Skip to main content

Maintaining Cooperation in the Legume-Rhizobia Symbiosis: Identifying Selection Pressures and Mechanisms

  • Chapter
Nitrogen-fixing Leguminous Symbioses

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Amarger, N. (1981). Competition for nodule formation between effective and ineffective strains of Rhizobium meliloti. Soil Biol. Biochem., 13, 475-480.

    Article  Google Scholar 

  • Axelrod, R., and Hamilton, W. D. (1981). The evolution of cooperation. Science, 211, 1390-1396.

    Article  PubMed  CAS  Google Scholar 

  • Bethlenfalvay, G. J., Abu-Shakra, S. S., and Phillips, D. A. (1978). Interdependence of nitrogen nutrition and photosynthesis in Pisum sativum L. II. Host plant response to nitrogen fixation by Rhizobium strains. Plant Physiol. 62 131-133.

    PubMed  CAS  Google Scholar 

  • Bever, J. D., and Simms, E. L. (2000). Evolution of nitrogen fixation in spatially structured populations of Rhizobium. Heredity, 85 366-372.

    Article  PubMed  CAS  Google Scholar 

  • Brewin, N. J. (1991). Development of the legume root nodule. Annu. Rev. Cell Biol., 7 191-226.

    Article  PubMed  CAS  Google Scholar 

  • Brockwell, J., Roughley, R. J., and Herridge, D. F. (1987). Population dynamics of Rhizobium japonicum strains used to inoculate three successive crops of soybean. Aust. J. Agric. Res., 38 61-74.

    Article  Google Scholar 

  • Bshary, R., and Grutter, A. S. (2002). Asymmetric cheating opportunities and partner control in a cleaner fish mutualism. Anim. Behav., 63 547-555.

    Article  Google Scholar 

  • Burdon, J. J., Gibson, A. H., Searle, S. D., Woods, M. J., and Brockwell, J. (1999). Variation in the effectiveness of symbiotic associations between native rhizobia and temperate Australian Acacia: Within-species interactions. J. Appl. Ecol., 36 398-408.

    Article  Google Scholar 

  • Bushby, H. V. A. (1993). Colonization of rhizospheres by Bradyrhizobium sp. in relation to strain persistence and nodulation of some pasture legumes. Soil Biol. Biochem., 25 597-605.

    Article  Google Scholar 

  • Cevallos, M. A., Encarnacion, S., Leija, A., Mora, Y., and Mora, J. (1996). Genetic and physiological characterization of a Rhizobium etli mutant strain unable to synthesize poly-β-hydroxybutyrate J. Bacteriol., 178 1646-1654.

    PubMed  CAS  Google Scholar 

  • Crespi, B. J. (2001). The evolution of social behavior in microorganisms. Trends Ecol. Evol., 16 178-183.

    Article  PubMed  Google Scholar 

  • Demezas, D. H., and Bottomley, P. J. (1986). Inter-strain competition between representatives of indigenous serotypes of Rhizobium trifolii. Appl. Environ. Microbiol., 52 1020-1025.

    PubMed  CAS  Google Scholar 

  • Denison, R. F. (2000). Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am. Nat. 156, 567-576.

    Article  Google Scholar 

  • Denison, R. F., Weisz, P. R., and Sinclair, T. R. (1983). Analysis of acetylene reduction rates of soybean nodules at low acetylene concentrations. Plant Physiol., 73 648-651.

    Article  PubMed  CAS  Google Scholar 

  • Denison, R. F., and Harter, B. L. (1995). Nitrate effects on nodule oxygen permeability and leghemoglobin. Nodule oximetry and computer modeling. Plant Physiol., 107 1355-1364.

    PubMed  CAS  Google Scholar 

  • Denison, R. F., Bledsoe, C., Kahn, M., O’Gara, F., Simms, E. L., and Thomashow, L. S. (2003). Cooperation in the rhizosphere and the “free rider” problem. Ecology, 84 838-845.

