Plant and Soil

, Volume 82, Issue 3, pp 273–284 | Cite as

Efficiencies and inefficiencies in the legume/Rhizobium symbiosis—A review

  • C. A. Atkins


Studies of the C and N economy of a range of temperate and tropical legume/Rhizobium symbioses indicate considerable variation (up to three-fold) in the cost of N2 fixation. Comparisons between and within symbioses indicate that the proportion of net photosynthate utilized in nodule functioning varies almost ten-fold from as low as 3% to as high as 25%. Factors possibly responsible for variation in efficiency of C use in nodules and in the proportioning of translocated photosynthetic products to nodules are discussed.

Key words

Legume Nitrogen fixation Rhizobium C and N economy 


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  1. 1.
    Abu-Shakra S S, Phillips D A and Huffaker R C 1978 Nitrogen fixation and delayed leaf senescence in soybeans. Science 199, 973–975.Google Scholar
  2. 2.
    Albrecht S L, Maier R J, Hanus F J, Russell S A, Emerich D W and Evans H J 1979 Hydrogenase inRhizobium japonicum increases nitrogen fixation by nodulated soybeans. Science 203, 1255–1257.Google Scholar
  3. 3.
    Atkins C A 1982 Ureide metabolism in legumes.In Advances in Agricultural Microbiology. Ed. N S S Rao. Oxford and IBH, New Delhi, pp 53–88.Google Scholar
  4. 4.
    Atkins C A, Herridge D F and Pate J S 1978 The economy of carbon and nitrogen in nitrogen-fixing annual legumes.In Isotopes in Biological Dinitrogen Fixation, Vienna, Int. At. Energy Agency, pp 211–242.Google Scholar
  5. 5.
    Atkins C A, Pate J S, Griffiths G J and White S T 1980 Economy of carbon and nitrogen in nodulated and non-nodulated NO3-grown cowpea (Vigna unguiculata (L.) Walp.). Plant Physiol. 66, 978–983.Google Scholar
  6. 6.
    Atkins C A, Pate J S and Layzell D B 1979 Assimilation and transport of nitrogen in non-nodulated (NO3-grown)Lupinus albus L. Plant Physiol. 64, 1078–1082.Google Scholar
  7. 7.
    Bedmar E J, Edie S A and Phillips D A 1983 Host plant cultivar effects on hydrogen evolution byRhizobium leguminosarum. Plant Physiol. 72, 1011–1015.Google Scholar
  8. 8.
    Butz R G and Jackson W A 1977 A mechanism for nitrate transport and reduction. Phytochem. 16, 409–417.Google Scholar
  9. 9.
    Canvin D T and Atkins C A 1974 Nitrate, nitrite and ammonia assimilation by leaves: Effect of light, carbon dioxide and oxygen. Planta 116, 207–224.CrossRefGoogle Scholar
  10. 10.
    Christeller J T, Laing W A and Sutton W D 1977 Carbon dioxide fixation by lupin root nodules. I. Characterization, association with phosphoenolpyruvate carboxylase and correlation with nitrogen fixation during nodule development. Plant Physiol. 60, 47–50.Google Scholar
  11. 11.
    Dart P J and Mercer F V 1965 The influence of NH4NO3 on the fine structure of nodules ofMedicago tribuloides Desr. andTrifolium subterraneum L. Arch Microbiol. 51, 233–257.Google Scholar
  12. 12.
    Dixon R O D 1978 Nitrogenase-hydrogenase interrelationships in rhizobia. Biochimie 60, 233–236.PubMedGoogle Scholar
  13. 13.
    Emerich D W, Lepo J E and Evans H J 1983 Nodule metabolism.In Nitrogen Fixation Vol 3 Legumes. Ed. W J Broughton, 213–244.Google Scholar
  14. 14.
    Ham G E and Caldwell A C 1978 Fertilizer placement effects on soybean seed yield, N2 fixation and P uptake. Agron J. 70, 779–783.Google Scholar
  15. 15.
