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Histone retention preserves epigenetic marks during heat stress-induced transcriptional memory in plants

ABSTRACT: Plants often experience recurrent stressful events, for example during heat waves. They can be primed by heat stress (HS) to improve survival of more severe heat stress conditions. At certain genes, sustained expression is induced for several days beyond the initial heat stress. This transcriptional memory is associated with hyper-methylation of histone H3 lysine 4 (H3K4me3), but it is unclear how this is maintained for extended periods. Here, we determined histone turnover by measuring chromatin association of HS-induced histone H3.3. Genome-wide histone turnover was not homogenous, in particular, H3.3 was retained longer at heat stress-memory genes compared to HS-induced non-memory genes during the memory phase. While low nucleosome turnover retained H3K4 methylation, methylation loss did not affect turnover, suggesting that low nucleosome turnover sustains H3K4 methylation, but not vice versa. Together, our results unveil the modulation of histone turnover as a mechanism to retain environmentally-mediated epigenetic modifications.

SUBMITTER: Prof. Isabel Bäurle

PROVIDER: S-SCDT-10_15252-EMBJ_2023113595 | biostudies-other |

REPOSITORIES: biostudies-other

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Histone retention preserves epigenetic marks during heat stress-induced transcriptional memory in plants.

Project description:Plants often experience recurrent stressful events, for example, during heat waves. They can be primed by heat stress (HS) to improve the survival of more severe heat stress conditions. At certain genes, sustained expression is induced for several days beyond the initial heat stress. This transcriptional memory is associated with hyper-methylation of histone H3 lysine 4 (H3K4me3), but it is unclear how this is maintained for extended periods. Here, we determined histone turnover by measuring the chromatin association of HS-induced histone H3.3. Genome-wide histone turnover was not homogenous; in particular, H3.3 was retained longer at heat stress memory genes compared to HS-induced non-memory genes during the memory phase. While low nucleosome turnover retained H3K4 methylation, methylation loss did not affect turnover, suggesting that low nucleosome turnover sustains H3K4 methylation, but not vice versa. Together, our results unveil the modulation of histone turnover as a mechanism to retain environmentally mediated epigenetic modifications.

| S-EPMC10711655 | biostudies-literature

Histone retention preserves epigenetic marks during heat stress-induced transcriptional memory

Project description:Plants often experience recurrent stressful events, for example during heat waves. They can adapt to such recurrent heat stress (HS), allowing subsequent survival of more severe HS conditions. At certain genes HS induces sustained expression for several days beyond the actual HS. This transcriptional memory is associated with hyper-methylation of histone H3 lysine 4 (H3K4me3), however, how this is maintained for extended periods of time is unclear. Here, we determined histone turnover by measuring chromatin association of a HS-induced histone H3.3. Genome-wide Histone turnover was not homogenous, in particular, H3.3 was retained longer at HS memory genes compared to HS-induced non-memory genes during the memory phase. While low nucleosome turnover retained H3K4 methylation, its loss did not affect turnover, suggesting that low nucleosome turnover sustains H3K4 methylation (and not vice versa). Together, our results unveil the modulation of histone turnover as a mechanism to retain environmentally-mediated epigenetic modifications.

2023-10-18 | GSE218234 | GEO

Histone retention preserves epigenetic marks during heat stress-induced transcriptional memory

Project description:Histone retention preserves epigenetic marks during heat stress-induced transcriptional memory

| PRJNA902769 | ENA

A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory.

Project description:In nature, plants often encounter chronic or recurring stressful conditions. Recent results indicate that plants can remember a past exposure to stress to be better prepared for a future stress incident. However, the molecular basis of this is poorly understood. Here, we report the involvement of chromatin modifications in the maintenance of acquired thermotolerance (heat stress [HS] memory). HS memory is associated with the accumulation of histone H3 lysine 4 di- and trimethylation at memory-related loci. This accumulation outlasts their transcriptional activity and marks them as recently transcriptionally active. High accumulation of H3K4 methylation is associated with hyper-induction of gene expression upon a recurring HS. This transcriptional memory and the sustained accumulation of H3K4 methylation depend on HSFA2, a transcription factor that is required for HS memory, but not initial heat responses. Interestingly, HSFA2 associates with memory-related loci transiently during the early stages following HS. In summary, we show that transcriptional memory after HS is associated with sustained H3K4 hyper-methylation and depends on a hit-and-run transcription factor, thus providing a molecular framework for HS memory.

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Evidence for novel epigenetic marks within plants.

