1. Microbiology and Infectious Disease
  2. Plant Biology

Oomycete small RNAs bind to the plant RNA-induced silencing complex for virulence

  1. Florian Dunker
  2. Adriana Trutzenberg
  3. Jan S Rothenpieler
  4. Sarah Kuhn
  5. Reinhard Pröls
  6. Tom Schreiber
  7. Alain Tissier
  8. Ariane Kemen
  9. Eric Kemen
  10. Ralph Hückelhoven
  11. Arne Weiberg  Is a corresponding author
  1. Ludwig Maximilian University of Munich, Germany
  2. Technical University of Munich, Germany
  3. Leibniz Institute of Plant Biochemistry, Germany
  4. University of Tübingen, Germany
https://doi.org/10.7554/eLife.56096
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  1. Florian Dunker
  2. Adriana Trutzenberg
  3. Jan S Rothenpieler
  4. Sarah Kuhn
  5. Reinhard Pröls
  6. Tom Schreiber
  7. Alain Tissier
  8. Ariane Kemen
  9. Eric Kemen
  10. Ralph Hückelhoven
  11. Arne Weiberg
(2020)
Oomycete small RNAs bind to the plant RNA-induced silencing complex for virulence
eLife 9:e56096.
https://doi.org/10.7554/eLife.56096
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Abstract

The exchange of small RNAs (sRNAs) between hosts and pathogens can lead to gene silencing in the recipient organism, a mechanism termed cross-kingdom RNAi (ck-RNAi). While fungal sRNAs promoting virulence are established, the significance of ck-RNAi in distinct plant pathogens is not clear. Here, we describe that sRNAs of the pathogen Hyaloperonospora arabidopsidis, which represents the kingdom of oomycetes and is phylogenetically distant from fungi, employ the host plant's Argonaute (AGO)/RNA-induced silencing complex for virulence. To demonstrate H. arabidopsidis sRNA (HpasRNA) functionality in ck-RNAi, we designed a novel CRISPR endoribonuclease Csy4/GUS reporter that enabled in situ visualization of HpasRNA-induced target suppression in Arabidopsis. The significant role of HpasRNAs together with AtAGO1 in virulence was revealed in plant atago1 mutants and by transgenic Arabidopsis expressing a short-tandem-target-mimic to block HpasRNAs, that both exhibited enhanced resistance. HpasRNA-targeted plant genes contributed to host immunity, as Arabidopsis gene knockout mutants displayed quantitative enhanced susceptibility.

Data availability

Sequencing data have been deposited in NCBI SRA (PRJNA395139).

The following data sets were generated

Article and author information

Author details

  1. Florian Dunker

    Genetics, Ludwig Maximilian University of Munich, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.

  2. Adriana Trutzenberg

    Genetics, Ludwig Maximilian University of Munich, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.

  3. Jan S Rothenpieler

    Genetics, Ludwig Maximilian University of Munich, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8892-8230

  4. Sarah Kuhn

    Genetics, Ludwig Maximilian University of Munich, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.

  5. Reinhard Pröls

    Phytopathology, School of Life Sciences Weihenstephan, Technical University of Munich, Freising, Germany
    Competing interests
    The authors declare that no competing interests exist.

  6. Tom Schreiber

    Department of Cell and Metabolic Biology, Leibniz Institute of Plant Biochemistry, Halle, Germany
    Competing interests
    The authors declare that no competing interests exist.

  7. Alain Tissier

    Department of Cell and Metabolic Biology, Leibniz Institute of Plant Biochemistry, Halle, Germany
    Competing interests
    The authors declare that no competing interests exist.

  8. Ariane Kemen

    Center for Plant Molecular Biology, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  9. Eric Kemen

    Center for Plant Molecular Biology, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  10. Ralph Hückelhoven

    Center for Plant Molecular BiologyPlant Biochemistry, Technical University of Munich, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.

  11. Arne Weiberg

    Genetics, Ludwig Maximilian University of Munich, Martinsried, Germany
    For correspondence
    a.weiberg@lmu.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4300-4864

Funding

Deutsche Forschungsgemeinschaft (WE 5707/1-1)

  • Arne Weiberg

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Axel A Brakhage, Hans Knöll Institute, Germany

Version history

  1. Received: February 17, 2020
  2. Accepted: May 21, 2020
  3. Accepted Manuscript published: May 22, 2020 (version 1)
  4. Accepted Manuscript updated: May 26, 2020 (version 2)
  5. Version of Record published: June 16, 2020 (version 3)

Copyright

© 2020, Dunker et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Florian Dunker
  2. Adriana Trutzenberg
  3. Jan S Rothenpieler
  4. Sarah Kuhn
  5. Reinhard Pröls
  6. Tom Schreiber
  7. Alain Tissier
  8. Ariane Kemen
  9. Eric Kemen
  10. Ralph Hückelhoven
  11. Arne Weiberg
(2020)
Oomycete small RNAs bind to the plant RNA-induced silencing complex for virulence
eLife 9:e56096.
https://doi.org/10.7554/eLife.56096

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