    Article  Google Scholar 

  • Denton, M. D., Coventry, D. R., Bellotti, W. D., and Howieson, J. G. (2000). Distribution, abundance and symbiotic effectiveness of Rhizobium leguminosarumbv. trifolii from alkaline pasture soils in South Australia. Aust. J. Exp. Agric., 40 25-35.

    Google Scholar 

  • Dowling, D. N., and Broughton, W. J. (1986). Competition for nodulation of legumes. Annu. Rev. Microbiol., 40 131-157.

    Article  PubMed  CAS  Google Scholar 

  • Ebert, D. (1998). Experimental evolution of parasites. Science, 282 1432-1435.

    Article  PubMed  CAS  Google Scholar 

  • Ferriére, R., Bronstein, J. L., Rinaldi, S., Law, R., and Gauduchon, M. (2002). Cheating and the evolutionary stability of mutualisms. Proc. Roy. Soc. LondonB , 269, 773-780.

    Google Scholar 

  • Frank, S. A. (1994a). Genetics of mutualism: The evolution of altruism between species. J. Theoret. Biol. 170, 393-400.

    Article  CAS  Google Scholar 

  • Frank, S. A. (1994b). Kin selection and virulence in the evolution of protocells and parasites. Proc. Roy. Soc. LondonB, 258, 153-161.

    Google Scholar 

  • Frank, S. A. (1995). Mutual policing and repression of competition in the evolution of cooperative groups. Nature, 377 520-522.

    Google Scholar 

  • Frank, S. A. (1998). Foundations of Social Evolution. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Gardner, A., and West, S. A. (2004). Cooperation and punishment, especially in humans. Am. Nat., 164, 736-764.

    Article  Google Scholar 

  • Gordon, D. M., Ryder, M. H., Heinrich, K., and Murphy, P. J. (1996). An experimental test of the rhizopine concept in Rhizobium meliloti. Appl. Environ. Microbiol., 62 3991-3996.

    PubMed  CAS  Google Scholar 

  • Gresshoff, P. M., and Rolfe, B. G. (1978). Viability of Rhizobium bacteroids isolated from soybean nodule protoplasts. Planta, 142 329-333.

    Article  Google Scholar 

  • Gutschick, V. P. (1981). Evolved strategies in nitrogen acquisition by plants. Am. Nat., 118 607-637.

    Article  CAS  Google Scholar 

  • Hagen, M. J., and Hamrick, J. L. (1996a). A hierarchical analysis of population genetic structure in Rhizobium leguminosarum bv. trifolii. Mol. Ecol., 5 177-186.

    Article  CAS  Google Scholar 

  • Hagen, M. J. and Hamrick, J. L. (1996b). Population level processes in Rhizobium leguminosarum bv. trifolii: The role of founder effects. Mol. Ecol., 5 707-714.

    Article  Google Scholar 

  • Hahn, M., and Studer, D. (1986). Competitiveness of a nif Bradyrhizobium japonicum mutant against the wild-type strain. FEMS Microbiol. Lett., 33 143-148.

    Google Scholar 

  • Hardin, G. (1968). The tragedy of the commons. The population problem has no technical solution; it requires a fundamental extension in morality. Science, 1621243–1248.

    Article  CAS  Google Scholar 

  • Hartwig, U., Boller, B., and Nösberger, J. (1987). Oxygen supply limits nitrogenase activity of clover nodules after defoliation. Ann. Bot., 59 285-291.

    CAS  Google Scholar 

  • Henrich, J., and Boyd, R. (2001). Why people punish defectors? Weak conformist transmission can stabilize costly enforcement of norms in cooperative dilemmas. J. Theoret. Biol., 208 79-89.

    Article  CAS  Google Scholar 

  • Herre, E. A. (1993). Population structure and the evolution of virulence in nematode parasites of fig wasps. Science, 259 1442-1445.

