The Populus pruinosa is a relic plant that has managed to survive in extremely harsh desert environments. Owing to intensifying global warming and desertification, research into ecological adaptation and speciation of P. pruinosa has attracted considerable interest, but the lack of a chromosome-scale genome has limited adaptive evolution research. Here, a 521.09 Mb chromosome-level reference genome of P. pruinosa was reported. Genome evolution and comparative genomic analysis revealed that tandemly duplicated genes and expanded gene families in P. pruinosa contributed to adaptability to extreme desert environments (especially high salinity and drought). The long terminal repeat retrotransposons (LTR-RTs) inserted genes in the gene body region might drive the adaptive evolution of P. pruinosa and species differentiation in saline-alkali desert environments. We recovered genetic differentiation in the populations of the northern Tianshan Mountain and southern Tianshan Mountain through whole-genome resequencing of 156 P. pruinosa individuals from 25 populations in China. Further analyses revealed that precipitation drove the local adaptation of P. pruinosa populations via some genetic sites, such as MAG2-interacting protein 2 (MIP2) and SET domain protein 25 (SDG25). This study will provide broad implications for adaptative evolution and population studies by integrating internal genetic and external environmental factors in P. pruinosa.

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