Epigenetic reprogramming drives the annual growth-dormancy cycle in Populus

The seasonal growth-dormancy cycle is a critical adaptive trait that enables perennials from boreal and temperate regions to survive winter. This cycle is largely governed by spatiotemporal gene activity in the shoot apex, where chromatin states dynamically respond to seasonal environmental cues. However, the chromatin regulatory mechanisms underlying this response remain poorly understood. Here, we characterize chromatin dynamics in Populus shoot meristems across 5 key stages of the annual growth-dormancy cycle. By integrating data on chromatin accessibility, histone modifications, and transcriptomic dynamics, we reveal stage-specific and distinct (proximal-distal) chromatin reprogramming events that closely align with transcriptomic changes. We further demonstrate that deposition of the repressive histone mark H3K27me3 by the Polycomb Repressive Complex 2 plays a vital role in regulating growth-dormancy transitions. Manipulation of Populus LIKE HETEROCHROMATIN PROTEIN 1 (PtLHP1) expression alters dormancy release and bud break in hybrid poplar. PtLHP1 extensively co-localized with H3K27me3-marked chromatin regions, supporting its role in maintaining H3K27me3 homeostasis during seasonal transitions. Our study provides a comprehensive epigenetic landscape of seasonal growth regulation in trees and identifies potential molecular targets for understanding the mechanisms underlying phenological plasticity.