Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism

  1. Isabel ML Saur
  2. Saskia Bauer
  3. Barbara Kracher
  4. Xunli Lu
  5. Lamprinos Franzeskakis
  6. Marion C Müller
  7. Björn Sabelleck
  8. Florian Kümmel
  9. Ralph Panstruga
  10. Takaki Maekawa
  11. Paul Schulze-Lefert  Is a corresponding author
  1. Max Planck Institute for Plant Breeding Research, Germany
  2. China Agricultural University, China
  3. RWTH Aachen University, Germany
  4. University of Zurich, Switzerland

Abstract

Nucleotide-binding domain and leucine-rich repeat (NLR)-containing proteins in plants and animals mediate intracellular pathogen-sensing. Plant NLRs typically detect strain-specific pathogen effectors and trigger immune responses often linked to localized host cell death. The barley Mla disease resistance locus has undergone extensive functional diversification in the host population and encodes numerous allelic NLRs each detecting a matching isolate-specific avirulence effector (AVRA) of the fungal pathogen Blumeria graminis f. sp. hordei (Bgh). We report here the isolation of Bgh AVRa7, AVRa9, AVRa10, and AVRa22, which encode small secreted proteins recognized by allelic MLA7, MLA9, MLA10, and MLA22 receptors, respectively. These effectors are sequence-unrelated, except for allelic AVRa10 and AVRa22 that are co-maintained in pathogen populations in the form of a balanced polymorphism. Contrary to numerous examples of indirect recognition of bacterial effectors by plant NLRs, co-expression experiments with matching Mla-AVRa pairs indicate direct detection of the sequence-unrelated fungal effectors by MLA receptors.

Data availability

RNA sequencing data have been deposited in GEO under accession code GSE110266 and improved Blumeria graminis f.sp. hordei isolate K1 assembly is deposited under the accession number PRJEB30373 at EBI-ENA. All data generated or analysed during this study are included in the manuscript and supporting files.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Isabel ML Saur

    Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Saskia Bauer

    Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4559-5063
  3. Barbara Kracher

    Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Xunli Lu

    Department of Plant Pathology, China Agricultural University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Lamprinos Franzeskakis

    Institute for Biology I, Unit of Plant Molecular Cell Biology, RWTH Aachen University, Aachen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Marion C Müller

    Department of Plant and Microbial Biology, University of Zurich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5594-2319
  7. Björn Sabelleck

    Institute for Biology I, Unit of Plant Molecular Cell Biology, RWTH Aachen University, Aachen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Florian Kümmel

    Institute for Biology I, Unit of Plant Molecular Cell Biology, RWTH Aachen University, Aachen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Ralph Panstruga

    Institute for Biology I, Unit of Plant Molecular Cell Biology, RWTH Aachen University, Aachen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3756-8957
  10. Takaki Maekawa

    Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  11. Paul Schulze-Lefert

    Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    For correspondence
    schlef@mpipz.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8978-1717

Funding

Deutsche Forschungsgemeinschaft (SFB670)

  • Barbara Kracher
  • Takaki Maekawa
  • Paul Schulze-Lefert

Max-Planck-Gesellschaft (Open-access funding)

  • Saskia Bauer
  • Paul Schulze-Lefert

European Molecular Biology Organization (ALTF 368-2016)

  • Isabel ML Saur

Cluster of Excellence in Plant Sciences (CEPLAS)

  • Paul Schulze-Lefert

Deutsche Forschungsgemeinschaft (SPP1819)

  • Lamprinos Franzeskakis
  • Ralph Panstruga

Daimler und Benz Stiftung

  • Isabel ML Saur

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

Reviewing Editor

  1. Thorsten Nürnberger, University of Tübingen, Germany

Publication history

  1. Received: December 17, 2018
  2. Accepted: February 13, 2019
  3. Accepted Manuscript published: February 19, 2019 (version 1)
  4. Version of Record published: March 12, 2019 (version 2)

Copyright

© 2019, Saur 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. Isabel ML Saur
  2. Saskia Bauer
  3. Barbara Kracher
  4. Xunli Lu
  5. Lamprinos Franzeskakis
  6. Marion C Müller
  7. Björn Sabelleck
  8. Florian Kümmel
  9. Ralph Panstruga
  10. Takaki Maekawa
  11. Paul Schulze-Lefert
(2019)
Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism
eLife 8:e44471.
https://doi.org/10.7554/eLife.44471

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