Evolutionarily Conserved Heat-Induced Chromatin Dynamics Drive Heat Stress Responses in Plants

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 heat-responsive Heat Shock Transcription Factors (HSFs) in chromatin remodeling and their evolutionary conservation remains unclear. Using chromatin accessibility profiling and transcriptomics in Marchantia polymorpha hsf mutants, we identify HSFA1 as a key determinant in positioning cis -regulatory elements (CREs) for HS-induced gene activation, a mechanism conserved across land plants, mice, and human cells. By integrating gene regulatory network modeling, we identify parallel transcription factor subnetworks, with MpWRKY10 and MpABI5B acting as indirect regulators of HS responses via phenylpropanoid pathways and general stress signaling. We further explore crosstalk between HS and abscisic acid (ABA) signaling, showing that while ABA modulates gene expression in an HSFA1-dependent manner, it does not induce broad chromatin remodeling, positioning it as a downstream regulator rather than a primary determinant of chromatin dynamics. To extend these insights, 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 chromatin and transcription dynamics. Our findings provide a conceptual framework for understanding how TFs coordinate chromatin architecture to drive stress adaptation in plants and potentially other eukaryotes.