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Dynamic enhancer transcription associates with reprogramming of immune genes during pattern triggered immunity in Arabidopsis

BACKGROUND: Enhancers are cis-regulatory elements present in eukaryote genomes, which constitute indispensable determinants of gene regulation by governing the spatiotemporal and quantitative expression dynamics of target genes, and are involved in multiple life processes, for instance during develo...

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Autores principales: Zhang, Ying, Tang, Meng, Huang, Mengling, Xie, Jiatao, Cheng, Jiasen, Fu, Yanping, Jiang, Daohong, Yu, Xiao, Li, Bo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9301868/
https://www.ncbi.nlm.nih.gov/pubmed/35864475
http://dx.doi.org/10.1186/s12915-022-01362-8
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author Zhang, Ying
Tang, Meng
Huang, Mengling
Xie, Jiatao
Cheng, Jiasen
Fu, Yanping
Jiang, Daohong
Yu, Xiao
Li, Bo
author_facet Zhang, Ying
Tang, Meng
Huang, Mengling
Xie, Jiatao
Cheng, Jiasen
Fu, Yanping
Jiang, Daohong
Yu, Xiao
Li, Bo
author_sort Zhang, Ying
collection PubMed
description BACKGROUND: Enhancers are cis-regulatory elements present in eukaryote genomes, which constitute indispensable determinants of gene regulation by governing the spatiotemporal and quantitative expression dynamics of target genes, and are involved in multiple life processes, for instance during development and disease states. The importance of enhancer activity has additionally been highlighted for immune responses in animals and plants; however, the dynamics of enhancer activities and molecular functions in plant innate immunity are largely unknown. Here, we investigated the involvement of distal enhancers in early innate immunity in Arabidopsis thaliana. RESULTS: A group of putative distal enhancers producing low-abundance transcripts either unidirectionally or bidirectionally are identified. We show that enhancer transcripts are dynamically modulated in plant immunity triggered by microbe-associated molecular patterns and are strongly correlated with open chromatin, low levels of methylated DNA, and increases in RNA polymerase II targeting and acetylated histone marks. Dynamic enhancer transcription is correlated with target early immune gene expression patterns. Cis motifs that are bound by immune-related transcription factors, such as WRKYs and SARD1, are highly enriched within upregulated enhancers. Moreover, a subset of core pattern-induced enhancers are upregulated by multiple patterns from diverse pathogens. The expression dynamics of putative immunity-related enhancers and the importance of WRKY binding motifs for enhancer function were also validated. CONCLUSIONS: Our study demonstrates the general occurrence of enhancer transcription in plants and provides novel information on the distal regulatory landscape during early plant innate immunity, providing new insights into immune gene regulation and ultimately improving the mechanistic understanding of the plant immune system. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01362-8.
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spelling pubmed-93018682022-07-22 Dynamic enhancer transcription associates with reprogramming of immune genes during pattern triggered immunity in Arabidopsis Zhang, Ying Tang, Meng Huang, Mengling Xie, Jiatao Cheng, Jiasen Fu, Yanping Jiang, Daohong Yu, Xiao Li, Bo BMC Biol Research Article BACKGROUND: Enhancers are cis-regulatory elements present in eukaryote genomes, which constitute indispensable determinants of gene regulation by governing the spatiotemporal and quantitative expression dynamics of target genes, and are involved in multiple life processes, for instance during development and disease states. The importance of enhancer activity has additionally been highlighted for immune responses in animals and plants; however, the dynamics of enhancer activities and molecular functions in plant innate immunity are largely unknown. Here, we investigated the involvement of distal enhancers in early innate immunity in Arabidopsis thaliana. RESULTS: A group of putative distal enhancers producing low-abundance transcripts either unidirectionally or bidirectionally are identified. We show that enhancer transcripts are dynamically modulated in plant immunity triggered by microbe-associated molecular patterns and are strongly correlated with open chromatin, low levels of methylated DNA, and increases in RNA polymerase II targeting and acetylated histone marks. Dynamic enhancer transcription is correlated with target early immune gene expression patterns. Cis motifs that are bound by immune-related transcription factors, such as WRKYs and SARD1, are highly enriched within upregulated enhancers. Moreover, a subset of core pattern-induced enhancers are upregulated by multiple patterns from diverse pathogens. The expression dynamics of putative immunity-related enhancers and the importance of WRKY binding motifs for enhancer function were also validated. CONCLUSIONS: Our study demonstrates the general occurrence of enhancer transcription in plants and provides novel information on the distal regulatory landscape during early plant innate immunity, providing new insights into immune gene regulation and ultimately improving the mechanistic understanding of the plant immune system. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01362-8. BioMed Central 2022-07-21 /pmc/articles/PMC9301868/ /pubmed/35864475 http://dx.doi.org/10.1186/s12915-022-01362-8 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Zhang, Ying
Tang, Meng
Huang, Mengling
Xie, Jiatao
Cheng, Jiasen
Fu, Yanping
Jiang, Daohong
Yu, Xiao
Li, Bo
Dynamic enhancer transcription associates with reprogramming of immune genes during pattern triggered immunity in Arabidopsis
title Dynamic enhancer transcription associates with reprogramming of immune genes during pattern triggered immunity in Arabidopsis
title_full Dynamic enhancer transcription associates with reprogramming of immune genes during pattern triggered immunity in Arabidopsis
title_fullStr Dynamic enhancer transcription associates with reprogramming of immune genes during pattern triggered immunity in Arabidopsis
title_full_unstemmed Dynamic enhancer transcription associates with reprogramming of immune genes during pattern triggered immunity in Arabidopsis
title_short Dynamic enhancer transcription associates with reprogramming of immune genes during pattern triggered immunity in Arabidopsis
title_sort dynamic enhancer transcription associates with reprogramming of immune genes during pattern triggered immunity in arabidopsis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9301868/
https://www.ncbi.nlm.nih.gov/pubmed/35864475
http://dx.doi.org/10.1186/s12915-022-01362-8
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