    Article  PubMed  CAS  Google Scholar 

  • Herre, E. A., Knowlton, N., Mueller, U. G., and Rehner, S. A. (1999). The evolution of mutualisms: Exploring the paths between conflict and cooperation. Trends Ecol. Evol., 14 49-53.

    Article  PubMed  Google Scholar 

  • Hetrick, B. A. D., Wilson, G. W. T., and Cox, T. S. (1993). Mycorrhizal dependence of modern wheat cultivars and ancestors: A synthesis. Can. J. Bot., 71 512-518.

    Google Scholar 

  • Hirsch, A. M. (1999). Role of lectins (and rhizobial exopolysaccharides) in legume nodulation. Curr. Opin. Plant Biol., 2320-326.

    Article  PubMed  CAS  Google Scholar 

  • Hirsch, P. R. (1996). Population dynamics of indigenous and genetically modified rhizobia in the field. New Phytol., 133 159-171.

    Article  Google Scholar 

  • Jimenez, J., and Casadesus, J. (1989). An altruistic model of the Rhizobium-legume association. J. Heredity, 80 335-337.

    Google Scholar 

  • Kahn, M. L., Kraus, J., and Somerville, J. E. (1985). A model of nutrient exchange in the Rhizobium-legume symbiosis. In H. J. Evans, P. J. Bottomley and W. E. Newton (Eds.), Nitrogen fixation research progress (pp. 193-199). Dordrecht, The Netherlands: Nijhoff Publishing.

    Google Scholar 

  • Kiers, E. T., West, S. A., and Denison, R. F. (2002). Mediating mutualisms: The influence of farm management practices on the evolutionary maintenance of symbiont cooperation. J. Appl. Ecol., 39 745-754.

    Article  Google Scholar 

  • Kiers, E. T., Rousseau R. A., West, S. A., and Denison, R. F. (2003). Host sanctions and the legume rhizobium mutualism. Nature, 425 78-81.

    Article  PubMed  CAS  Google Scholar 

  • Kretovich, V. L., Romanov, V. I., Yushkova, L. A., Shramko, V. I., and Fedulova, N. G. (1977). Nitrogen fixation and poly-β-hydroxybutyric acid content in bacteroids of Rhizobium lupini and Rhizobium leguminosarum. Plant Soil, 48 291-302.

    Article  CAS  Google Scholar 

  • Layzell, D. B., and Hunt, S. (1990). Oxygen and the regulation of nitrogen-fixation in legume nodules. Physiol. Plant., 80 322-327.

    Article  CAS  Google Scholar 

  • Leigh, Jr., E. G., and Rowell, T. E. (1995). The evolution of mutualism and other forms of harmony at various levels of biological organization. Ècologie, 26 131-158.

    Google Scholar 

  • Lindemann, W. C., Schmidt, E. L., and Ham, G. E. (1974). Evidence for double infection within soybean nodules. Soil Sci., 118 274-279.

    Article  Google Scholar 

  • Lodwig, E. M., Hosie, A. H. F., Bourdés, A., Findlay, K., Allaway, D., Karunakaran, R., et al. (2003). Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature, 422 722-726.

    Google Scholar 

  • Lodwig, E. M., and Poole, P. (2003). Metabolism of Rhizobium bacteroids. Crit. Rev. Plant Sci., 22 37-78.

    Article  CAS  Google Scholar 

  • Maske, G. G. B. (1989). Genetical analysis of the efficiency of VA mycorrhiza with spring wheat. Agric. Ecosys. Environ., 29 273-280.

    Article  Google Scholar 

  • Maynard-Smith, J., and Szathmary, E. (1995). The Major Transitions in Evolution. Oxford, UK: W.H. Freeman.

    Google Scholar 

  • McDermott, T. R., Graham, P. H., and Brandwein, D. H. (1987). Viability of Bradyrhizobium japonicum bacteroids. Arch. Microbiol., 148 100-106.

    Article  CAS  Google Scholar 

  • Murphy, P. J., Wexler, W., Grzemski, W., Rao, J. P., and Gordon, D. (1995). Rhizopines - their role in symbiosis and competition. Soil Biol. Biochem., 27 525-529.

