Histone retention preserves epigenetic marks during heat stress-induced transcriptional memory
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ABSTRACT:
ORGANISM(S): Arabidopsis thaliana
PROVIDER: GSE218234 | GEO | 2023/10/18
REPOSITORIES: GEO
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Project description:Adaptive plasticity in stress responses is a key element of plant survival strategies. For instance, moderate heat stress (HS) primes a plant to acquire thermotolerance, which allows subsequent survival of more severe HS conditions. Acquired thermotolerance is actively maintained over several days (HS memory) and involves the sustained induction of memory-related genes. We find FORGETTER3/ HEAT SHOCK TRANSCRIPTION FACTOR A3 (FGT3/HSFA3) to be specifically required for physiological HS memory and maintaining high memory-gene expression during the days following a HS exposure. HSFA3 mediates HS memory by direct transcriptional activation of memory-related genes after return to normal growth temperatures. HSFA3 binds HSFA2, and in vivo both proteins form heteromeric complexes with additional HSFs. Our results indicate that only complexes containing both HSFA2 and HSFA3 efficiently promote transcriptional memory by promoting histone H3 lysine 4 (H3K4) hyper-methylation. In summary, our work defines the major HSF complex controlling transcriptional memory and elucidates the in vivo dynamics of HSF complexes during somatic stress memory.
2021-05-04 | GSE162434 | GEO
Project description:Transcriptional regulation is a key aspect of environmental stress responses. Heat stress (HS) induces transcriptional memory 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 crops is an important breeding goal. However, not all HS-inducible genes show sustained induction/transcriptional memory and it is unclear what distinguishes memory and non-memory genes. To address this issue and understand the (epi-) genome architecture in transcriptional memory after HS, we investigated genome-wide target genes of the two key memory heat shock transcription factors, HSFA2 and HSFA3. We determined the binding kinetics of these factors to their target genes and asked whether genes that show sustained induction of transcription carry specific features that allow prediction and potentially engineering of memory gene behaviour. HSFA2 and HSFA3 show near identical binding patterns. In vitro binding strength as determined by DAP-seq analysis correlates strongly with in vivo binding strength, confirming the importance of sequence features. However, no single distinctive sequence motif appears to be required for memory behaviour. Instead, HS memory genes are characterized by a combination of features: low expression levels in the absence of HS, chromatin environment and an enrichment of H3K4 methylation after HS. Our findings are confirmed by an orthogonal transcriptomic data set using both de novo clustering and an established definition of memory genes. In summary, our findings provide an integrated view of HSF-dependent transcriptional memory and shed light on its sequence and chromatin determinants. They will contribute to the prediction and engineering of genes with transcriptional memory.
2023-05-07 | GSE192427 | GEO
Project description:Transcriptional regulation is a key aspect of environmental stress responses. Heat stress (HS) induces transcriptional memory 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 crops is an important breeding goal. However, not all HS-inducible genes show sustained induction/transcriptional memory and it is unclear what distinguishes memory and non-memory genes. To address this issue and understand the (epi-) genome architecture in transcriptional memory after HS, we investigated genome-wide target genes of the two key memory heat shock transcription factors, HSFA2 and HSFA3. We determined the binding kinetics of these factors to their target genes and asked whether genes that show sustained induction of transcription carry specific features that allow prediction and potentially engineering of memory gene behaviour. HSFA2 and HSFA3 show near identical binding patterns. In vitro binding strength as determined by DAP-seq analysis correlates strongly with in vivo binding strength, confirming the importance of sequence features. However, no single distinctive sequence motif appears to be required for memory behaviour. Instead, HS memory genes are characterized by a combination of features: low expression levels in the absence of HS, chromatin environment and an enrichment of H3K4 methylation after HS. Our findings are confirmed by an orthogonal transcriptomic data set using both de novo clustering and an established definition of memory genes. In summary, our findings provide an integrated view of HSF-dependent transcriptional memory and shed light on its sequence and chromatin determinants. They will contribute to the prediction and engineering of genes with transcriptional memory.
