Natural Variation in Abiotic Stress Responsive Gene Expression and Local Adaptation to Climate in Arabidopsis thaliana

TLDR

Gene expression varies widely in natural populations, but the proximate and ultimate causes of this variation and its impact on abiotic stress tolerance, fitness, and adaptation remain poorly understood. The study tested whether genes with natural genetic variation in their expression responses to abiotic stress are involved in local adaptation to climate in Arabidopsis thaliana. The authors compared genes with consistent expression responses to environmental stress (eSR) to genes with genetically variable responses (eGEI) to assess differences in promoter polymorphism, climate association, and regulatory element variation. Genes with eGEI in drought or cold showed higher promoter polymorphism, stronger climate associations, and more polymorphic ABA‑responsive elements, whereas eSR genes displayed lower promoter diversity, fewer nonsynonymous variants, and greater haplotype sharing, indicating purifying selection or sweeps, and suggesting that cis‑regulatory evolution of stress‑responsive expression contributes to local adaptation.

Abstract

Gene expression varies widely in natural populations, yet the proximate and ultimate causes of this variation are poorly known. Understanding how variation in gene expression affects abiotic stress tolerance, fitness, and adaptation is central to the field of evolutionary genetics. We tested the hypothesis that genes with natural genetic variation in their expression responses to abiotic stress are likely to be involved in local adaptation to climate in Arabidopsis thaliana. Specifically, we compared genes with consistent expression responses to environmental stress (expression stress responsive, "eSR") to genes with genetically variable responses to abiotic stress (expression genotype-by-environment interaction, "eGEI"). We found that on average genes that exhibited eGEI in response to drought or cold had greater polymorphism in promoter regions and stronger associations with climate than those of eSR genes or genomic controls. We also found that transcription factor binding sites known to respond to environmental stressors, especially abscisic acid responsive elements, showed significantly higher polymorphism in drought eGEI genes in comparison to eSR genes. By contrast, eSR genes tended to exhibit relatively greater pairwise haplotype sharing, lower promoter diversity, and fewer nonsynonymous polymorphisms, suggesting purifying selection or selective sweeps. Our results indicate that cis-regulatory evolution and genetic variation in stress responsive gene expression may be important mechanisms of local adaptation to climatic selective gradients.