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Soil nematodes mediate positive interactions between legume plants and rhizobium bacteria

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Abstract

Symbiosis between legume species and rhizobia results in the sequestration of atmospheric nitrogen into ammonium, and the early mechanisms involved in this symbiosis have become a model for plant-microbe interactions and thus highly amenable for agricultural applications. The working model for this interaction states that the symbiosis is the outcome of a chemical/molecular dialogue initiated by flavonoids produced by the roots of legumes and released into the soil as exudates, which specifically induce the synthesis of nodulation factors in rhizobia that initiate the nodulation process. Here, we argue that other organisms, such as the soil nematode Caenorhabditis elegans, also mediate the interaction between roots and rhizobia in a positive way, leading to nodulation. We report that C. elegans transfers the rhizobium species Sinorhizobium meliloti to the roots of the legume Medicago truncatula in response to plant-released volatiles that attract the nematode. These findings reveal a biologically-relevant and largely unknown interaction in the rhizosphere that is multitrophic and may control the initiation of the symbiosis.

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Acknowledgements

We thank Drs. Ray Fall and Lou Bjostad for scientific discussions on the subject and technical advice. We also thank Emily Wortman-Wunder for editorial assistance. JH acknowledges the financial support from Japan Society for the Promotion of Science. This work was supported by the Colorado State University Agricultural Experiment Station (JMV). JMV is an NSF-CAREER faculty fellow (MCB 0093014).

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Authors and Affiliations

  1. Department of Horticulture and Landscape Architecture, Colorado State University, 217 Shepardson Building, Fort Collins, CO, 80523, USA

    Jun-ichiro Horiuchi, Balakrishnan Prithiviraj, Harsh P. Bais & Jorge M. Vivanco

  2. Graduate Degree Program in Ecology, Colorado State University, Fort Collins, CO, 80523, USA

    Bruce A. Kimball & Jorge M. Vivanco

  3. Center for Rhizosphere Biology, Colorado State University, Fort Collins, CO, 80523, USA

    Jun-ichiro Horiuchi, Balakrishnan Prithiviraj, Harsh P. Bais & Jorge M. Vivanco

  4. United States Department of Agriculture, Wildlife Services, National Wildlife Research Center, Fort Collins, CO, 80521, USA

    Bruce A. Kimball

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  1. Jun-ichiro Horiuchi
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  2. Balakrishnan Prithiviraj
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  3. Harsh P. Bais
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Correspondence to Jorge M. Vivanco.

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Horiuchi, Ji., Prithiviraj, B., Bais, H.P. et al. Soil nematodes mediate positive interactions between legume plants and rhizobium bacteria. Planta 222, 848–857 (2005). https://doi.org/10.1007/s00425-005-0025-y

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