2023-05-07 | GSE192407 | GEO
Project description:In nature, plants are often exposed to recurring adverse environmental conditions. Acclimation to high temperature stress entails transcriptional responses that are mediated by heat-shock transcription factors (HSFs), and they are primed to better withstand subsequent stress events. This heat stress (HS)-induced transcriptional memory results in more efficient re-induction of transcription upon recurring HS. However, the mechanisms by which HSFs recruit and enact the transcriptional machinery remain unclear. Here, we identified two subunits of the kinase module of the Mediator transcriptional co-regulator complex, CDK8 and MED12, as regulators of HS memory in Arabidopsis thaliana. Enhanced re-induction of gene expression after recurrent HS and physiological HS memory, as well as H3K4 methylation are compromised in cdk8 and med12 mutants. HSFA2 interacts with CDK8 during and after HS and recruits it to memory gene loci, where CDK8 binds in the promoter but also the gene body, together with core Mediator and RNA polymerase II (Pol II). Our data suggest that CDK8 resolves stalled Pol II complexes or promotes efficient recycling for subsequent cycles of transcription. As HSFA2, CDK8 is largely dispensable for the initial induction of gene expression after HS and thus promotes transcriptional memory independently of HS-dependent primary gene induction. Our findings provide a model for the complex role of the Mediator kinase module during transcriptional memory in multicellular eukaryotes through interaction with transcription factors, chromatin modifications and promotion of Pol II productivity.
2023-12-12 | GSE232094 | GEO
Project description:We developed a system to study the DNA replication-independent turnover nucleosomes containing the histone variant H3.3 in mammalian cells. By measuring the genome-wide incorporation of H3.3 at different time points following epitope-tagged H3.3 expression, we find three categories of H3.3-nucleosome turnover in vivo: rapid turnover, intermediate turnover and, specifically at telomeres, slow turnover. Our data indicate that H3.3-containing nucleosomes at enhancers and promoters undergo a rapid turnover that is associated with active histone modification marks including H3K4me1, H3K4me3, H3K9ac, H3K27ac and the histone variant H2A.Z. The rate of turnover is negatively correlated with H3K27me3 at regulatory regions and with H3K36me3 at gene bodies. Examination of incorporation dynamics of histone variant H3.3
2013-10-23 | E-GEOD-51505 | biostudies-arrayexpress
Project description:In nature, plants are constantly exposed to many transient, but recurring, stresses. Thus, to complete their life cycles they require a dynamic balance between capacities to recover following cessation of stress and maintenance of stress memory. Recently, we uncovered a new functional role of autophagy in regulating recovery from heat stress (HS) and resetting cellular memory of HS in Arabidopsis thaliana. Here, we demonstrate that NBR1 (Next-to-BRCA1) plays a crucial role as an adaptor receptor for selective autophagy during recovery from HS. Immunoblot analysis and confocal microscopy revealed that levels of NBR1 protein, NBR1-labeled puncta and NBR1 activities were all higher during the HS recovery phase than before and after this phase. Co-immunoprecipitation analysis of proteins interacting with NBR1 and comparative proteomic analysis of a nbr1 knockout mutant and wild-type plants identified 58 proteins as potential novel targets of NBR1. Cellular, biochemical and functional genetic studies confirmed that NBR1 targets Heat Shock Protein 90 (HSP90) and ROF1, a member of the FKBP family, and mediates their degradation by autophagy, which represses the expression of HSPs regulated by HsfA2 transcription factor and the response to HS. Accordingly, loss-of-function mutation of NBR1 resulted in a stronger HS memory phenotype. Together our results provide new insights into the mechanistic principles by which autophagy regulates plant response to recurrent HS.
2022-02-15 | PXD015027 | Pride
Project description:We developed a system to study the DNA replication-independent turnover nucleosomes containing the histone variant H3.3 in mammalian cells. By measuring the genome-wide incorporation of H3.3 at different time points following epitope-tagged H3.3 expression, we find three categories of H3.3-nucleosome turnover in vivo: rapid turnover, intermediate turnover and, specifically at telomeres, slow turnover. Our data indicate that H3.3-containing nucleosomes at enhancers and promoters undergo a rapid turnover that is associated with active histone modification marks including H3K4me1, H3K4me3, H3K9ac, H3K27ac and the histone variant H2A.Z. The rate of turnover is negatively correlated with H3K27me3 at regulatory regions and with H3K36me3 at gene bodies.
