Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair

De La Concepcion, Juan Carlos, Vega Benjumea, Javier, Bialas, Aleksandra, Terauchi, Ryohei, Kamoun, Sophien ORCID: https://orcid.org/0000-0002-0290-0315 and Banfield, Mark J. (2021) Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair. eLife, 10. ISSN 2050-084X

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Abstract

Cooperation between receptors from the nucleotide-binding, leucine-rich repeats (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.

Item Type: Article
Additional Information: Funding Information: We thank present and former members of the Banfield and Kamoun laboratories for discussions that have shaped this manuscript, and colleagues at Iwate Biotechnology Research Center for stimulating discussions on NLR biology. We specially thank Dr. Cristina Barragan and Dr. Adam Bentham for critical reading of the manuscript. We also thank Andrew Davies and Phil Robinson from JIC Scientific Photography for the UV pictures of the cell death assays. This work was supported by the Biotechnology and Biological Sciences Research Council (BBSRC, UK, grant BB/012574, BBS/E/J/000PR9795), the BBSRC Doctoral Training Partnership at Norwich Research Park (grant: BB/M011216/1, project reference 1771322), the European Research Council (proposal 743165), the John Innes Foundation, the Gatsby Charitable Foundation, the European Commission through the Erasmus+ programme, and JSPS Grant 20H05681. Publisher Copyright: © De la Concepcion et al.
Uncontrolled Keywords: neuroscience(all),biochemistry, genetics and molecular biology(all),immunology and microbiology(all) ,/dk/atira/pure/subjectarea/asjc/2800
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 20 Nov 2021 01:40
Last Modified: 23 Oct 2022 03:21
URI: https://ueaeprints.uea.ac.uk/id/eprint/82247
DOI: 10.7554/eLife.71662

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