Linking genomic signatures of selection to expression variation and direct evidence of local adaptation

Understanding how genomic and expression variation is linked to adaptation of plants to local environments is fundamental to the fields of evolutionary biology and species conservation. Using locally adapted Arabidopsis thaliana Italy and Sweden populations, we examine how variation in gene expression under control and cold acclimation conditions, is linked to allele frequency differentiation (AFD); linkage disequilibrium (LD); selective constraint at nonsynonymous sites; and genetic-tradeoff quantitative trait loci (GT-QTL). Our results indicate that contrary to genes showing a main effect in environment (E), expression genotype by environment interactions (GxE) show significantly higher AFD along cis-regulatory and nonsynonymous sites than the neutral expectation; and interestingly, highly differentiated GxE genes show higher expression and inter-species selective constraint than the rest of the genes. When examining the association between genomic signatures of selection along GxE/E genes and GT-QTL, we find that GxE genes showing a high AFD and LD, display a significant and much higher enrichment along GT-QTL than the genome-wide/E set of genes. Nonetheless, E genes show a higher enrichment than the genome-wide control. In summary, our results suggest, that these highly expressed and selectively constrained GxE genes, may have been part of a cold-responsive regulon of E genes that experienced recent selection when migrating to new environments. Candidate GxE genes underlying GT-QTL reveal interesting biological processes that may underlie local adaptation to temperature, including flowering time, light-dependent cold acclimation, freezing tolerance, and response to hypoxia. Finally, we find no evidence linking lower expression of the CBF-dependent freezing tolerance pathway to genetic-tradeoffs and adaptation to warmer climates.