The super-pangenome of Populus unveil genomic facets for its adaptation and diversification in widespread forest trees

Understanding the underlying mechanisms and links between genome evolution and adaptive innovations stands as a key goal in evolutionary studies. Poplars, among the world’s most widely distributed and cultivated trees, exhibit extensive phenotypic diversity and environmental adaptability. In this study, we present a genus-level super-pangenome comprising 19 Populus genomes, revealing the likely pivotal role of private genes in facilitating local environmental and climate adaptation. Through the integration of pan-genomes with transcriptomes, methylomes and chromatin accessibility mapping, we unveil that the evolutionary trajectories of pan-genes and duplicated genes are closely linked to local genomic landscapes of regulatory and epigenetic architectures, notably CG methylation in gene-body regions. Further comparative genomic analyses have enabled the identification of 142,202 structural variants (SVs) across species, which intersect with a significant number of genes and contribute substantially to both phenotypic and adaptive divergence. We have experimentally validated a ∼180 bp presence/absence variant impacting the expression of the CUC2 gene, crucial for leaf serration formation. Finally, we developed a user-friendly web-based tool encompassing the multi-omics resources associated with the Populus super-pangenome (http://www.populus-superpangenome.com/). Together, the present pioneering super-pangenome resource in forest trees not only aid in the advancement of breeding efforts of this globally important tree genus but also offer valuable insights into potential avenues for comprehending tree biology.