A heat stress-responsive epigenome defines the dynamic 3D chromatin structure in Chinese cabbage

Plants have evolved genome plasticity to adapt to fluctuating environments. However, how environmental cues induce dynamic chromatin remodeling in plants remains largely unclear. Here, we report a close relationship between the epigenome and the 3D chromatin structure in the plant response to heat stress. Through Hi-C, whole-genome bisulfite sequencing, and transcriptome analyses in Chinese cabbage (Brassica rapa), we found that heat stress rapidly induces chromatin compaction and aggregation predominantly in centromeric and telomeric regions. Heat stress also markedly altered A/B compartment transitions and the number and length of TAD-like domains and loops, as well as genome-wide DNA methylation profiles that were linked to the maintenance of chromatin stability and transcription levels. We simulated and inferred an unexpected "Rabl" model for chromatin distribution in leaf cell nuclei of Chinese cabbage seedlings. Furthermore, CHH methylation (mCHH) was associated with morphological fluctuations in chromatin under heat stress. Thus, the heat stress-responsive epigenome might be involved in defining the dynamic 3D chromatin structure through mCHH-directed changes in DNA-DNA and/or DNA-protein interactions within centromeric regions. Such chromatin structural dynamics may also have a feedback influence on epigenome establishment under heat stress in Chinese cabbage.