Transcription Factors Mediate Enhancer-promoter Interactions and Alter 3D Chromatin Conformation in Tomato

Due to the complexity of the chromatin structure within the nucleus and the dynamic changes in its three-dimensional spatial structure, it is challenging to deeply explore the three-dimensional genome spatial structure, the formation of chromatin loops and the impact on gene expression regulation. Recently, the team of Professor Moussa Benhamed from the Institute of Plant Sciences, Paris-Saclay University, France, published a recent research result entitled "HSFA1a modulates plant heat stress responses and alters the 3D chromatin organization of enhancer-promoter interactions" in the journal Nature Communications.

The sessile nature of plants makes them evolve complex and fine regulatory mechanisms to quickly respond to adverse effects of environmental changes, maintain a relatively stable intracellular environment to ensure normal growth and reproduction of plants. Previous studies have found that the three-dimensional structure of chromatin in Drosophila, Arabidopsis, and rice has changed to a certain extent in response to heat stress. In animals, the formation of chromatin loops (the interaction between chromatin) can depend on CTCF and Cohesin, etc., but CTCF, etc. are lacking in plants, and the formation mechanism of chromatin loops remains to be further studied. Therefore, exploring how plants induce chromatin reorganization in response to stress, and the relationship between dynamic changes in plant three-dimensional chromatin structure and gene regulation levels under stress conditions is crucial to plant growth and development. In this context, the team of Professor Moussa Benhamed took tomato as the research object, based on heat shock stress, highly integrated genetics, transcriptomics, chromatin openness analysis (ATAC-seq) and three-dimensional epigenomics technology (HiC, HiChIP, Capture HiC, 3C) and other methods to explore the mechanisms of chromatin dynamic regulation in plants under heat stress. This study reveals that under heat stress, the transcription factor HSFA1a, which is necessary for tomato heat stress tolerance, can mediate the interaction between enhancers and promoters and change the three-dimensional conformation of chromatin. This study reveals, for the first time in plants, the critical role of transcription factors in enhancer-promoter chromatin looping.

In addition, the study found through integrated analysis of ATAC-Seq and ChIP-Seq (H3K4me3, H3K9ac, H3K18ac, H3K27ac) data under different heat shock conditions (heat shock 0h, 1h, 6h): The distal and proximal regulatory elements (REs) in tomato showed distinct chromatin characteristics in response to heat shock, which laid the foundation for the subsequent in-depth study of distal and proximal REs.

Reference

Huang, Y., An, J., Sircar, S. et al. HSFA1a modulates plant heat stress responses and alters the 3D chromatin organization of enhancer-promoter interactions. Nat Commun 14, 469 (2023). https://doi.org/10.1038/s41467-023-36227-3