Multi-omics analysis links short-term epigenetic plasticity to long-term genetic adaptation to heat stress in a montane tree species

Rising temperatures increasingly threaten plant survival, particularly for long-lived forest trees repeated exposed to extreme climatic events. However, the specific mechanisms underlying transient transcriptomic and epigenetic responses to thermal stress, and how these responses are shaped by evolutionary selection, remain poorly understood. Here, we present a near-telomere-to-telomere genome assembly of Populus wilsonii, a montane tree species endemic to the eastern Hengduan Mountains. To investigate the multi-omic basis of thermotolerance, we integrated transcriptomic, methylomic, and small RNAome profiling under control, heat stress, and recovery conditions, with population-scale genome resequencing. In addition to revealing extensive transcriptomic responses to heat stress, our findings uncovered rapid regulatory mechanisms-including transposable element (TE) activation and repression, CHH methylation reprogramming, and small RNA-mediated pathways-that collectively modulate heat-responsive gene expression. Furthermore, population genomic analyses revealed that these heat-induced genes were under stronger purifying selection and exhibited epigenetic priming that may be maintained over evolutionary timescales. We infer that the epigenetic plasticity conferred by dynamic CHH methylation and TE activity likely acts as a crucial short-term buffer that promotes plant survival by modulating vital stress-response genes subjected to strong evolutionary constraints over longer timescales. This study provides new insights into how forest trees balance transient epigenetic flexibility with enduring genetic stability to survive accelerating climate change.