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Genomic and epigenomic determinants of heat stress-induced transcriptional memory in Arabidopsis

  • Background Transcriptional regulation is a key aspect of environmental stress responses. Heat stress induces transcriptional memory, i.e., sustained induction or enhanced re-induction of transcription, that allows plants to respond more efficiently to a recurrent HS. In light of more frequent temperature extremes due to climate change, improving heat tolerance in crop plants is an important breeding goal. However, not all heat stress-inducible genes show transcriptional memory, and it is unclear what distinguishes memory from non-memory genes. To address this issue and understand the genome and epigenome architecture of transcriptional memory after heat stress, we identify the global target genes of two key memory heat shock transcription factors, HSFA2 and HSFA3, using time course ChIP-seq. Results HSFA2 and HSFA3 show near identical binding patterns. In vitro and in vivo binding strength is highly correlated, indicating the importance of DNA sequence elements. In particular, genes with transcriptional memory are stronglyBackground Transcriptional regulation is a key aspect of environmental stress responses. Heat stress induces transcriptional memory, i.e., sustained induction or enhanced re-induction of transcription, that allows plants to respond more efficiently to a recurrent HS. In light of more frequent temperature extremes due to climate change, improving heat tolerance in crop plants is an important breeding goal. However, not all heat stress-inducible genes show transcriptional memory, and it is unclear what distinguishes memory from non-memory genes. To address this issue and understand the genome and epigenome architecture of transcriptional memory after heat stress, we identify the global target genes of two key memory heat shock transcription factors, HSFA2 and HSFA3, using time course ChIP-seq. Results HSFA2 and HSFA3 show near identical binding patterns. In vitro and in vivo binding strength is highly correlated, indicating the importance of DNA sequence elements. In particular, genes with transcriptional memory are strongly enriched for a tripartite heat shock element, and are hallmarked by several features: low expression levels in the absence of heat stress, accessible chromatin environment, and heat stress-induced enrichment of H3K4 trimethylation. These results are confirmed by an orthogonal transcriptomic data set using both de novo clustering and an established definition of memory genes. Conclusions Our findings provide an integrated view of HSF-dependent transcriptional memory and shed light on its sequence and chromatin determinants, enabling the prediction and engineering of genes with transcriptional memory behavior.show moreshow less

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Author details:Christian KappelORCiDGND, Thomas Friedrich, Vicky OberkoflerORCiDGND, Li JiangORCiD, Tim CrawfordORCiD, Michael LenhardORCiDGND, Isabel BäurleORCiDGND
DOI:https://doi.org/10.1186/s13059-023-02970-5
ISSN:1474-760X
ISSN:1465-6906
Pubmed ID:https://pubmed.ncbi.nlm.nih.gov/37254211
Title of parent work (English):Genome biology : biology for the post-genomic era
Publisher:BioMed Central
Place of publishing:London
Publication type:Article
Language:English
Date of first publication:2023/05/30
Publication year:2023
Release date:2024/06/20
Tag:Arabidopsis thaliana; ChIP-seq; HSFA2; HSFA3; Heat stress; Histone H3K4 trimethylation; Priming; Transcriptional memory
Volume:24
Issue:1
Article number:129
Number of pages:23
Organizational units:Mathematisch-Naturwissenschaftliche Fakultät / Institut für Biochemie und Biologie
DDC classification:5 Naturwissenschaften und Mathematik / 57 Biowissenschaften; Biologie / 570 Biowissenschaften; Biologie
Peer review:Referiert
Publishing method:Open Access / Gold Open-Access
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License (German):License LogoCC-BY - Namensnennung 4.0 International
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