Convergent Epigenetic Mechanisms Avoid Constitutive Expression of Immune Receptor Gene Subsets

The gene pool encoding PRR and NLR immune receptors determines the ability of a plant to resist microbial infections. Basal expression of these genes is prevented by diverse mechanisms since their hyperactivity can be harmful. To approach the study of epigenetic control of PRR/NLR genes we here anal...

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Autores principales: Cambiagno, Damian Alejandro, Torres, José Roberto, Alvarez, María Elena
Formato: Artículo
Lenguaje:Inglés
Publicado: Frontiers Media 2021
Materias:
Acceso en línea:http://hdl.handle.net/20.500.12123/10217
https://www.frontiersin.org/articles/10.3389/fpls.2021.703667/full
https://doi.org/10.3389/fpls.2021.703667
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author Cambiagno, Damian Alejandro
Torres, José Roberto
Alvarez, María Elena
author_browse Alvarez, María Elena
Cambiagno, Damian Alejandro
Torres, José Roberto
author_facet Cambiagno, Damian Alejandro
Torres, José Roberto
Alvarez, María Elena
author_sort Cambiagno, Damian Alejandro
collection INTA Digital
description The gene pool encoding PRR and NLR immune receptors determines the ability of a plant to resist microbial infections. Basal expression of these genes is prevented by diverse mechanisms since their hyperactivity can be harmful. To approach the study of epigenetic control of PRR/NLR genes we here analyzed their expression in mutants carrying abnormal repressive 5-methyl cytosine (5-mC) and histone 3 lysine 9 dimethylation (H3K9me2) marks, due to lack of MET1, CMT3, MOM1, SUVH4/5/6, or DDM1. At optimal growth conditions, none of the mutants showed basal expression of the defense gene marker PR1, but all of them had greater resistance to Pseudomonas syringae pv. tomato than wild type plants, suggesting they are primed to stimulate immune cascades. Consistently, analysis of available transcriptomes indicated that all mutants showed activation of particular PRR/NLR genes under some growth conditions. Under low defense activation, 37 PRR/NLR genes were expressed in these plants, but 29 of them were exclusively activated in specific mutants, indicating that MET1, CMT3, MOM1, SUVH4/5/6, and DDM1 mediate basal repression of different subsets of genes. Some epigenetic marks present at promoters, but not gene bodies, could explain the activation of these genes in the mutants. As expected, suvh4/5/6 and ddm1 activated genes carrying 5-mC and H3K9me2 marks in wild type plants. Surprisingly, all mutants expressed genes harboring promoter H2A.Z/H3K27me3 marks likely affected by the chromatin remodeler PIE1 and the histone demethylase REF6, respectively. Therefore, MET1, CMT3, MOM1, SUVH4/5/6, and DDM1, together with REF6, seemingly contribute to the establishment of chromatin states that prevent constitutive PRR/NLR gene activation, but facilitate their priming by modulating epigenetic marks at their promoters.
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institution Instituto Nacional de Tecnología Agropecuaria (INTA -Argentina)
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spelling INTA102172021-09-09T13:22:56Z Convergent Epigenetic Mechanisms Avoid Constitutive Expression of Immune Receptor Gene Subsets Cambiagno, Damian Alejandro Torres, José Roberto Alvarez, María Elena Epigenetics Gene Pools Immune Response Reservas Genéticas Respuesta Inmunológica Epigenético PRR/NLR Immune Receptor Genes 5-mC/H3K9me2 and H2A.Z/H3K27me3 Marks Defense Cascades Priming Acervo Genético The gene pool encoding PRR and NLR immune receptors determines the ability of a plant to resist microbial infections. Basal expression of these genes is prevented by diverse mechanisms since their hyperactivity can be harmful. To approach the study of epigenetic control of PRR/NLR genes we here analyzed their expression in mutants carrying abnormal repressive 5-methyl cytosine (5-mC) and histone 3 lysine 9 dimethylation (H3K9me2) marks, due to lack of MET1, CMT3, MOM1, SUVH4/5/6, or DDM1. At optimal growth conditions, none of the mutants showed basal expression of the defense gene marker PR1, but all of them had greater