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Comparing gene expression patterns and genetic polymorphisms between populations is of central importance for understanding the origin and maintenance of biodiversity. Based on population-specific gene expression levels and allele frequency differences, we sought to identify population divergence (PD) genes across the introgression-resistant genomic regions of Populus trichocarpa. Genes containing highly diverged loci [i.e., genetic divergence (GD)] or showing expression divergence (ED) between populations were widely distributed in the genome and substantially enriched in functional categories related to stress responses, disease resistance, timing of flowering, cell cycle regulation, plant growth, and development. Nine genomic regions showing evidence of strong positive selection were overlapped with GD genes, which had significant differences between Oregon (a southernmost peripheral deme) and the other demes. However, we did not find evidence that genes under positive selection show an enrichment for ED. PD genes and genes under selection pertained to the same gene classes, such as SERINE/CYSTEINE PROTEASE, ABC TRANSPORTER, GLYCOSYLTRANSFERASE and other transferases. Our analysis also revealed that GD genes were polymorphic within the species (41.9 ± 3.66 biallelic variants per gene), as previously reported in herbaceous plants. By contrast, ED genes contained less genetic variants (10.73 ± 1.14) and were likely highly expressed. In addition, we found that trans- rather than cis-acting variants considerably contribute to the evolution of &gt;90% PD genes. Overall, this study elucidates that cohorts of PD genes agree with the general attributes of known speciation genes and GD genes will provide substrates for positive selection to operate on.

Transcriptome-wide analysis of introgression-resistant regions reveals genetic divergence genes under positive selection in Populus trichocarpa