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Heat Shock Transcription Factors (HSFs) Mediate Multilayer Regulations of Heat-Induced Chromatin Dynamics in Plants [RNA-Seq]

ABSTRACT: Eukaryotic organisms remodel chromatin landscapes to regulate gene expression in response to environmental stress. In plants, heat stress (HS) induces widespread chromatin changes, yet the role of early responsive Heat Shock Transcription Factors (HSFs) in chromatin remodeling and their evolutionary conservation remain unclear. Here, we use chromatin accessibility profiling and transcriptomics in Marchantia polymorpha hsf mutants to reveal HSFA1 as a key determinant in positioning cis-regulatory elements (CREs) for stress-induced gene activation. Comparative analysis suggests that this HSFA1-dependent chromatin remodeling mechanism is evolutionarily conserved across land plants. Multi-layered gene regulatory network (GRN) analysis further identifies MpWRKY10 and MpABI5B as HSF-independent regulators of HS responses, providing insights into parallel transcriptional subnetworks. We develop a cross-species and cross-condition machine learning framework that accurately predicts chromatin accessibility and gene expression, demonstrating a conserved regulatory logic of stress-responsive transcription. Our findings establish a scalable computational approach for decoding gene regulatory networks and provide a conceptual framework for how TFs coordinate chromatin architecture to drive stress adaptation in plants and other eukaryotes.

ORGANISM(S): Arabidopsis thaliana Marchantia polymorpha

PROVIDER: GSE290176 | GEO | 2025/11/13

REPOSITORIES: GEO

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Heat Shock Transcription Factors (HSFs) Mediate Multilayer Regulations of Heat-Induced Chromatin Dynamics in Plants [DAP-seq]

Project description:Eukaryotic organisms remodel chromatin landscapes to regulate gene expression in response to environmental stress. In plants, heat stress (HS) induces widespread chromatin changes, yet the role of early responsive Heat Shock Transcription Factors (HSFs) in chromatin remodeling and their evolutionary conservation remain unclear. Here, we use chromatin accessibility profiling and transcriptomics in Marchantia polymorpha hsf mutants to reveal HSFA1 as a key determinant in positioning cis-regulatory elements (CREs) for stress-induced gene activation. Comparative analysis suggests that this HSFA1-dependent chromatin remodeling mechanism is evolutionarily conserved across land plants. Multi-layered gene regulatory network (GRN) analysis further identifies MpWRKY10 and MpABI5B as HSF-independent regulators of HS responses, providing insights into parallel transcriptional subnetworks. We develop a cross-species and cross-condition machine learning framework that accurately predicts chromatin accessibility and gene expression, demonstrating a conserved regulatory logic of stress-responsive transcription. Our findings establish a scalable computational approach for decoding gene regulatory networks and provide a conceptual framework for how TFs coordinate chromatin architecture to drive stress adaptation in plants and other eukaryotes.

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Heat Shock Transcription Factors (HSFs) Mediate Multilayer Regulations of Heat-Induced Chromatin Dynamics in Plants [ATAC-Seq]

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Heat stress responsive HvHSFA2e gene regulates the heat and drought tolerance in barley through modulation of phytohormone and secondary metabolic pathways

Project description:High temperature and drought are the primary yield-limiting environmental constraints for staple food crops. Heat shock transcription factors (HSF) terminally regulate the plant abiotic stress responses to maintain growth and development under extreme environmental conditions. HSF genes of Subclass A2 predominantly express under heat stress (HS) and activate the transcriptional cascade of defense-related genes. In this study, a highly heat-inducible HSF, HvHSFA2e was constitutively expressed in barley (Hordeum vulgareL.) to investigate its role in abiotic stress response and plant development. Transgenic barley plants displayed enhanced heat and drought tolerance in terms of increased chlorophyll content, improved membrane stability, reduced lipid peroxidation, and less accumulation of ROS in comparison to wild-type (WT) plants. Transcriptome analysis revealed that HvHSFA2e positively regulates the expression of abiotic stress-related genes encoding HSFs, HSPs, and enzymatic antioxidants, contributing to improved stress tolerance in transgenic plants. The major genes of ABA biosynthesis pathway, flavonoid, and terpene metabolism were also upregulated in transgenics. Our findings show that HvHSFA2e mediated upregulation of heat-responsive genes, modulation in ABA and flavonoid biosynthesis pathways enhance drought and heat stress tolerance.

