Article | Published:

Root microbiota drive direct integration of phosphate stress and immunity

Nature volume 543, pages 513518 (23 March 2017) | Download Citation

Abstract

Plants live in biogeochemically diverse soils with diverse microbiota. Plant organs associate intimately with a subset of these microbes, and the structure of the microbial community can be altered by soil nutrient content. Plant-associated microbes can compete with the plant and with each other for nutrients, but may also carry traits that increase the productivity of the plant. It is unknown how the plant immune system coordinates microbial recognition with nutritional cues during microbiome assembly. Here we establish that a genetic network controlling the phosphate stress response influences the structure of the root microbiome community, even under non-stress phosphate conditions. We define a molecular mechanism regulating coordination between nutrition and defence in the presence of a synthetic bacterial community. We further demonstrate that the master transcriptional regulators of phosphate stress response in Arabidopsis thaliana also directly repress defence, consistent with plant prioritization of nutritional stress over defence. Our work will further efforts to define and deploy useful microbes to enhance plant performance.

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Acknowledgements

Support by NSF INSPIRE grant IOS-1343020 and DOE-USDA Feedstock Award DE-SC001043 to J.L.D. S.H.P. was supported by NIH Training Grant T32 GM067553-06 and is a Howard Hughes Medical Institute International Student Research Fellow. P.J.P.L.T. was supported by The Pew Latin American Fellows Program in the Biomedical Sciences. J.L.D. is an Investigator of the Howard Hughes Medical Institute, supported by the HHMI and the Gordon and Betty Moore Foundation (GBMF3030). M.E.F. and O.M.F. are supported by NIH NRSA Fellowships F32-GM112345-02 and F32-GM117758-01, respectively. N.W.B. was supported by NIH NRSA Fellowship F32-GM103156. J.P.-A. is funded by the Spanish Ministry of Economy and Competitiveness (MINECO BIO2014-60453-R and EUI2008-03748). We thank S. Barth and E. Getzen for technical assistance, the Dangl laboratory microbiome group for useful discussions and S. Grant, D. Lundberg, F. El Kasmi, P. Schulze-Lefert and his colleagues for critical comments on the manuscript. Supplement contains additional data. Raw sequence data are available at the EBI Sequence Read Archive accession PRJEB15671 for microbiome 16S profiling, and at the Gene Expression Omnibus accessions GSE87339 for transcriptomic experiments. J.L.D. is a co-founder of, and shareholder in, and S.H.P. collaborates with, AgBiome LLC, a corporation whose goal is to use plant-associated microbes to improve plant productivity.

Author information

Author notes

    • Laura de Lorenzo
    •  & Natalie W. Breakfield

    Present addresses: NewLeaf Symbiotics, St. Louis, Missouri 63132, USA (N.W.B.); Department of Plant and Soil Sciences, University of Kentucky, Lexington, Kentucky 40546, USA (L.d.L.).

    • Gabriel Castrillo
    • , Paulo José Pereira Lima Teixeira
    •  & Sur Herrera Paredes

    These authors contributed equally to this work.

Affiliations

  1. Department of Biology, University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA

    • Gabriel Castrillo
    • , Paulo José Pereira Lima Teixeira
    • , Sur Herrera Paredes
    • , Theresa F. Law
    • , Meghan E. Feltcher
    • , Omri M. Finkel
    • , Natalie W. Breakfield
    • , Corbin D. Jones
    •  & Jeffery L. Dangl
  2. Howard Hughes Medical Institute, University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA

    • Gabriel Castrillo
    • , Paulo José Pereira Lima Teixeira
    • , Sur Herrera Paredes
    • , Theresa F. Law
    • , Meghan E. Feltcher
    • , Omri M. Finkel
    • , Natalie W. Breakfield
    •  & Jeffery L. Dangl
  3. Curriculum in Bioinformatics and Computational Biology, University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA

    • Sur Herrera Paredes
    • , Corbin D. Jones
    •  & Jeffery L. Dangl
  4. Department of Plant Molecular Genetics, Centro Nacional de Biotecnología, CNB-CSIC, Darwin 3, 28049 Madrid, Spain

    • Laura de Lorenzo
    •  & Javier Paz-Ares
  5. Department of Genetics, University of North Carolina, Chapel Hill, North Carolina, USA

    • Piotr Mieczkowski
    •  & Corbin D. Jones
  6. Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA

    • Piotr Mieczkowski
    •  & Corbin D. Jones
  7. Carolina Center for Genome Sciences, University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA

    • Piotr Mieczkowski
    • , Corbin D. Jones
    •  & Jeffery L. Dangl
  8. Curriculum in Genetics and Molecular Biology, University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA

    • Corbin D. Jones
    •  & Jeffery L. Dangl
  9. Department of Microbiology and Immunology, University of North Carolina, Chapel Hill, North Carolina 27599-3280, USA

    • Jeffery L. Dangl

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Contributions

G.C., P.J.P.L.T., S.H.P. and J.L.D. designed the project, G.C., S.H.P., T.F.L. and M.E.F. set up the experiments, collected samples and organized construction of 16S sequencing libraries. G.C. and T.F.L. performed control experiments related with PSR induced by the SynCom. G.C., N.W.B., M.E.F. and T.F.L. set up the experiments, collected samples and isolated RNA. P.J.P.L.T. organized, performed construction of RNA-seq libraries and analysed RNA-seq data. S.H.P. analysed 16S sequencing data. S.H.P. and P.J.P.L.T. oversaw data deposition. G.C., T.F.L. and P.J.P.L.T. performed pathology experiments. G.C., P.J.P.L.T., S.H.P., T.F.L., O.M.F. and J.L.D. analysed data and created figures. L.d.L. performed the ChIP–seq experiment. C.D.J. and P.M. advised on sequencing process and statistical methods. G.C., P.J.P.L.T., S.H.P. and J.L.D. wrote the manuscript with input from O.M.F., C.D.J. and J.P.-A.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Jeffery L. Dangl.

Reviewer Information Nature thanks P. Finnegan and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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https://doi.org/10.1038/nature21417

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