Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair
- Gregor Mendel Institute of Molecular Plant Biology, Austria
- Hospital Universitario Puerta de Hierro, Spain
- The Sainsbury Laboratory, University of East Anglia, United Kingdom
- Iwate Biotechnology Research Center, Japan
- 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.
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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.
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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.
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Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair
eLife 10:e71662.
https://doi.org/10.7554/eLife.71662