Project description:Variation in patterns of gene expression can result from modifications in the genome that occur without a change in the sequence of the DNA; such modifications include methylation of cytosine to generate 5-methylcytosine (5mC) resulting in the generation of heritable epimutation and novel epialleles. This type of non-sequence variation is called epigenetics. The enzymes responsible for generation of such DNA modifications in mammals are named DNA methyltransferases (DNMT) including DNMT1, DNMT2 and DNMT3. The later stages of oxidations to these modifications are catalyzed by Ten Eleven Translocation (TET) proteins, which contain catalytic domains belonging to the 2-oxoglutarate dependent dioxygenase family. In various mammalian cells/tissues including embryonic stem cells, cancer cells and brain tissues, it has been confirmed that these proteins are able to induce the stepwise oxidization of 5-methyl cytosine to 5-hydroxymethylcytosine (5hmC), 5-formylcytosine (5fC), and finally 5-carboxylcytosine (5caC). Each stage from initial methylation until the end of the DNA demethylation process is considered as a specific epigenetic mark that may regulate gene expression. This review discusses controversial evidence for the presence of such oxidative products, particularly 5hmC, in various plant species. Whereas some reports suggest no evidence for enzymatic DNA demethylation, other reports suggest that the presence of oxidative products is followed by the active demethylation and indicate the contribution of possible TET-like proteins in the regulation of gene expression in plants. The review also summarizes the results obtained by expressing the human TET conserved catalytic domain in transgenic plants.

| S-EPMC6949463 | biostudies-literature

Stress-induced epigenetic transcriptional memory of acetylcholinesterase by HDAC4.

Project description:Stress induces long-lasting changes in neuronal gene expression and cholinergic neurotransmission, but the underlying mechanism(s) are incompletely understood. Here, we report that chromatin structure and histone modifications are causally involved in this transcriptional memory. Specifically, the AChE gene encoding the acetylcholine-hydrolyzing enzyme acetylcholinesterase is known to undergo long-lasting transcriptional and alternative splicing changes after stress. In mice subjected to stress, we identified two alternative 5' exons that were down-regulated after stress in the hippocampus, accompanied by reduced acetylation and elevated trimethylation of H3K9 at the corresponding promoter. These effects were reversed completely by daily administration of the histone deacetylase (HDAC) inhibitor sodium butyrate for 1 wk after stress. H3K9 hypoacetylation was associated with a selective, sodium butyrate-reversible promoter accumulation of HDAC4. Hippocampal suppression of HDAC4 in vivo completely abolished the long-lasting AChE-related and behavioral stress effects. Our findings demonstrate long-lasting stress-inducible changes in AChE's promoter choices, identify the chromatin changes that support this long-term transcriptional memory, and reveal HDAC4 as a mediator of these effects in the hippocampus.

| S-EPMC3535662 | biostudies-literature

Heat can erase epigenetic marks of vernalization in Arabidopsis.

Project description:Vernalization establishes a memory of winter that must be maintained for weeks or months in order to promote flowering the following spring. The stability of the vernalized state varies among plant species and depends on the duration of cold exposure. In Arabidopsis thaliana, winter leads to epigenetic silencing of the floral repressor gene FLOWERING LOCUS C (FLC) and the duration of cold is measured through the dynamics of chromatin modifications during and after cold. The growing conditions encountered post-vernalization are thus critical for the maintenance of the vernalized state. We reported that high temperature leads to devernalization and, consistently, to FLC reactivation in Arabidopsis seedlings. Here we show that the repressive epigenetic mark H3K27me3 decreases at the FLC locus when vernalized seedlings are grown at 30°C, unless they were first exposed to a stabilizing period at 20°C. Ambient temperature thus controls the epigenetic memory of winter.

| S-EPMC4622702 | biostudies-literature

The marks, mechanisms and memory of epigenetic states in mammals.

Project description:It is well recognized that there is a surprising degree of phenotypic variation among genetically identical individuals, even when the environmental influences, in the strict sense of the word, are identical. Genetic textbooks acknowledge this fact and use different terms, such as 'intangible variation' or 'developmental noise', to describe it. We believe that this intangible variation results from the stochastic establishment of epigenetic modifications to the DNA nucleotide sequence. These modifications, which may involve cytosine methylation and chromatin remodelling, result in alterations in gene expression which, in turn, affects the phenotype of the organism. Recent evidence, from our work and that of others in mice, suggests that these epigenetic modifications, which in the past were thought to be cleared and reset on passage through the germline, may sometimes be inherited to the next generation. This is termed epigenetic inheritance, and while this process has been well recognized in plants, the recent findings in mice force us to consider the implications of this type of inheritance in mammals. At this stage we do not know how extensive this phenomenon is in humans, but it may well turn out to be the explanation for some diseases which appear to be sporadic or show only weak genetic linkage.

| S-EPMC1221806 | biostudies-other

Heteromeric HSFA2/HSFA3 complexes drive transcriptional memory after heat stress in Arabidopsis.

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. Here we show that FORGETTER3/ HEAT SHOCK TRANSCRIPTION FACTOR A3 (FGT3/HSFA3) is 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 positively influencing 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.

| S-EPMC8187452 | biostudies-literature

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

Project description:BackgroundTranscriptional 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.ResultsHSFA2 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.ConclusionsOur 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.

| S-EPMC10230730 | biostudies-literature

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