2013-10-23 | GSE51505 | GEO
Project description:Stressful environmental conditions, including heat stress (HS), are a major limiting factor in crop yield. Understanding the molecular mechanisms of plant stress memory and resilience is important for improving crop yield. We performed a temporal atlas of DNA methylation to reveal the biological pathways and potential functional inter-layer associations affected by HS
2023-03-17 | E-MTAB-12727 | biostudies-arrayexpress
Project description:Epigenetic environment of histone H3.3 on promoters revealed by integration of imaging and genome-scale chromatin and methyl-DNA immunoprecipitation information. Chromatin regions with different transcriptional outputs are distinguished by the deposition of histone variants. Histone H3.3 is incorporated into chromatin in a replication-independent manner; yet the relationship between H3.3 deposition, chromatin environment is incompletely understood. We have integrated imaging and genome-scale chromatin and methyl-DNA immunoprecipitation approaches to investigate the genomic distribution of epitope-tagged H3.3 in relation to histone modifications, DNA methylation and transcription. Results: Imaging shows that H3.3, in contrast to replicative H3.1 or H2B, is enriched in chromatin marked by histone modifications of active genes. A genome-wide survey identifies 1,649 H3.3-enriched promoters, only a subset of which is co-enriched in H3K4me3, H3K9me3 and/or H3K27me3, with a preference for H3K4me3, corroborating imaging data. H3.3-enriched promoters are depleted of H3.3 at the TSS in a transcription-independent manner. H3.3 is found predominantly on CpG-rich unmethylated promoters, creating a condition favourable for transcription. In undifferentiated mesenchymal stem cells, H3.3 target genes are linked to signaling and mesodermal differentiation, suggesting that H3.3 may be a mark of lineage priming. Conclusions: A minor fraction of H3.3 is targeted to promoters, which are predominantly CpG-rich, DNA unmethylated and devoid of detectable trimethylated H3K4, K9 and K27. Among H3.3 target promoters co-marked by methylated H3, H4K4me3 is preferred, with or without H3K27me3, arguing that in mesenchymal stem cells H3.3 marks transcriptionally active or potentially active promoters. Key words: Imaging, ChIP-chip, MeDIP-chip, histone H3.3, mesenchymal stem cells ChIP-chip and MeDIP-chip experiments: Performed with two independent biological replicates. Gene expression profiling experiments: Total RNA obtained from H3.3-EGFP transfected or empty-EGFP transfected mesenchymal stem cells compared to untransfected mesenchymal stem cells. Raw expression data linked below as supplementary file (GSE17053_Illumina_non-normalized_data.txt).
2010-05-12 | E-GEOD-17053 | biostudies-arrayexpress
Project description:Turnover and exchange of nucleosomal histones and their variants, a process long believed to be static in post-replicative cells, remains largely unexplored in brain. Here, we describe a novel mechanistic role for HIRA (histone cell cycle regulator) and proteasomal degradation associated histone dynamics in the regulation of activity-dependent transcription, synaptic connectivity and behavior. We uncover a dramatic developmental profile of nucleosome occupancy across the lifespan of both rodents and humans, with the histone variant H3.3 accumulating to near saturating levels throughout the neuronal genome by mid-adolescence. Despite such accumulation, H3.3 containing nucleosomes remain highly dynamic–in a modification independent manner–to control neuronal- and glial- specific gene expression patterns throughout life. Manipulating H3.3 dynamics in both embryonic and adult neurons confirmed its essential role in neuronal plasticity and cognition. Our findings establish histone turnover as a critical, and previously undocumented, regulator of cell-type specific transcription and plasticity in mammalian brain. All RNA-seq samples were generated to test the impact of neuronal activity/adult physiological plasticity on histone turnover turnover mediated alterations in mRNA expression in the central nervous system. This was tested in cultured neurons and astrocytes, and embryonic/adult brain tissues
2015-06-23 | E-GEOD-69807 | biostudies-arrayexpress