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Plasma membrane association and resistosome formation of plant helper immune receptors

Intracellular plant immune receptors, termed NLRs (Nucleotide-binding Leucine-rich repeat Receptors), confer effector-triggered immunity. Sensor NLRs are responsible for pathogen effector recognition. Helper NLRs function downstream of sensor NLRs to transduce signaling and induce cell death and imm...

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Autores principales: Wang, Zaiqing, Liu, Xiaoxiao, Yu, Jie, Yin, Shuining, Cai, Wenjuan, Kim, Nak Hyun, El Kasmi, Farid, Dangl, Jeffery L., Wan, Li
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10410763/
https://www.ncbi.nlm.nih.gov/pubmed/37523563
http://dx.doi.org/10.1073/pnas.2222036120
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author Wang, Zaiqing
Liu, Xiaoxiao
Yu, Jie
Yin, Shuining
Cai, Wenjuan
Kim, Nak Hyun
El Kasmi, Farid
Dangl, Jeffery L.
Wan, Li
author_facet Wang, Zaiqing
Liu, Xiaoxiao
Yu, Jie
Yin, Shuining
Cai, Wenjuan
Kim, Nak Hyun
El Kasmi, Farid
Dangl, Jeffery L.
Wan, Li
author_sort Wang, Zaiqing
collection PubMed
description Intracellular plant immune receptors, termed NLRs (Nucleotide-binding Leucine-rich repeat Receptors), confer effector-triggered immunity. Sensor NLRs are responsible for pathogen effector recognition. Helper NLRs function downstream of sensor NLRs to transduce signaling and induce cell death and immunity. Activation of sensor NLRs that contain TIR (Toll/interleukin-1receptor) domains generates small molecules that induce an association between a downstream heterodimer signalosome of EDS1 (EnhancedDisease Susceptibility 1)/SAG101 (Senescence-AssociatedGene 101) and the helper NLR of NRG1 (NRequired Gene 1). Autoactive NRG1s oligomerize and form calcium signaling channels largely localized at the plasma membrane (PM). The molecular mechanisms of helper NLR PM association and effector-induced NRG1 oligomerization are not well characterized. We demonstrate that helper NLRs require positively charged residues in their N-terminal domains for phospholipid binding and PM association before and after activation, despite oligomerization and conformational changes that accompany activation. We demonstrate that effector activation of a TIR-containing sensor NLR induces NRG1 oligomerization at the PM and that the cytoplasmic pool of EDS1/SAG101 is critical for cell death function. EDS1/SAG101 cannot be detected in the oligomerized NRG1 resistosome, suggesting that additional unknown triggers might be required to induce the dissociation of EDS1/SAG101 from the previously described NRG1/EDS1/SAG101 heterotrimer before subsequent NRG1 oligomerization. Alternatively, the conformational changes resulting from NRG1 oligomerization abrogate the interface for EDS1/SAG101 association. Our data provide observations regarding dynamic PM association during helper NLR activation and underpin an updated model for effector-induced NRG1 resistosome formation.
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spelling pubmed-104107632023-08-10 Plasma membrane association and resistosome formation of plant helper immune receptors Wang, Zaiqing Liu, Xiaoxiao Yu, Jie Yin, Shuining Cai, Wenjuan Kim, Nak Hyun El Kasmi, Farid Dangl, Jeffery L. Wan, Li Proc Natl Acad Sci U S A Biological Sciences Intracellular plant immune receptors, termed NLRs (Nucleotide-binding Leucine-rich repeat Receptors), confer effector-triggered immunity. Sensor NLRs are responsible for pathogen effector recognition. Helper NLRs function downstream of sensor NLRs to transduce signaling and induce cell death and immunity. Activation of sensor NLRs that contain TIR (Toll/interleukin-1receptor) domains generates small molecules that induce an association between a downstream heterodimer signalosome of EDS1 (EnhancedDisease Susceptibility 1)/SAG101 (Senescence-AssociatedGene 101) and the helper NLR of NRG1 (NRequired Gene 1). Autoactive NRG1s oligomerize and form calcium signaling channels largely localized at the plasma membrane (PM). The molecular mechanisms of helper NLR PM association and effector-induced NRG1 oligomerization are not well characterized. We demonstrate that helper NLRs require positively charged residues in their N-terminal domains for phospholipid binding and PM association before and after activation, despite oligomerization and conformational changes that accompany activation. We demonstrate that effector activation of a TIR-containing sensor NLR induces NRG1 oligomerization at the PM and that the cytoplasmic pool of EDS1/SAG101 is critical for cell death function. EDS1/SAG101 cannot be detected in the oligomerized NRG1 resistosome, suggesting that additional unknown triggers might be required to induce the dissociation of EDS1/SAG101 from the previously described NRG1/EDS1/SAG101 heterotrimer before subsequent NRG1 oligomerization. Alternatively, the conformational changes resulting from NRG1 oligomerization abrogate the interface for EDS1/SAG101 association. Our data provide observations regarding dynamic PM association during helper NLR activation and underpin an updated model for effector-induced NRG1 resistosome formation. National Academy of Sciences 2023-07-31 2023-08-08 /pmc/articles/PMC10410763/ /pubmed/37523563 http://dx.doi.org/10.1073/pnas.2222036120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Wang, Zaiqing
Liu, Xiaoxiao
Yu, Jie
Yin, Shuining
Cai, Wenjuan
Kim, Nak Hyun
El Kasmi, Farid
Dangl, Jeffery L.
Wan, Li
Plasma membrane association and resistosome formation of plant helper immune receptors
title Plasma membrane association and resistosome formation of plant helper immune receptors
title_full Plasma membrane association and resistosome formation of plant helper immune receptors
title_fullStr Plasma membrane association and resistosome formation of plant helper immune receptors
title_full_unstemmed Plasma membrane association and resistosome formation of plant helper immune receptors
title_short Plasma membrane association and resistosome formation of plant helper immune receptors
title_sort plasma membrane association and resistosome formation of plant helper immune receptors
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10410763/
https://www.ncbi.nlm.nih.gov/pubmed/37523563
http://dx.doi.org/10.1073/pnas.2222036120
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