    Hardy R W F and Havelka U D 1976 Photosynthate as a major factor limiting nitrogen fixation by field-grown legumes with emphasis on soybeans.In Symbiotic Nitrogen Fixation in plants. Ed P S Nutman, Cambridge Univ. Press, pp 421–439.Google Scholar
  16. 16.
    Herridge D F and Pate J S 1977 Utilization of net photosynthate for nitrogen fixation and protein production in an annual legume. Plant Physiol. 60, 759–764.Google Scholar
  17. 17.
    Hunter W J, Fahring C J, Olsen S R and Porter L K 1982 Location of nitrate reduction in different soybean cultivars. Crop. Sci. 22, 944–948.Google Scholar
  18. 18.
    Kueneman E A, Wallace D H and Ludford P M 1979 Photosynthetic measurements of field-grown dry beans and their relation to selection for yield. J. Am. Soc. Hortic. Sci. 104, 480–482.Google Scholar
  19. 19.
    Lawn R J and Brun W A 1974 Symbiotic nitrogen fixation in soybeans. I. Effect of photosynthetic source-sink manipulations. Crop Sci. 14, 11–16.Google Scholar
  20. 20.
    Layzell D B, Rainbird R M, Atkins C A and Pate J S 1979 Economy of photosynthate use in N-fixing legume nodules. Observations on two contrasting symbioses. Plant Physiol. 64, 888–891.Google Scholar
  21. 21.
    Mahon J D 1982 Field evaluation of growth and nitrogen fixation in peas selected for high and low photosynthetic CO2 exchange. Can. J. Plant Sci. 62, 5–17.Google Scholar
  22. 22.
    Mahon J D 1983 Energy relationships.In Nitrogen Fixation Vol. 3 Legumes. Ed. W J Broughton, Clarendon Press Oxford, pp 299–325.Google Scholar
  23. 23.
    Mahon J D and Hobbs S L A 1981 Selection of peas for photosynthetic CO2 exchange rate under field conditions. Crop Sci. 21, 616–621.Google Scholar
  24. 24.
    Maier R J and Brill W J 1978 Mutant strains ofRhizobium japonicum with increased ability to fix nitrogen for soybean. Science 201, 448–450.Google Scholar
  25. 25.
    Malik N S A 1983 Grafting experiments on the nature of the decline of N2 fixation during fruit development in soybean. Physiol. Plant 57, 561–564.Google Scholar
  26. 26.
    Neves M C P, Minchin F R and Summerfield R J 1981 Carbon metabolism, nitrogen assimilation and seed yield of cowpea (Vigna unguiculata) plants dependent on nitratenitrogen or on one of two strains ofRhizobium. Trop. Agric. 58, 115–132.Google Scholar
  27. 27.
    Nooden L D and Leopold A C 1978 Hormonal control of senescence and abscission.In Phytohormones and Related Compounds, Vol. II. Eds. D S Letham, T J Higgins and P B Goodwin, Elsevier Amsterdam, pp 329–369.Google Scholar
  28. 28.
    Oghoghorie C G O and Pate J S 1971 The nitrate stress syndrome of the nodulated field pea (Pisum arvense L.). Techniques for measurement and evaluation in physiological terms. Plant and Soil Spec. Vol. pp 185–202.Google Scholar
  29. 29.
    Pate J S and Atkins C A 1983 Nitrogen Uptake, Transport and Utilization.In Nitrogen Fixation Vol. 3. Legumes. Ed. W J Broughton, Clarendon Press, Oxford, pp 245–298.Google Scholar
  30. 30.
    Pate J S, Atkins C A and Rainbird R M 1981 Theoretical and experimental costing of nitrogen fixation and related processes in nodules of legumes.In Current Perspectives in Nitrogen Fixation. Eds. A H Gibson and W Newton; Aust. Acad. Sci. Canberra, pp 105–116.Google Scholar
  31. 31.
    Pate J S, Atkins C A, White S T, Rainbird R M and Woo K C 1980 Nitrogen nutrition and xylem transport of nitrogen in ureide-producing grain legumes. Plant Physiol. 65, 961–965.Google Scholar