    Article  CAS  Google Scholar 

  • Olivieri, I., and Frank, S. A. (1994). The evolution of nodulation in rhizobium: Altruism in the rhizosphere. J. Heredity, 85 46-47.

    Google Scholar 

  • Pate, J. S. (1986). Economy of symbiotic nitrogen fixation. In T.J. Givnish (Ed.), On the economy of plant form and function (pp. 299-326). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Pellmyr, O., and Huth, C. J. (1994). Evolutionary stability of mutualism between yuccas and yucca moths. Nature 372 257-260.

    Google Scholar 

  • Provorov, N. A. (1998). Coevolution of rhizobia with legumes: Facts and hypotheses. Symbiosis, 24 337-368.

    Google Scholar 

  • Queller, D. C. (1992). Does population viscosity promote kin selection? Trends Ecol. Evol., 7 322-324.

    Article  Google Scholar 

  • Queller, D. C. (1994). Genetic relatedness in viscous populations. Evol. Ecol. Res., 8, 70-73.

    Article  Google Scholar 

  • Ratnieks, F. L. W., Monnin, T., and Foster, K. R. (2001). Inclusive fitness theory: Novel predictions and tests in eusocial Hymenoptera. Ann. Zool. Fennici, 38 201-214.

    Google Scholar 

  • Roche, P. F., Debelle, F., Maillet, F., Lerouge, P., Faucher, C., Dènariè, J., and Prome, J. C. (1991). Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell, 671131-1143.

    Article  PubMed  CAS  Google Scholar 

  • Rolfe, B. G., and Gresshoff, P. M. (1980). Rhizobium trifolii mutant interactions during the establishment of nodulation in white clover. Aust. J. Biol. Sci., 33 491-504.

    Google Scholar 

  • Schwartz, M. W., and Hoeksema, J. D. (1998). Specialization and resource trade: Biological markets as a model of mutualisms. Ecology, 79, 1029-1038.

    Article  Google Scholar 

  • Sheehy, J. E., Minchin, F. R., and Witty, J. F. (1983). Biological controls of the resistance to oxygen flux in nodules. Ann. Bot., 52 565-571.

    Google Scholar 

  • Simms, E. L., and Bever, J. D. (1998). Evolutionary dynamics of rhizopine within spatially structured rhizobium populations. Proc. Roy. Soc. LondonB, 265, 1713-1719.

    Google Scholar 

  • Simms, E. L., and Taylor, D. L. (2002). Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia. Integ. Comp. Biol., 42 369-380.

    Article  Google Scholar 

  • Singleton, P. W., and Stockinger, K. R. (1983). Compensation against ineffective nodulation in soybean. Crop Sci., 23 69-72.

    Article  Google Scholar 

  • Souza, V., Bain, J., Silva, C., Bouchet, V., Valera, A., Marquez, E., et al.(1997). Ethnomicrobiology: Do agricultural practices modify the population structure of the nitrogen fixing bacteria Rhizobium etlibiovar phaseoli. J. Ethnobiol., 17 249-266.

    Google Scholar 

  • Sprent, J. I., Sutherland, J. M., and de Faria, S. M. (1987). Some aspects of the biology of nitrogen-fixing organisms. Phil. Trans. Roy. Soc. LondonB, 317, 111-129.

    Article  Google Scholar 

  • Sprent, J. I. (2003). Mutual sanctions. Nature, 422 672-674.

    Article  PubMed  CAS  Google Scholar 

  • Taylor, P. D. (1992). Altruism in viscous populations - an inclusive fitness model. Evol. Ecol., 6 352-356.

    Article  Google Scholar 

  • Thornton, H. G. (1930). The influence of the host plant in inducing parasitism in lucerne and clover nodules. Proc. Roy. Soc. LondonB, 106, 110-122.

