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Amino-acid cycling drives nitrogen fixation in the legume–Rhizobium symbiosis

Nature volume 422, pages 722–726 (2003)Cite this article

Abstract

The biological reduction of atmospheric N2 to ammonium (nitrogen fixation) provides about 65% of the biosphere's available nitrogen. Most of this ammonium is contributed by legume–rhizobia symbioses1, which are initiated by the infection of legume hosts by bacteria (rhizobia), resulting in formation of root nodules. Within the nodules, rhizobia are found as bacteroids, which perform the nitrogen fixation: to do this, they obtain sources of carbon and energy from the plant, in the form of dicarboxylic acids2,3. It has been thought that, in return, bacteroids simply provide the plant with ammonium. But here we show that a more complex amino-acid cycle is essential for symbiotic nitrogen fixation by Rhizobium in pea nodules. The plant provides amino acids to the bacteroids, enabling them to shut down their ammonium assimilation. In return, bacteroids act like plant organelles to cycle amino acids back to the plant for asparagine synthesis. The mutual dependence of this exchange prevents the symbiosis being dominated by the plant, and provides a selective pressure for the evolution of mutualism.

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Figure 1: Effect of mutation of amino-acid uptake in R. leguminosarum on growth and nodulation of peas.
Figure 2: Growth and nodulation of peas infected by either wild type or a mutant unable to transport amino acids.
Figure 3: Nitrogen fixation and assimilation of peas infected by either wild type or a mutant unable to transport amino acids.
Figure 4: The role of amino-acid cycling in nitrogen fixation in pea nodules.

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Acknowledgements

We thank the BBSRC for supporting this research. We thank A. Hepburn and M. Heaps for GC-MS and nitrogen analysis and A. East for manuscript preparation.

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Author notes

  1. E. M. Lodwig, A. H. F. Hosie, K. Findlay and J. A. Downie: These authors contributed equally to this work

Authors and Affiliations

  1. School of Animal and Microbial Sciences, University of Reading, Whiteknights, PO Box 228, RG6 6AJ, Reading, UK

    E. M. Lodwig, A. H. F. Hosie, A. Bourdès, D. Allaway, R. Karunakaran & P. S. Poole

  2. John Innes Centre, Norwich, Colney Lane, NR4 7UH, UK

    K. Findlay & J. A. Downie

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  1. E. M. Lodwig
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  2. A. H. F. Hosie
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  3. A. Bourdès
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  4. K. Findlay
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  8. P. S. Poole
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Correspondence to P. S. Poole.

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Lodwig, E., Hosie, A., Bourdès, A. et al. Amino-acid cycling drives nitrogen fixation in the legume–Rhizobium symbiosis. Nature 422, 722–726 (2003). https://doi.org/10.1038/nature01527

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