. O'Hara G W, Dilworth M J, Boonkerd N and Parkpian P 1988a Iron deficiency specifically limits nodule development in peanut inoculated withBradyrhizobium sp. New Phytol. 108, 51–57.Google Scholar
  89. O'Hara G W, Hartzook A, Bell R W and Loneragan J F 1988b Response toBradyrhizobium strain of peanut cultivars grown under iron stress. J. Plant Nutr. (In press).Google Scholar
  90. Olsson J E and Rolfe B G 1985 Stem and root nodulation of the tropical legumeSesbania rostrata by Rhizobium strains ORS-571 and WE7. J. Plant Physiol. 121, 199–210.Google Scholar
  91. Reisenauer H M 1966 Concentrations of nutrient ions in soil solution.In Environmental Biology. Federation of American Societies for EWxperimental Biology. Bethesda. Ed. P H Altman, pp 507–508.Google Scholar
  92. Rerkasem B, Netsangtip R, Loneragan J F and Bell R W 1987 Boron deficiency in grain legumes.In Proc. Int. Workshop on Food Legume Improvement in Asian Farming Systems. Khon Kaen, Thailand. ACIAR. no. 18, p 267.Google Scholar
  93. Riley I T and Dilworth M J 1982 Cobalt and the contribution of crown and lateral nodules to nitrogen fixation ofLupinus angustifolius L. New Phytol. 90, 717–721.Google Scholar
  94. Riley I T and Dilworth M J 1985a Cobalt status and the effects on soil populations ofRhizobium lupini, rhizosphere colonization and nodule initiation. Soil Biol. Biochem. 17, 81–85.CrossRefGoogle Scholar
  95. Riley I T and Dilworth M J 1985b Cobalt requirement for nodule formation and function inLupinus angustifolius L. New Phytol. 100, 347–359.Google Scholar
  96. Riley I T and Dilworth 1985c Recovery of cobalt-deficient root nodules inLupinus angustifolius L. New Phytol. 100, 361–365.Google Scholar
  97. Rioux C R, Jordan D C and Rattray J B M 1986a Iron requirement ofRhizobium leguminosarum and secretion of anthranilic acid during growth on an iron-deficient medium. Arch. Biochem. Biophys. 248, 175–182.PubMedGoogle Scholar
  98. Rioux C R, Jordan D C and Rattray J B M 1986b Anthranilate-promoted iron uptake inRhizobium leguminosarum. Arch. Biochem. Biophys. 248, 183–189.PubMedGoogle Scholar
  99. Robertson J G, Lyttleton P, Bullivant S and Graston G F 1978a. Membranes in lupine root nodules. 1. The role of Golgi bodies in the biogenesis of infection threads and peribacteroid membranes. J. Cell. Sci 30, 129–149.PubMedGoogle Scholar
  100. Robertson J G, Warburton M P, Lyttleton P, Fordyce A M and Bullivant S 1978b Membranes in lupine root nodules. II. Preparation and properties of peribacteroid membranes and bacteroid envelope inner membranes from developing root nodules. J. Cell. Sci. 30, 151–174.PubMedGoogle Scholar
  101. Robson A D 1978 Mineral nutrients limiting nitrogen fixation in legumes.In The Mineral Nutrition of Legumes in Tropical and Subtropical Soils. Eds. C S Andrew and E J Kamprath, pp 277–293 CSIRO Melbourne.Google Scholar
  102. Robson A D 1983 Mineral nutrition.In Nitrogen Fixation. Vol. III. Ed. W J Broughton. pp 36–55. Clarendon Press Oxford.Google Scholar
  103. Robson A D and Pitman M 1983 Interaction between nutrients in higher plants.In Encyclopedia of Plant Physiology, Vol. 15, Inorganic Plant Nutrition. Eds. A Lauchli and R Bieleski, pp 147–180. Berlin, Springer-Verlag.Google Scholar
  104. Robson A D, O'Hara G W and Abbott L K 1981 Inovlvement of phosphorus in nitrogen fixation by subterranean clover (Trifolium subterraneum L.). Aust. J. Plant Physiol 8, 427–436.Google Scholar
  105. Roessler P G and Nadler K D 1982 Effects of iron deficiency on heme biosynthesis inRhizobium japonicum. J. Bacteriol. 149, 1021–1026.PubMedGoogle Scholar
  106. Rolfe B G, Djordjeric M, Scott K F, Hughes J E, Badenoch Jones J, Gresshoff P M, Cen Y, Dudman W F, Zurkowski W and Shine J 1981 Analysis of the nodule forming ability of fast growing Rhizobium strainsIn Current Perspectives in Nitrogen Fixation. Eds. A H Gibson and W E Newton, Aust. Acad. Sci., Canberra.Google Scholar
  107. Sato K, Seki T, Unukai S and Shimiza S 1982 Effects of vitamin B12-dependent enzymes and folate compounds on morphological changes ofRhizobium meliloti. Agric. Biol. Chem. 46, 501–505.Google Scholar
  108. Sethi R S and Reporter M 1981 Calcium localization pattern in clover root hair cells associated with infection process: studies with aureonycin. Protoplasma 105, 321–325.CrossRefGoogle Scholar