    Google Scholar 

  • Thrall, P. H., Burdon, J. J., and Woods, M. J. (2000). Variation in the effectiveness of symbiotic associations between native rhizobia and temperate Australian legumes: Interactions within and between genera. J. Appl. Ecol., 37 52-65.

    Article  Google Scholar 

  • Timmers, A. C. J., Soupene, E., Auriac, M. C., de Billy, F., Vasse, J., Boistard, P., et al.(2000). Saprophytic intracellular rhizobia in alfalfa nodules. Mol. Plant-Microbe Interact., 13 1204-1213.

    Article  PubMed  CAS  Google Scholar 

  • Trinick, M. J., Rhodes, R. L., and Galbraith, J. H. (1983). Competition between fast- and slow-growing tropical legume rhizobia for nodulation of Vigna unguiculata. Plant Soil, 73 105-115.

    Article  Google Scholar 

  • Udvardi, M. K., and Kahn, M. L. (1993). Evolution of the (Brady)Rhizobium-legume symbiosis: Why do bacteroids fix nitrogen? Symbiosis, 1487-101.

    Google Scholar 

  • Vance, C. P., Johnson, L. E. B., Halvorsen, A. M., Heichel, G. H., and Barnes, D. K. (1980). Histological and ultrastructural observations of Medicago sativa root nodule senescence after foliage removal. Can. J. Bot., 58 295-309.

    Google Scholar 

  • Vlassak, K. M., and Vanderleyden, J. (1997). Factors influencing nodule occupancy by inoculant rhizobia. Crit. Rev. Plant Sci., 16 163-229.

    Article  Google Scholar 

  • West, S. A., and Herre, E. A. (1994). The ecology of the New World fig parasitizing wasps Idarnes and implications for the evolution of the fig-pollinator mutualism. Proc. Roy. Soc. LondonB, 258, 67-72.

    Google Scholar 

  • West, S. A., Murray, M. G., Machado, C. A., Griffin, A. S., and Herre, E. A. (2001). Testing Hamilton’s rule with competition between relatives. Nature, 409 510-513.

    Article  PubMed  CAS  Google Scholar 

  • West, S. A., Kiers, E. T., Simms, E. L., and Denison, R. F. (2002a). Sanctions and mutualism stability: Why do rhizobia fix nitrogen? Proc. Roy. Soc. LondonB, 269, 685-694.

    Google Scholar 

  • West, S. A., Kiers, E. T., Pen, I., and Denison, R. F. (2002b). Sanctions and mutualism stability: When should less beneficial mutualists be tolerated? J. Evol. Biol., 15 830-837.

    Google Scholar 

  • Williams, G. C., and Nesse, R. M. (1991). The dawn of Darwinian medicine. Quart. Rev. Biol., 66 1-22.

    Article  PubMed  CAS  Google Scholar 

  • Wong, P. P., and Evans, H. J. (1971). Poly-β-hydroxybutyrate utilization by soybean (Glycine max Merr.) nodules and assessment of its role in maintenance of nitrogenase activity. Plant Physiol., 47, 750-755.

    PubMed  CAS  Google Scholar 

  • Yu, D. W. (2001). Parasites of mutualisms. Biol. J. Linn. Soc., 72 529-546.

    Article  Google Scholar 

  • Zhou, J. C., Tchan, Y. T., and Vincent, J. M. (1985). Reproductive capacity of bacteroids in nodules of Trifolium repens (L.) and Glycine max (L.) Merr. Planta, 163 473-482.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Kiers, E.T., West, S.K., Denison, R.F. (2008). Maintaining Cooperation in the Legume-Rhizobia Symbiosis: Identifying Selection Pressures and Mechanisms. In: Dilworth, M.J., James, E.K., Sprent, J.I., Newton, W.E. (eds) Nitrogen-fixing Leguminous Symbioses. Nitrogen Fixation: Origins, Applications, and Research Progress, vol 7. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-3548-7_3

Download citation

Publish with us

Policies and ethics