resistance to Pseudomonas syringae pv. tomato than wild type plants, suggesting they are primed to stimulate immune cascades. Consistently, analysis of available transcriptomes indicated that all mutants showed activation of particular PRR/NLR genes under some growth conditions. Under low defense activation, 37 PRR/NLR genes were expressed in these plants, but 29 of them were exclusively activated in specific mutants, indicating that MET1, CMT3, MOM1, SUVH4/5/6, and DDM1 mediate basal repression of different subsets of genes. Some epigenetic marks present at promoters, but not gene bodies, could explain the activation of these genes in the mutants. As expected, suvh4/5/6 and ddm1 activated genes carrying 5-mC and H3K9me2 marks in wild type plants. Surprisingly, all mutants expressed genes harboring promoter H2A.Z/H3K27me3 marks likely affected by the chromatin remodeler PIE1 and the histone demethylase REF6, respectively. Therefore, MET1, CMT3, MOM1, SUVH4/5/6, and DDM1, together with REF6, seemingly contribute to the establishment of chromatin states that prevent constitutive PRR/NLR gene activation, but facilitate their priming by modulating epigenetic marks at their promoters. Instituto de Fisiología y Recursos Genéticos Vegetales Fil: Cambiagno, Damián Alejandro . Consejo Nacional de Investigaciones Científicas y Técnicas. Unidad de Estudios Agropecuarios (UDEA); Argentina Fil: Cambiagno, Damián Alejandro. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Fisiología y Recursos Genéticos Vegetales; Argentina Fil: Torres, José Roberto. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Departamento de Química Biológica Ranwel Caputto; Argentina Fil: Torres, José Roberto. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro de Investigaciones en Química Biológica de Córdoba (CIQUIBIC); Argentina Fil: Alvarez, María Elena. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Departamento de Química Biológica Ranwel Caputto; Argentina Fil: Alvarez, María Elena. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro de Investigaciones en Química Biológica de Córdoba (CIQUIBIC); Argentina 2021-09-09T13:14:10Z 2021-09-09T13:14:10Z 2021-09-07 info:ar-repo/semantics/artículo info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion http://hdl.handle.net/20.500.12123/10217 https://www.frontiersin.org/articles/10.3389/fpls.2021.703667/full 1664-462X (online) https://doi.org/10.3389/fpls.2021.703667 eng info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by-nc-sa/4.0/ Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) application/pdf Frontiers Media Frontiers in Plant Science 12 : 703667 (September 2021)
spellingShingle Epigenetics
Gene Pools
Immune Response
Reservas Genéticas
Respuesta Inmunológica
Epigenético
PRR/NLR Immune Receptor Genes
5-mC/H3K9me2 and H2A.Z/H3K27me3 Marks
Defense Cascades
Priming
Acervo Genético
Cambiagno, Damian Alejandro
Torres, José Roberto
Alvarez, María Elena
Convergent Epigenetic Mechanisms Avoid Constitutive Expression of Immune Receptor Gene Subsets
title Convergent Epigenetic Mechanisms Avoid Constitutive Expression of Immune Receptor Gene Subsets
title_full Convergent Epigenetic Mechanisms Avoid Constitutive Expression of Immune Receptor Gene Subsets
title_fullStr Convergent Epigenetic Mechanisms Avoid Constitutive Expression of Immune Receptor Gene Subsets
title_full_unstemmed Convergent Epigenetic Mechanisms Avoid Constitutive Expression of Immune Receptor Gene Subsets
title_short Convergent Epigenetic Mechanisms Avoid Constitutive Expression of Immune Receptor Gene Subsets
title_sort convergent epigenetic mechanisms avoid constitutive expression of immune receptor gene subsets
topic Epigenetics
Gene Pools
Immune Response
Reservas Genéticas
Respuesta Inmunológica
Epigenético
PRR/NLR Immune Receptor Genes
5-mC/H3K9me2 and H2A.Z/H3K27me3 Marks
Defense Cascades
Priming
Acervo Genético
url http://hdl.handle.net/20.500.12123/10217
https://www.frontiersin.org/articles/10.3389/fpls.2021.703667/full
https://doi.org/10.3389/fpls.2021.703667
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AT alvarezmariaelena convergentepigeneticmechanismsavoidconstitutiveexpressionofimmunereceptorgenesubsets