An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species

  1. Hiroaki Adachi
  2. Mauricio Contreras
  3. Adeline Harant
  4. Chih-hang Wu
  5. Lida Derevnina
  6. Toshiyuki Sakai
  7. Cian Duggan
  8. Eleonora Moratto
  9. Tolga O Bozkurt
  10. Abbas Maqbool
  11. Joe Win
  12. Sophien Kamoun  Is a corresponding author
  1. The Sainsbury Laboratory, University of East Anglia, United Kingdom
  2. Imperial College London, United Kingdom

Abstract

The molecular codes underpinning the functions of plant NLR immune receptors are poorly understood. We used in vitro Mu transposition to generate a random truncation library and identify the minimal functional region of NLRs. We applied this method to NRC4—a helper NLR that functions with multiple sensor NLRs within a Solanaceae receptor network. This revealed that the NRC4 N-terminal 29 amino acids are sufficient to induce hypersensitive cell death. This region is defined by the consensus MADAxVSFxVxKLxxLLxxEx (MADA motif) that is conserved at the N-termini of NRC family proteins and ~20% of coiled-coil (CC)-type plant NLRs. The MADA motif matches the N-terminal a1 helix of Arabidopsis NLR protein ZAR1, which undergoes a conformational switch during resistosome activation. Immunoassays revealed that the MADA motif is functionally conserved across NLRs from distantly related plant species. NRC-dependent sensor NLRs lack MADA sequences indicating that this motif has degenerated in sensor NLRs over evolutionary time.

Data availability

All sequence data used for bioinformatic and phylogenetic analyses are included in the manuscript and supporting files

The following previously published data sets were used

Article and author information

Author details

  1. Hiroaki Adachi

    The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7184-744X
  2. Mauricio Contreras

    The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  3. Adeline Harant

    The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  4. Chih-hang Wu

    The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom
    Competing interests
    Chih-hang Wu, SK, LD and CH-W filed a patent on NRCs.(WO/2019/108619).
  5. Lida Derevnina

    The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom
    Competing interests
    Lida Derevnina, SK, LD and CH-W filed a patent on NRCs. (WO/2019/108619).
  6. Toshiyuki Sakai

    The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  7. Cian Duggan

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7302-7472
  8. Eleonora Moratto

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    No competing interests declared.
  9. Tolga O Bozkurt

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0507-6875
  10. Abbas Maqbool

    The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  11. Joe Win

    The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  12. Sophien Kamoun

    The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom
    For correspondence
    sophien.kamoun@tsl.ac.uk
    Competing interests
    Sophien Kamoun, SK, LD and CH-W filed a patent on NRCs. SK receives funding from industry on NLR biology.(WO/2019/108619).
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0290-0315

Funding

Gatsby Charitable Foundation

  • Sophien Kamoun

Biotechnology and Biological Sciences Research Council

  • Sophien Kamoun

European Research Council

  • Sophien Kamoun

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

Reviewing Editor

  1. Jian-Min Zhou, Chinese Academy of Sciences, China

Publication history

  1. Received: July 9, 2019
  2. Accepted: November 23, 2019
  3. Accepted Manuscript published: November 27, 2019 (version 1)
  4. Version of Record published: January 6, 2020 (version 2)

Copyright

© 2019, Adachi 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. Hiroaki Adachi
  2. Mauricio Contreras
  3. Adeline Harant
  4. Chih-hang Wu
  5. Lida Derevnina
  6. Toshiyuki Sakai
  7. Cian Duggan
  8. Eleonora Moratto
  9. Tolga O Bozkurt
  10. Abbas Maqbool
  11. Joe Win
  12. Sophien Kamoun
(2019)
An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species
eLife 8:e49956.
https://doi.org/10.7554/eLife.49956

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