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

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...

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Autores principales:	Juan Carlos De la Concepcion, Javier Vega Benjumea, Aleksandra Bialas, Ryohei Terauchi, Sophien Kamoun, Mark J Banfield
Formato:	article
Lenguaje:	EN
Publicado:	eLife Sciences Publications Ltd 2021
Materias:	plant immunity effectors NLR hybrid necrosis evolution Medicine R Science Q Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/6058f1abd2ea48d89e24caf824a7b030
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spelling	oai:doaj.org-article:6058f1abd2ea48d89e24caf824a7b0302021-11-30T11:56:35ZFunctional diversification gave rise to allelic specialization in a rice NLR immune receptor pair10.7554/eLife.716622050-084Xe71662https://doaj.org/article/6058f1abd2ea48d89e24caf824a7b0302021-11-01T00:00:00Zhttps://elifesciences.org/articles/71662https://doaj.org/toc/2050-084XCooperation 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.Juan Carlos De la ConcepcionJavier Vega BenjumeaAleksandra BialasRyohei TerauchiSophien KamounMark J BanfieldeLife Sciences Publications Ltdarticleplant immunityeffectorsNLRhybrid necrosisevolutionMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	plant immunity effectors NLR hybrid necrosis evolution Medicine R Science Q Biology (General) QH301-705.5
spellingShingle	plant immunity effectors NLR hybrid necrosis evolution Medicine R Science Q Biology (General) QH301-705.5 Juan Carlos De la Concepcion Javier Vega Benjumea Aleksandra Bialas Ryohei Terauchi Sophien Kamoun Mark J Banfield Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair
description	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.
format	article
author	Juan Carlos De la Concepcion Javier Vega Benjumea Aleksandra Bialas Ryohei Terauchi Sophien Kamoun Mark J Banfield
author_facet	Juan Carlos De la Concepcion Javier Vega Benjumea Aleksandra Bialas Ryohei Terauchi Sophien Kamoun Mark J Banfield
author_sort	Juan Carlos De la Concepcion
title	Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair
title_short	Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair
title_full	Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair
title_fullStr	Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair
title_full_unstemmed	Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair
title_sort	functional diversification gave rise to allelic specialization in a rice nlr immune receptor pair
publisher	eLife Sciences Publications Ltd
publishDate	2021
url	https://doaj.org/article/6058f1abd2ea48d89e24caf824a7b030
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_version_	1718406624080560128

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

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