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A G-type lectin receptor kinase negatively regulates Arabidopsis immunity against root-knot nematodes

Root-knot nematodes (Meloidogyne spp., RKN) are responsible for extensive crop losses worldwide. During infection, they penetrate plant roots, migrate between plant cells, and establish feeding sites, known as giant cells, near the root vasculature. Previously, we found that nematode perception and...

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Autores principales: Zhou, Dongmei, Godinez-Vidal, Damaris, He, Jiangman, Teixeira, Marcella, Guo, Jingzhe, Wei, Lihui, Van Norman, Jaimie M, Kaloshian, Isgouhi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469371/
https://www.ncbi.nlm.nih.gov/pubmed/37103588
http://dx.doi.org/10.1093/plphys/kiad253
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author Zhou, Dongmei
Godinez-Vidal, Damaris
He, Jiangman
Teixeira, Marcella
Guo, Jingzhe
Wei, Lihui
Van Norman, Jaimie M
Kaloshian, Isgouhi
author_facet Zhou, Dongmei
Godinez-Vidal, Damaris
He, Jiangman
Teixeira, Marcella
Guo, Jingzhe
Wei, Lihui
Van Norman, Jaimie M
Kaloshian, Isgouhi
author_sort Zhou, Dongmei
collection PubMed
description Root-knot nematodes (Meloidogyne spp., RKN) are responsible for extensive crop losses worldwide. During infection, they penetrate plant roots, migrate between plant cells, and establish feeding sites, known as giant cells, near the root vasculature. Previously, we found that nematode perception and early responses in plants were similar to those of microbial pathogens and required the BRI1-ASSOCIATED KINASE1/SOMATIC EMBRYOGENESIS RECEPTOR KINASE3 (BAK1/SERK3) coreceptor in Arabidopsis (Arabidopsis thaliana) and tomato (Solanum lycopersicum). Here, we implemented a reverse genetic screen for resistance or sensitivity to RKN using Arabidopsis T-DNA alleles of genes encoding transmembrane receptor–like kinases to identify additional receptors involved in this process. This screen identified a pair of allelic mutations with enhanced resistance to RKN in a gene we named ENHANCED RESISTANCE TO NEMATODES1 (ERN1). ERN1 encodes a G-type lectin receptor kinase (G-LecRK) with a single-pass transmembrane domain. Further characterization showed that ern1 mutants displayed stronger activation of MAP kinases, elevated levels of the defense marker MYB51, and enhanced H(2)O(2) accumulation in roots upon RKN elicitor treatments. Elevated MYB51 expression and ROS bursts were also observed in leaves of ern1 mutants upon flg22 treatment. Complementation of ern1.1 with 35S- or native promoter–driven ERN1 rescued the RKN infection and enhanced defense phenotypes. Our results indicate that ERN1 is an important negative regulator of immunity.
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spelling pubmed-104693712023-09-01 A G-type lectin receptor kinase negatively regulates Arabidopsis immunity against root-knot nematodes Zhou, Dongmei Godinez-Vidal, Damaris He, Jiangman Teixeira, Marcella Guo, Jingzhe Wei, Lihui Van Norman, Jaimie M Kaloshian, Isgouhi Plant Physiol Research Article Root-knot nematodes (Meloidogyne spp., RKN) are responsible for extensive crop losses worldwide. During infection, they penetrate plant roots, migrate between plant cells, and establish feeding sites, known as giant cells, near the root vasculature. Previously, we found that nematode perception and early responses in plants were similar to those of microbial pathogens and required the BRI1-ASSOCIATED KINASE1/SOMATIC EMBRYOGENESIS RECEPTOR KINASE3 (BAK1/SERK3) coreceptor in Arabidopsis (Arabidopsis thaliana) and tomato (Solanum lycopersicum). Here, we implemented a reverse genetic screen for resistance or sensitivity to RKN using Arabidopsis T-DNA alleles of genes encoding transmembrane receptor–like kinases to identify additional receptors involved in this process. This screen identified a pair of allelic mutations with enhanced resistance to RKN in a gene we named ENHANCED RESISTANCE TO NEMATODES1 (ERN1). ERN1 encodes a G-type lectin receptor kinase (G-LecRK) with a single-pass transmembrane domain. Further characterization showed that ern1 mutants displayed stronger activation of MAP kinases, elevated levels of the defense marker MYB51, and enhanced H(2)O(2) accumulation in roots upon RKN elicitor treatments. Elevated MYB51 expression and ROS bursts were also observed in leaves of ern1 mutants upon flg22 treatment. Complementation of ern1.1 with 35S- or native promoter–driven ERN1 rescued the RKN infection and enhanced defense phenotypes. Our results indicate that ERN1 is an important negative regulator of immunity. Oxford University Press 2023-04-27 /pmc/articles/PMC10469371/ /pubmed/37103588 http://dx.doi.org/10.1093/plphys/kiad253 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Zhou, Dongmei
Godinez-Vidal, Damaris
He, Jiangman
Teixeira, Marcella
Guo, Jingzhe
Wei, Lihui
Van Norman, Jaimie M
Kaloshian, Isgouhi
A G-type lectin receptor kinase negatively regulates Arabidopsis immunity against root-knot nematodes
title A G-type lectin receptor kinase negatively regulates Arabidopsis immunity against root-knot nematodes
title_full A G-type lectin receptor kinase negatively regulates Arabidopsis immunity against root-knot nematodes
title_fullStr A G-type lectin receptor kinase negatively regulates Arabidopsis immunity against root-knot nematodes
title_full_unstemmed A G-type lectin receptor kinase negatively regulates Arabidopsis immunity against root-knot nematodes
title_short A G-type lectin receptor kinase negatively regulates Arabidopsis immunity against root-knot nematodes
title_sort g-type lectin receptor kinase negatively regulates arabidopsis immunity against root-knot nematodes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469371/
https://www.ncbi.nlm.nih.gov/pubmed/37103588
http://dx.doi.org/10.1093/plphys/kiad253
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