Dynamic enhancer transcription associates with reprogramming of immune genes during pattern triggered immunity in Arabidopsis
Abstract 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 durin...
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| Format: | Article |
| Language: | English |
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BMC
2022-07-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-022-01362-8 |
| _version_ | 1818188599701536768 |
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| author | Ying Zhang Meng Tang Mengling Huang Jiatao Xie Jiasen Cheng Yanping Fu Daohong Jiang Xiao Yu Bo Li |
| author_facet | Ying Zhang Meng Tang Mengling Huang Jiatao Xie Jiasen Cheng Yanping Fu Daohong Jiang Xiao Yu Bo Li |
| author_sort | Ying Zhang |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-12-11T23:29:29Z |
| format | Article |
| id | doaj.art-c5d63ba6fd3645c49ba5b6b2d06bab37 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-12-11T23:29:29Z |
| publishDate | 2022-07-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-c5d63ba6fd3645c49ba5b6b2d06bab372022-12-22T00:46:04ZengBMCBMC Biology1741-70072022-07-0120112010.1186/s12915-022-01362-8Dynamic enhancer transcription associates with reprogramming of immune genes during pattern triggered immunity in ArabidopsisYing Zhang0Meng Tang1Mengling Huang2Jiatao Xie3Jiasen Cheng4Yanping Fu5Daohong Jiang6Xiao Yu7Bo Li8State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityHubei Key Lab of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityAbstract 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.https://doi.org/10.1186/s12915-022-01362-8Plant innate immunityTranscriptional regulationCis-regulatory elementsEnhancersEnhancer RNAs |
| spellingShingle | Ying Zhang Meng Tang Mengling Huang Jiatao Xie Jiasen Cheng Yanping Fu Daohong Jiang Xiao Yu Bo Li Dynamic enhancer transcription associates with reprogramming of immune genes during pattern triggered immunity in Arabidopsis BMC Biology Plant innate immunity Transcriptional regulation Cis-regulatory elements Enhancers Enhancer RNAs |
| 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 | Plant innate immunity Transcriptional regulation Cis-regulatory elements Enhancers Enhancer RNAs |
| url | https://doi.org/10.1186/s12915-022-01362-8 |
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