  32. 32.
    Pate J S and Herridge D F 1978 Partitioning and utilization of net photosynthate in a nodulated annual legume. J. Exp. Bot. 29, 401–412.Google Scholar
  33. 33.
    Pate J S, Layzell D B and Atkins C A 1979 Economy of C and N in a nodulated and non-nodulated (NO3-grown) legume. Plant Physiol. 64, 1083–1088.Google Scholar
  34. 34.
    Peet M M, Bravo A, Wallace D H and Ozbun J L 1977 Photosynthesis, stomatal resistance, and enzyme activities in relation to yield of field grain dry bean varieties. Crop Sci. 17, 287–293.Google Scholar
  35. 35.
    Penning de Vries F W T 1975 The cost of maintenance processes in plant cells. Ann. Bot. 39, 77–92.Google Scholar
  36. 36.
    Penning de Vries F W T, Brunsting A H M and Van Laar H H 1974 Products, requirements and efficiency of biosynthesis: A quantitative approach. J. Theoret. Biol. 45, 337–339.Google Scholar
  37. 37.
    Peoples M B, Pate J S and Atkins C A 1983 Mobilization of nitrogen in fruiting plants of a cultivar of cowpea. J. Exp. Bot. 34, 563–578.Google Scholar
  38. 38.
    Phillips D A 1980 Efficiency of symbiotic nitrogen fixation in legumes. Annu. Rev. Plant Physiol. 31, 29–49.CrossRefGoogle Scholar
  39. 39.
    Rainbird R M, Atkins C A, Pate J S and Sanford P 1983 The significance of hydrogen evolution in the carbon and nitrogen economy of nodulated cowpea. Plant Physiol. 71, 122–127.Google Scholar
  40. 40.
    Rainbird R M, Atkins C A and Pate J S 1983 Diurnal variation in the functioning of cowpea. Plant Physiol. 72, 308–312.Google Scholar
  41. 41.
    Rainbird R M, Atkins C A and Pate J S 1983 Effect of temperature on nitrogenase functioning in cowpea nodules. Plant Physiol. 73, 392–394.Google Scholar
  42. 42.
    Schubert K R (Ed.) 1982 The energetics of biological nitrogen fixation. Workshop Summaries. I. Am. Soc. Plant Physiol. Maryland, USA pp 1–30.Google Scholar
  43. 43.
    Schubert K R and Evans H J 1976 Hydrogen evolution: a major factor affecting the efficiency of nitrogen fixation in nodulated symbionts. Proc. Natl. Acad. Sci. USA 73, 1207–1211.Google Scholar
  44. 44.
    Sheehy J E 1983 Relationships between senescence, photosynthesis, nitrogen fixation and seed filling in soya bean (Glycine max (L.) Merr. Ann. Bot. 51, 679–682.Google Scholar
  45. 45.
    Sinclair T R and de Wit C T 1975 Photosynthate and nitrogen requirements for seed production by various crops. Science 189, 565–567.Google Scholar
  46. 46.
    Somerville C R and Ogren W L 1982 Genetic modification of Photorespiration. Trends in Biochem. Sci. 7, 171–174.CrossRefGoogle Scholar
  47. 47.
    Sprent J I 1980 Root nodule anatomy, type of export product and evolutionary origin in someLeguminoscae. Plant Cell Environ. 3, 35–43.Google Scholar
  48. 48.
    Sutton W D 1983 Nodule development and senescence.In Nitrogen Fixation Vol. 3. Legumes. Ed. W J Broughton, Clarendon Press, Oxford. pp 144–212.Google Scholar
  49. 49.
    Woolhouse H W 1982 Leaf senescence.In The Molecular Biology of Plant Development. Eds. H Smith and D Grierson, Oxford, Blackwells. pp 256–281.Google Scholar

Copyright information

© Martinus Nijhoff/Dr W. Junk Publishers 1984

Authors and Affiliations

  • C. A. Atkins
    • 1
  1. 1.Botany DepartmentThe University of Western AustraliaNedlandsAustralia

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