Abstract Understanding the underlying mechanisms between genome evolution and phenotypic and adaptive innovations is a key goal of evolutionary studies. Poplars are the world’s most widely distributed and cultivated trees, with extensive phenotypic diversity and environmental adaptability. Here we report a genus-level super-pangenome of 19 Populus genomes. After integrating pan-genomes with transcriptomes, methylomes and chromatin accessibility mapping, we reveal that the evolutionary fate of pan-genes and duplicated genes are largely associated with local genomic landscapes of regulatory and epigenetic architectures. Further comparative genomic analyses enabled to identify 142,202 structural variations (SVs) across species, which overlap with substantial genes and play key roles in both phenotypic and adaptive divergence. We experimentally validated a ∼180 bp presence/absence variant located in the promoter of the CUC2 gene, which contributed critically to leaf serration divergence between species. Together, this first super-pangenome resource in forest trees will not only accelerate molecular functional studies and genetic breeding of this globally important tree genus, but also lays a foundation for our understanding of tree biology.

The super-pangenome ofPopulusunveil genomic facets for adaptation and diversification in widespread forest trees