Integrated pangenomics and population genomics reveal climate adaptation and maladaptation in an East Asian tree

Characterizing genomic variation in keystone forest trees is critical for understanding and predicting the adaptation and maladaptation of terrestrial ecosystems to global climate change. In this study, we integrate five high-quality genomes and high-depth whole-genome resequencing data from 222 individuals across 44 natural populations of Populus davidiana in East Asia. Our findings reveal that genome divergence strongly correlates with epigenetic and regulatory features, with variable genomic regions closely associated with dynamic transposon activity linked to epigenetic modifications. A population-scale genotype-environment association analysis identifies 10,372 adaptive single nucleotide polymorphisms (SNPs) and 1322 adaptive structural variations (SVs). Among these, a temperature-associated SV and a precipitation-associated SV undergo functional validation providing evidence of their roles in the expression of PdaMSL10, a mechanosensitive ion channel, and the transcription factor PdaWRKY40, respectively. Overexpression and RNAi experiments demonstrate that differential expression of PdaWRKY40 is strongly associated with drought sensitivity or tolerance, facilitating adaptation to diverse environmental conditions. Additionally, genomic vulnerability forecasts under future climate scenarios highlight the increasingly significant role of SVs in environmental adaptation. These findings advance our understanding of the genetic mechanisms underlying climate adaptation in non-model keystone species and provide invaluable genetic resources for breeding programs aimed at enhancing climate resilience.