1. Plant Biology
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Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair

  1. Juan Carlos De la Concepcion  Is a corresponding author
  2. Javier Vega Benjumea
  3. Aleksandra Bialas
  4. Ryohei Terauchi
  5. Sophien Kamoun
  6. Mark J Banfield  Is a corresponding author
  1. Gregor Mendel Institute of Molecular Plant Biology, Austria
  2. Hospital Universitario Puerta de Hierro, Spain
  3. The Sainsbury Laboratory, University of East Anglia, United Kingdom
  4. Iwate Biotechnology Research Center, Japan
  5. John Innes Centre, United Kingdom
Research Article
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Cite this article as: eLife 2021;10:e71662 doi: 10.7554/eLife.71662

Abstract

Cooperation between receptors from the NLR superfamily is important for intracellular activation of immune responses. NLRs can function in pairs that, upon pathogen recognition, trigger hypersensitive cell death and stop pathogen invasion. Natural selection drives specialization of host immune receptors towards an optimal response, whilst keeping a tight regulation of immunity in the absence of pathogens. However, the molecular basis of co-adaptation and specialization between paired NLRs remains largely unknown. Here, we describe functional specialization in alleles of the rice NLR pair Pik that confers resistance to strains of the blast fungus Magnaporthe oryzae harbouring AVR-Pik effectors. We revealed that matching pairs of allelic Pik NLRs mount effective immune responses whereas mismatched pairs lead to autoimmune phenotypes, a hallmark of hybrid necrosis in both natural and domesticated plant populations. We further showed that allelic specialization is largely underpinned by a single amino acid polymorphism that determines preferential association between matching pairs of Pik NLRs. These results provide a framework for how functionally linked immune receptors undergo co-adaptation to provide an effective and regulated immune response against pathogens. Understanding the molecular constraints that shape paired NLR evolution has implications beyond plant immunity given that hybrid necrosis can drive reproductive isolation.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Plots and Blots.

Article and author information

Author details

  1. Juan Carlos De la Concepcion

    Gregor Mendel Institute of Molecular Plant Biology, Vienna, Austria
    For correspondence
    juan.concepcion@gmi.oeaw.ac.at
    Competing interests
    No competing interests declared.
  2. Javier Vega Benjumea

    Servicio de Bioquímica-Análisis clínicos, Hospital Universitario Puerta de Hierro, Madrid, Spain
    Competing interests
    No competing interests declared.
  3. Aleksandra Bialas

    The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom
    Competing interests
    No competing interests declared.
  4. Ryohei Terauchi

    Division of Genomics and Breeding, Iwate Biotechnology Research Center, Iwate, Japan
    Competing interests
    No competing interests declared.
  5. Sophien Kamoun

    The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom
    Competing interests
    Sophien Kamoun, SK receives funding from industry on NLR biology.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0290-0315
  6. Mark J Banfield

    Department of Biological Chemistry, John Innes Centre, Norwich, United Kingdom
    For correspondence
    Mark.banfield@jic.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8921-3835

Funding

Biotechnology and Biological Sciences Research Council (BB/012574)

  • Sophien Kamoun
  • Mark J Banfield

Biotechnology and Biological Sciences Research Council (BBS/E/J/000PR9795)

  • Sophien Kamoun
  • Mark J Banfield

Biotechnology and Biological Sciences Research Council (BB/M011216/1,project reference 1771322)

  • Aleksandra Bialas

ERC Horizon 2020 (743165)

  • Sophien Kamoun
  • Mark J Banfield

John Innes Foundation

  • Juan Carlos De la Concepcion

Gatsby Charitable Foundation

  • Sophien Kamoun

Erasmus+

  • Javier Vega Benjumea

Japan Society for the Promotion of Science (20H05681)

  • Ryohei Terauchi

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: June 25, 2021
  2. Accepted: November 15, 2021
  3. Accepted Manuscript published: November 16, 2021 (version 1)

Copyright

© 2021, De la Concepcion 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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