  109. Sherwood M T 1970 Improved synthetic medium for the growth ofRhizobium. J. Appl. Bacteriol. 33, 708–13.PubMedGoogle Scholar
  110. Smart J B, Robson A D and Dilworth M J 1984a A continuous culture study of the phosphorus nutrition ofRhizobium trifolii WU95, Rhizobium NGR 234 and Brady-rhizobium CB756. Arch. Microbiol. 140, 276–280.Google Scholar
  111. Smart J B, Robson A D and Dilworth M J 1984b Effect of phosphorus supply on phosphate uptake and alkaline phosphatase activity in rhizobia. Arch. Microbiol. 140, 281–286.Google Scholar
  112. Smith M J and Neilands J B 1984 Rhizobactin, a siderophore fromRhizobium meliloti. J. Plant Nutr. 7, 449–458.Google Scholar
  113. Smith M J, Shooler J N, Schwyn B, Holden I and Neilands J B 1985 Rhizobactin, a structurally novel siderophore fromRhizobium meliloti. J. Am. Chem. Soc. 107, 1739–1743.Google Scholar
  114. Snowball K, Robson A D and Loneragan J F 1980 The effect of copper on nitrogen fixation in subterraneum clover (Trifoluim subterraneum) New Phytol. 85, 63–72.Google Scholar
  115. Steinberg R A 1938 Applicability of nutrient-solution purification to the study of trace-element requirements of Rhizobium and Azotobacter. J. Agric. Res. 57, 471–6.Google Scholar
  116. Strachan R C, Aranha H, Lodge J S, Arceneaux J E L and Byers B P 1982 Teflon chemostat for studies of trace metal metabolism inStreptococcus mutans and other bacteria. Appl. Environ. Microbiol. 43, 257–260.PubMedGoogle Scholar
  117. Stults L W, Mallick S and Maier R J 1987 Nickel uptake inBradyrhizobium japonicum. J. Bacteriol. 169, 1398–1402.PubMedGoogle Scholar
  118. Rhorne D W and Walker R H 1936 Physiological studies onRhizobium. VI. accessory factors. soil Sci. 42, 231–40.Google Scholar
  119. Truesdell H W 1917 The effect of phosphorus on alfalfa and alfalfa bacteria. Soil Sci. 3, 77–98.Google Scholar
  120. Van der Elst F H, McNaught K J and Rolt W F 1961 Effects of copper deficiency in white clover on nitrogen fixation. Nature 192, 1315.Google Scholar
  121. Verma D P S and Long S 1983 The molecular biology ofRhizobium—legume symbiosis.In Int. Rev. Cytol. Suppl. 14. Ed. K Jeon, pp 211–245, Academic Press, New York.Google Scholar
  122. Verma D P S and Nadler K 1984 Legume—Rhizobium symbiosis: Hosts point of view.In Genes Involved in Microbe Plant Interactions. Eds. D P S Verma and Th Hohn, pp 57–93, Springer-Verlag, New York.Google Scholar
  123. Vincent J M 1962 Influence of calcium and magnesium on the growth of Rhizobium. J. Gen. Microbiol. 28, 653–63.PubMedGoogle Scholar
  124. Vincent J M 1977 Rhizobium: General microbiology.In A treatise on Dinitrogen Fixation III. Eds. R W F Hardy and W S Silver, pp 277–366, New York, Wiley.Google Scholar
  125. Vincent J M 1980 Factors controlling the legume—Rhizobium symbiosis.In Nitrogen Fixation, II. Eds. W E Newton and W H Orme-Johnson, pp 103–120. University Park Press, Baltimore.Google Scholar
  126. Vincent J M and Colburn J R 1961 Cytological abnormalities inRhizobium trifolii due to a deficiency of calcium or magnesium. Aust. J. Sci. 23, 269–270.Google Scholar
  127. Vincent J M and Humphrey B A 1963 Partition of divalent cations between bacterial wall and cell contents. Nature 199, 149–153.PubMedGoogle Scholar
  128. Vincent J M and Humphrey B A 1968 Modification of the antigenic surface ofRhizobium trifolii by a deficiency of calcium. J. Gen. Microbiol. 54, 397–405.PubMedGoogle Scholar
  129. Walker T W and Adams A F R 1958 Competition for sulphur in a grass-clover association. Plant and Soil 9, 353–66.CrossRefGoogle Scholar
  130. Weber D F, Caldwell B E, Sloger C and Vest H G 1971 Some USDA studies on the soybeanRhizobium symbiosis. Plant Soil, Special Volume, 293–304.Google Scholar
  131. Werner D, Kuhlmann K P, Goystein F and Richter F W 1985 Calcium, iron and cobalt accumulation in root hairs of soybean (Glycine max). Z. Naturforsch 40, 912–913.Google Scholar
  132. Wilson D D and Reisenauer H M 1970 Effect of manganese and zinc ions on the growth of Rhizobium. J. Bacteriol. 102, 729–32.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1988

Authors and Affiliations

  • Graham W. O'hara
    • 1
  • Nantakorn Boonkerd
    • 2
  • Michael J. Dilworth
    • 1
  1. 1.Nitrogen Fixation Research Group, School of Environmental and Life SciencesMurdoch UniversityMurdochAustralia
  2. 2.Soil Science Division, Department of AgricultureBNF Resource CenterBangkokThailand

Personalised recommendations