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

Abstract

Rising temperatures increasingly threaten plant survival, particularly for long-lived forest trees that face repeated exposure to extreme climatic events. However, the specific mechanisms underlying transient transcriptomic and epigenetic responses to thermal stress, and how these relate to 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 responses related to thermotolerance, we integrated transcriptomic, methylomic, and small RNAome profiling under control, heat-stress, and recovery conditions, alongside population-scale genome resequencing. In addition to an extensive transcriptomic response to heat stress, our findings uncover immediate 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 are under stronger purifying selection and exhibit epigenetic priming that may be maintained over evolutionary timescales. We infer that the epigenetic plasticity provided by dynamic CHH methylation and TEs likely acts as a crucial short-term buffer for plant survival, modulating vital stress-response genes that are further maintained by strict evolutionary constraints over long timescales. This study offers novel insights into how forest trees balance transient epigenetic flexibility with enduring genetic stability to survive accelerating climate change.