HSFA1a modulates plant heat stress responses and alters the 3D chromatin organization of enhancer-promoter interactions

Abstract

The complex and dynamic three-dimensional organization of chromatin within the nucleus makes understanding the control of gene expression challenging, but also opens up possible ways to epigenetically modulate gene expression. Because plants are sessile, they evolved sophisticated ways to rapidly modulate gene expression in response to environmental stress, that are thought to be coordinated by changes in chromatin conformation to mediate specific cellular and physiological responses. However, to what extent and how stress induces dynamic changes in chromatin reorganization remains poorly understood. Here, we comprehensively investigated genome-wide chromatin changes associated with transcriptional reprogramming response to heat stress in tomato. Our data show that heat stress induces rapid changes in chromatin architecture, leading to the transient formation of promoter-enhancer contacts, likely driving the expression of heat-stress responsive genes. Furthermore, we demonstrate that chromatin spatial reorganization requires HSFA1a, a transcription factor (TF) essential for heat stress tolerance in tomato. In light of our findings, we propose that TFs play a key role in controlling dynamic transcriptional responses through 3D reconfiguration of promoter-enhancer contacts.

Multi-omic dissection of ancestral heat stress memory responses inBrachypodium distachyon

“…Clustering analysis of expression profiles revealed five clusters, of which cluster 3 showed a continuous increase of gene expression during HS, thus capturing genes with a mixture of Type I (sustained) and Type II (enhanced) expression patterns (Figure 2A). The biological function of the genes in cluster 3 is also in line with the biological processes important for HS survival, acclimation, and memory: protein (synthesis, modification, homeostasis, translocation)(Zhou et al, 2014; Garcia-Molina et al, 2020), metabolism (respiration, lipids)(Shiva et al, 2020; Scafaro et al, 2021) and chromatin organization (Huang et al, 2023).…”

The CLAMP GA-binding transcription factor regulates heat stress-induced transcriptional repression by associating with 3D loop anchors

“…One prior report suggests that HS induces the re-localization of architectural proteins from TAD borders to increase long-range interactions enriched with Polycomb marks, thereby regulating repression (12). In plants, HS alters the 3D arrangement of promoter-enhancer interactions to regulate the activation of heat shock-responsive genes (23–25). In contrast, other reports could not find a correlation between global three-dimensional chromatin changes and transcriptional changes after heat shock (2).…”

“…Repression of transcription after HS is an essential global phenomenon for cells to survive under stress because it conserves energy and prevents the formation of potentially toxic protein and RNA aggregates. CLAMP is known to regulate 3D chromatin loop formation (16), which can be sensitive to changes in temperature (23). Therefore, we asked whether changes in CLAMP-bound 3D loops are associated with HS-induced transcriptional repression.…”

Heat stress response and transposon control in plant shoot stem cells

“…Furthermore, heat stress induced large-scale chromatin organization changes, with an involvement of HSFA1a, another heat response transcription factor, and modifies numerous interactions of regulatory sequences in tomato (Huang et a., 2023). Future studies are necessary to comprehensively capture the changes at all levels and distinguish transient effects from those with long-lasting and transgenerational consequences.…”