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Transcription profiling of heat stress response in Arabidopsis wild type and hsf1x3 double knockout mutant lines

Project description:The aim of the expression profiling was to define and to apply criteria that allow discrimination between the effects of heat stress (HS) and HSF-dependent gene expression in Arabidopsis. Therefore we determined and analyzed the expression profiles of wild type (WT) and homozygous hsf1--/hsf3-- double knock out mutant plants (abbreviated hsf1/3). Hsf1/3 plants are deficient in HSF1 and HSF3 activity and unable to induce the fast transient expression of mRNAs of a number of HS genes tested (Lohmann et al., 2004).<br> The effects of HS on gene expression were analyzed after one hour heat treatment (37C) of leaf tissue.

2004-12-15 | E-MEXP-98 | biostudies-arrayexpress

Genome-wide binding profile for Heat Shock Factor (HSF).

Project description:Sequence-specific transcription factors (TFs) are critical for specifying patterns and levels of gene expression, but the DNA elements to which they can bind are not always sufficient to specify their binding in vivo. In eukaryotes, the binding of a TF is in competition with a constellation of other proteins, including histones which package DNA into nucleosomes. Here, we examine using the ChIP-seq assay, the genome-wide distribution of Drosophila Heat Shock Factor (HSF), a TF whose binding activity is mediated by heat shock-induced trimerization. We detect HSF binding to 464 sites, the vast majority of which contain HSF Sequence-binding Elements (HSEs) in Drosophila S2 cells, but these HSF-bound sites represent only a small fraction of HSEs present in the genome. We find a strong correlation of bound HSEs to active chromatin marks present prior to HSF binding, indicating an HSEM-bM-^@M-^Ys residence in open chromatin is a primary determinant of whether HSF can bind following heat shock. A single mock immunoprecipitation (IP) using the pre-innoculated animal serum was used as a background dataset for this study. For each condition (NHS and 20minute HS), we performed two independent HSF-ChIP-seq experiments. In addition, we performed two independent HSF-ChIP-seq experiments for each condition (NHS and 20minute HS) in cells that were highly depleted of HSF by RNAi.

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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. 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

HSFA2 and HSFA3 binding after heat acclimation [ChIP-seq]

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

HSFA2 and HSFA3 binding after heat acclimation [DAP-seq]

2023-05-07 | GSE192407 | GEO

Reprogramming of transcriptome after hormetic heat stress by the endoribonuclease ENDU 2 improves lifespan and stress resistance in C. elegans

Project description:Organisms' ability to respond to life-threatening environmental impacts is crucial for their survival. While acute stress responses to unfavorable factors are well known, the physiological consequences of transient stress experiences over time, as well as their underlying mechanisms, are not well understood. In this study, we investigated the long-term effects of a short heat shock (HS) exposure on the transcriptome of C. elegans. We found that the canonical HS response was followed by a profound transcriptional reprogramming affecting many genes involved in innate immunity response. This reprogramming relies on the endoribonuclease ENDU-2 but not the heat shock factor 1 (HSF-1). ENDU-2 in this context co-localizes with chromatin and interacts with RNA polymerase Pol II, enabling specific regulation of transcription in the post-HS period. Failure to activate this post-HS response does not impair animal survival under continuous HS insult but eliminates the beneficial effects of hormetic HS. In summary, our work discovers that the RNA-binding protein ENDU-2 mediates the hormetic long-term effects of transient HS to determine aging and longevity.

2023-06-29 | PXD041872 | Pride

Immediate transcriptional responses to heat shock of plant leaf

Project description:Ambient temperature is one of the most important environment factors that direct all organisms for morphogenesis, metabolisms and growth. Plants have evolved efficient mechanisms adapting temperature fluctuation such as heat stress response (HSR). Although transcriptional regulatory network of plant HSR has been established, little is known on the genome-wide transcriptional changes within first several minutes upon heat shock (HS). To precisely measure the very first wave of transcriptional response to HS, we investigated the nascent RNA and mature mRNA from plant leaf tissue exposure to 5-min HS treatment using global run-on sequencing (GRO-seq) and RNA sequencing (RNA-seq) methods. We found that only a small group of genes were both up- or down-regulated at nascent RNA and mRNA levels. Primed plants that already exposed to a mild heat stress induced a more drastic transcriptomic alteration than naïve plants which had not experienced a heat stress. Group A1 HEAT SHOCK TRANSCRIPTION FACTORs (HsfA1s) are the major transcription factors in charge of the very early transcriptional HSR. Within 5-minute HS, we also observed that: 1) Engaged RNA polymerase II (Pol II) was accumulated downstream of transcription start sites; 2) 5' pause-release is a rate limiting step for induction of some heat shock protein genes; 3) A good number of genes switched transcription modes; 4) Pervasive read-through was induced at terminators. Plants' HSR is transcriptionally very quick. GRO-seq is sensitive and robust to detect quick response to HS. Heat stress memory takes place at multiple steps of transcription cycles such as Pol II recruitment, 5' pausing, elongation and termination.

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