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FERONIA restricts Pseudomonas in the rhizosphere microbiome via regulation of reactive oxygen species

Nature Plants volume 7, pages 644–654 (2021)Cite this article

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Abstract

Maintaining microbiome structure is critical for the health of both plants and animals. By re-screening a collection of Arabidopsis mutants affecting root immunity and hormone crosstalk, we identified a FERONIA (FER) receptor kinase mutant (fer-8) with a rhizosphere microbiome enriched in Pseudomonas fluorescens without phylum-level dysbiosis. Using microbiome transplant experiments, we found that the fer-8 microbiome was beneficial. The effect of FER on rhizosphere pseudomonads was largely independent of its immune scaffold function, role in development and jasmonic acid autoimmunity. We found that the fer-8 mutant has reduced basal levels of reactive oxygen species (ROS) in roots and that mutants deficient in NADPH oxidase showed elevated rhizosphere pseudomonads. The addition of RALF23 peptides, a FER ligand, was sufficient to enrich P. fluorescens. This work shows that FER-mediated ROS production regulates levels of beneficial pseudomonads in the rhizosphere microbiome.

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Fig. 1: HSM13/FER inhibits rhizosphere Pseudomonas growth.
Fig. 2: Pseudomonadaceae are enriched in the rhizosphere microbiome of fer-8.
Fig. 3: The fer-8 microbiome is beneficial.
Fig. 4: Pseudomonas enrichment in fer-8 is largely independent of jasmonic acid signalling.
Fig. 5: FER regulates root ROS to control pseudomonads.
Fig. 6: RALF enriches Pseudomonas levels in the rhizosphere.

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Data availability

The microbiome sequencing data have been deposited in the National Center for Biotechnology Information BioProject database under accession PRJNA559927. The RNA-seq raw sequencing and analysed data have been deposited in the National Center for Biotechnology Information Gene Expression Omnibus database under accession GSE167143.

Code availability

The code related to microbiome sequencing and RNA-seq analysis is available from the Haney laboratory GitHub repository (https://github.com/haneylab/).

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Acknowledgements

We thank F. M. Ausubel for critical reading of the manuscript and generous provision of the hsm mutant collection; A. Y. Cheung, Z. Y. Wang, X. Li, Y. Zhang and G. Wasteneys for kindly providing seed stocks; and the laboratory of M. Hirst for assistance with sequencing. This work was supported by an NSERC Discovery Grant (NSERC-RGPIN-2016-04121) and Weston Seeding Food Innovation grants awarded to C.H.H. Y.S. was supported by a kick-start award from the Michael Smith Laboratories (UBC) and a fellowship from the Chinese Postdoctoral Science Foundation. Early stages of this work were supported by NIH R37 grant GM48707 and NSF grants MCB-0519898 and IOS-0929226 awarded to F. Ausubel.

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Author notes

  1. Xue-Cheng Zhang

    Present address: DermBiont, Boston, MA, USA

Authors and Affiliations

  1. Department of Microbiology and Immunology, The University of British Columbia, Vancouver, British Columbia, Canada

    Yi Song, Andrew J. Wilson, David Thoms, Siyu Song, Quentin Geissmann, Yang Liu, Lauren Walgren & Cara H. Haney

  2. Michael Smith Laboratories, The University of British Columbia, Vancouver, British Columbia, Canada

    Yi Song, David Thoms, Quentin Geissmann & Cara H. Haney

  3. Department of Molecular Biology, Massachusetts General Hospital, Boston, MA, USA

    Xue-Cheng Zhang

  4. Department of Genetics, Harvard Medical School, Boston, MA, USA

    Xue-Cheng Zhang

  5. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI, USA

    Reza Sohrabi & Sheng Yang He

  6. Department of Biology, Duke University, Durham, NC, USA

    Sheng Yang He

  7. Howard Hughes Medical Institute, Duke University, Durham, NC, USA

    Sheng Yang He

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Contributions

C.H.H. and Y.S. conceived of the project and designed the experiments. Y.S. performed the majority of experiments and data analysis. X.-C.Z. performed the previous hsm screen. A.J.W. analysed the RNA-seq and microbiome profiling data. D.T. conducted the confocal microscopy imaging. Q.G. performed statistical analysis for the expression of hormone-responsive genes and Pearson correlation assays. S.S., Y.L. and L.W. helped with the gnotobiotic plant assays. Experiments related to mfec were performed by R.S. with input from S.Y.H. C.H.H. and Y.S. wrote the manuscript with input from all authors.

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Correspondence to Cara H. Haney.

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Song, Y., Wilson, A.J., Zhang, XC. et al. FERONIA restricts Pseudomonas in the rhizosphere microbiome via regulation of reactive oxygen species. Nat. Plants 7, 644–654 (2021). https://doi.org/10.1038/s41477-021-00914-0

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