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

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.

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.

Metrics

  • 1,850
    views
  • 425
    downloads
  • 35
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Juan Carlos De la Concepcion
  2. Javier Vega Benjumea
  3. Aleksandra Bialas
  4. Ryohei Terauchi
  5. Sophien Kamoun
  6. Mark J Banfield
(2021)
Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair
eLife 10:e71662.
https://doi.org/10.7554/eLife.71662

Share this article

https://doi.org/10.7554/eLife.71662

Further reading

    1. Plant Biology
    Maryam Rahmati Ishka, Hayley Sussman ... Magdalena M Julkowska
    Research Article

    Soil salinity is one of the major threats to agricultural productivity worldwide. Salt stress exposure alters root and shoots growth rates, thereby affecting overall plant performance. While past studies have extensively documented the effect of salt stress on root elongation and shoot development separately, here we take an innovative approach by examining the coordination of root and shoot growth under salt stress conditions. Utilizing a newly developed tool for quantifying the root:shoot ratio in agar-grown Arabidopsis seedlings, we found that salt stress results in a loss of coordination between root and shoot growth rates. We identify a specific gene cluster encoding domain-of-unknown-function 247 (DUF247), and characterize one of these genes as Salt Root:shoot Ratio Regulator Gene (SR3G). Further analysis elucidates the role of SR3G as a negative regulator of salt stress tolerance, revealing its function in regulating shoot growth, root suberization, and sodium accumulation. We further characterize that SR3G expression is modulated by WRKY75 transcription factor, known as a positive regulator of salt stress tolerance. Finally, we show that the salt stress sensitivity of wrky75 mutant is completely diminished when it is combined with sr3g mutation. Together, our results demonstrate that utilizing root:shoot ratio as an architectural feature leads to the discovery of a new stress resilience gene. The study’s innovative approach and findings not only contribute to our understanding of plant stress tolerance mechanisms but also open new avenues for genetic and agronomic strategies to enhance crop environmental resilience.

    1. Cell Biology
    2. Plant Biology
    Baihong Zhang, Shuqin Huang ... Wenli Chen
    Research Article

    Autophagy-related gene 6 (ATG6) plays a crucial role in plant immunity. Nonexpressor of pathogenesis-related genes 1 (NPR1) acts as a signaling hub of plant immunity. However, the relationship between ATG6 and NPR1 is unclear. Here, we find that ATG6 directly interacts with NPR1. ATG6 overexpression significantly increased nuclear accumulation of NPR1. Furthermore, we demonstrate that ATG6 increases NPR1 protein levels and improves its stability. Interestingly, ATG6 promotes the formation of SINCs (SA-induced NPR1 condensates)-like condensates. Additionally, ATG6 and NPR1 synergistically promote the expression of pathogenesis-related genes. Further results showed that silencing ATG6 in NPR1-GFP exacerbates Pst DC3000/avrRps4 infection, while double overexpression of ATG6 and NPR1 synergistically inhibits Pst DC3000/avrRps4 infection. In summary, our findings unveil an interplay of NPR1 with ATG6 and elucidate important molecular mechanisms for enhancing plant immunity.