Cis-regulatory evolution spotlights species differences in the adaptive potential of gene expression plasticity

Abstract

Phenotypic plasticity is the variation in phenotype that a single genotype can produce in different environments and, as such, is an important component of individual fitness. However, whether the effect of new mutations, and hence evolution, depends on the direction of plasticity remains controversial. Here, we identify the cis-acting modifications that have reshaped gene expression in response to dehydration stress in three Arabidopsis species. Our study shows that the direction of effects of most cis-regulatory variants differentiating the response between A. thaliana and the sister species A. lyrata and A. halleri depends on the direction of pre-existing plasticity in gene expression. A comparison of the rate of cis-acting variant accumulation in each lineage indicates that the selective forces driving adaptive evolution in gene expression favors regulatory changes that magnify the stress response in A. lyrata. The evolutionary constraints measured on the amino-acid sequence of these genes support this interpretation. In contrast, regulatory changes that mitigate the plastic response to stress evolved more frequently in A. halleri. Our results demonstrate that pre-existing plasticity may be a stepping stone for adaptation, but its selective remodeling differs between lineages.

Strength of purifying selection on the amino-acid sequence is associated with the amount of non-additive variance in gene expression.

“…In order to differentiate these alternatives, the segregation of molecular variation within species can be used to infer the fitness effect of new mutations and quantify the strength of the evolutionary constraints imposed on the amino-acid sequence. We took advantage of a previous study, which determined the demographic history of the same two parental populations of A. lyrata 25,32 . We inferred the distribution of fitness effects (DFE) of new non-synonymous variants in these gene sets, following a method described in 25 that incorporates the specific demographic parameters of each population (Supplementary Figure S3).…”

Positive selection and heat‐response transcriptomes reveal adaptive features of the Brassicaceae desert model, Anastatica hierochuntica

“…The contrasting global transcriptome responses of A. thaliana , E. salsugineum and A. hierochuntica to stress also emphasize the importance of generation and maintenance of new cis ‐acting elements in the adaptive evolution of plants to extreme habitats (Oh et al ., 2014 ; He et al ., 2021 ).…”

Environmental response in gene expression and DNA methylation reveals factors influencing the adaptive potential ofArabidopsis lyrata

“…We found that environmentally induced expression responses were highly consistent across our experimental plants, indicating that regulatory elements (both cis and trans ) are largely conserved between the three A. lyrata populations. Previous studies examining environmentally responsive genes have found that the regulatory conservation is frequently associated with the conservation of the gene product (He et al, 2021; Hodgins et al, 2016; Hunt et al, 2013; Lasky et al, 2014; Lowry et al, 2013; Zhang et al, 2017). Although our results qualitatively support these findings, as genes showing consistent expression responses to the environment (DEG ~ Field) were under stronger purifying selection than those showing genetically variable responses (DEG ~ Field:Population), we discovered that both gene sets exhibited stronger than expected signals of evolutionary constraint.…”

“…In most cases, plasticity in morphological, developmental, and physiological traits is thought to result from changes in gene expression (West-Eberhard, 2003), making the study of expression plasticity a promising approach for uncovering the genetic basis of phenotypic plasticity. Although studies of environmentally responsive genes have discovered a wide range of expression responses (Hodgins-Davis and Townsend, 2009), many populations and species have reacted consistently to environmental stress (He et al, 2021; Lowry et al, 2013; Wos et al, 2021a; Yeaman et al, 2014). As gene expression is primarily controlled by regulatory elements acting either in cis (affecting nearby genes) or trans (affecting distant genes), the conserved expression responses are indicative of conserved regulatory systems (Horvath et al, 2021; Lu et al, 2019; Rodgers-Melnick et al, 2016).…”