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Host sanctions and the legume–rhizobium mutualism

Nature volume 425, pages 78–81 (2003)Cite this article

Abstract

Explaining mutualistic cooperation between species remains one of the greatest problems for evolutionary biology1,2,3,4. Why do symbionts provide costly services to a host, indirectly benefiting competitors sharing the same individual host? Host monitoring of symbiont performance and the imposition of sanctions on ‘cheats’ could stabilize mutualism5,6. Here we show that soybeans penalize rhizobia that fail to fix N2 inside their root nodules. We prevented a normally mutualistic rhizobium strain from cooperating (fixing N2) by replacing air with an N2-free atmosphere (Ar:O2). A series of experiments at three spatial scales (whole plants, half root systems and individual nodules) demonstrated that forcing non-cooperation (analogous to cheating) decreased the reproductive success of rhizobia by about 50%. Non-invasive monitoring implicated decreased O2 supply as a possible mechanism for sanctions against cheating rhizobia. More generally, such sanctions by one or both partners may be important in stabilizing a wide range of mutualistic symbioses.

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Figure 1: Rhizobia fixing N2 grew to larger numbers in whole-plant and split-root experiments.
Figure 2: Rhizobia fixing N2 grew to larger numbers in the single-nodule experiment.
Figure 3: O2 relations in single nodules where rhizobia were allowed to fix (N2:O2) or prevented from fixing (Ar:O2) N2.
Figure 4: Nodule structure and the life history of rhizobia.

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Acknowledgements

We thank R. Grosberg, S. Nee, A. Griffin, D. Shuker and M. Stanton for comments, P. Graham, D. Phillips and M. King for advice on methods, R. Nelson and D. Smith for soybean cultivars ‘T243’ and ‘S0066’, and P. van Berkum for B. japonicum 110ARS. This work was supported by the NSF (grant to R.F.D. and graduate fellowship to E.T.K.), the California Agricultural Experiment Station, the Land Institute, the Royal Society, the BBSRC and the NERC.

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Authors and Affiliations

  1. Agronomy and Range Science, University of California, 1 Shields Avenue, California, 95616, Davis, USA

    E. Toby Kiers, Robert A. Rousseau & R. Ford Denison

  2. Institute of Cell, Animal & Population Biology, University of Edinburgh, King's Buildings, West Mains Road, EH9 3JT, Edinburgh, UK

    Stuart A. West

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Correspondence to R. Ford Denison.

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Kiers, E., Rousseau, R., West, S. et al. Host sanctions and the legume–rhizobium mutualism. Nature 425, 78–81 (2003). https://doi.org/10.1038/nature01931

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