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For trees originating from boreal and temperate regions, the dormancy‐to‐active transition, also known as bud dormancy release and bud break, are crucial processes that allow trees to reactive growth in the spring. The molecular mechanisms underlying these two processes remain poorly understood. Here, through integrative multiomics analysis of the transcriptome, DNA methylome, and proteome, we gained insights into the reprogrammed cellular processes associated with bud dormancy release and bud break. Our findings revealed multilayer regulatory landscapes governing bud dormancy release and bud break regulation, providing a valuable reference framework for future functional studies. Based on the multiomics analysis, we have determined a novel long intergenic noncoding RNA named Phenology Responsive Intergenic lncRNA 1 (PRIR1) plays a role in the activation of bud break. that the molecular mechanism of PRIR1 has been preliminary explored, and it may partially promote bud break by activating its neighbouring gene, EXORDIUM LIKE 5 (PtEXL5), which has also been genetically confirmed as an activator for bud break. This study has revealed a lncRNA‐mediated regulatory mechanism for the control of bud break in Populus, operating independently of known regulatory pathways. Summary statement: we report the multilayer regulatory landscapes of dormancy release and bud break regulation in hybrid poplar (Populus tremula x alba). We also identify a long intergenic noncoding RNA PRIR1 and characterise its role in dormancy release. Our study provides a useful reference framework for dormancy release and bud break regulation studies. [ABSTRACT FROM AUTHOR]

For perennials in boreal and temperate ecosystems, bud dormancy is crucial for survival in harsh winter. Dormancy is released by prolonged exposure to low temperatures and is followed by reactive growth in the spring. Lysine acetylation (Kac) is one of the major post‐translational modifications (PTMs) that are involved in plant response to environmental signals. However, little information is available on the effects of Kac modification on bud dormancy release. Here, we report the dynamics of lysine acetylome in hybrid poplar (Populus tremula × Populus alba) dormant buds. A total of 7,594 acetyl‐sites from 3,281 acetyl‐proteins were identified, representing a large dataset of lysine acetylome in plants. Of them, 229 proteins were differentially acetylated during bud dormancy release and were mainly involved in the primary metabolic pathways. Site‐directed mutagenesis enzymatic assays showed that Kac strongly modified the activities of two key enzymes of primary metabolism, pyruvate dehydrogenase (PDH) and isocitrate dehydrogenase (IDH). We thus propose that Kac of enzymes could be an important strategy for reconfiguration of metabolic processes during bud dormancy release. In all, our results reveal the importance of Kac in bud dormancy release and provide a new perspective to understand the molecular mechanisms of seasonal growth of trees. We report the dynamics of lysine acetylome in hybrid poplar (Populus tremula × Populus alba) dormant buds and reveal their involvements in reconfiguring metabolic processes during bud dormancy release. Our study gives a new perspective to understand the molecular mechanisms on how trees adapt to the seasonal climate changes. [ABSTRACT FROM AUTHOR]