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Associations with rhizosphere bacteria can confer an adaptive advantage to plants

Nature Plants volume 1, Article number: 15051 (2015) Cite this article

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Abstract

Host-associated microbiomes influence host health. However, it is unclear whether genotypic variations in host organisms influence the microbiome in ways that have adaptive consequences for the host. Here, we show that wild accessions of Arabidopsis thaliana differ in their ability to associate with the root-associated bacterium Pseudomonas fluorescens, with consequences for plant fitness. In a screen of 196 naturally occurring Arabidopsis accessions we identified lines that actively suppress Pseudomonas growth under gnotobiotic conditions. We planted accessions that support disparate levels of fluorescent Pseudomonads in natural soils; 16S ribosomal RNA sequencing revealed that accession-specific differences in the microbial communities were largely limited to a subset of Pseudomonadaceae species. These accession-specific differences in Pseudomonas growth resulted in enhanced or impaired fitness that depended on the host’s ability to support Pseudomonas growth, the specific Pseudomonas strains present in the soil and the nature of the stress. We suggest that small host-mediated changes in a microbiome can have large effects on host health.

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Figure 1: Natural variation in Arabidopsis affects growth of Pseudomonas in the rhizosphere.
Figure 2: The effect of Arabidopsis genotype is largely limited to OTUs in the family Pseudomonadaceae.
Figure 3: Incompatible Arabidopsis accessions actively inhibit growth of Pseudomonas.
Figure 4: Pseudomonas strains do not promote the growth of incompatible accessions.
Figure 5: Addition of Pseudomonas has a minor but significant effect on soil and rhizosphere community composition.
Figure 6: Disease outcome depends on host genotype, the Pseudomonas strain present and the pathogen.

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Acknowledgements

C.H.H. is funded by MGH Toteston and Fund for Medical Discovery Fellowship grant 2014A051303 and previously by the Gordon and Betty Moore Foundation through Grant GBMF 2550.01 to the Life Sciences Research Foundation. B.S.S. was funded by a Charles King Trust Sr. Postdoctoral Fellowship. This work was supported by NIH R37 grant GM48707 and NSF grants MCB-0519898 and IOS-0929226 awarded to F.M.A. We thank J. Meyer, D. McEwan, J. Griffitts and L. Shapiro for critical reading of the manuscript and A. Diener and members of the Ausubel Lab for helpful comments and discussion.

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  1. Buck S. Samuel

    Present address: †Present address: Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas 77030, USA.,

Authors and Affiliations

  1. Department of Genetics, Harvard Medical School, Boston, 02114, Massachusetts, USA

    Cara H. Haney, Buck S. Samuel & Frederick M. Ausubel

  2. Department of Molecular Biology, Massachusetts General Hospital, Boston, 02114, Massachusetts, USA

    Cara H. Haney, Buck S. Samuel, Jenifer Bush & Frederick M. Ausubel

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Contributions

C.H.H. and F.M.A. conceived experiments and discussed results. C.H.H. and J.B. designed assays and performed experiments. B.S.S. and C.H.H. analysed data. C.H.H. wrote the manuscript with input from F.M.A., J.B. and B.S.S.

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Correspondence to Frederick M. Ausubel.

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Haney, C., Samuel, B., Bush, J. et al. Associations with rhizosphere bacteria can confer an adaptive advantage to plants. Nature Plants 1, 15051 (2015). https://doi.org/10.1038/nplants.2015.51

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