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

F He,A Beyer,J De Meaux,K A Steige,U Göbel,P D Keightley,V Kovacova,M Bouzid

doi:10.1038/s41467-021-23558-2

F He, A Beyer + Show 6 more

Open Access

https://doi.org/10.1038/s41467-021-23558-2

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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.

Highlights

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
We investigate how cis-acting modifications have shaped the divergence in gene expression of the sister species A. lyrata and A. halleri in reaction to stress triggered by acute dehydration
Results indicate that mutations increasing expression plasticity to dehydration stress were favored in A. lyrata, whereas mutations decreasing stress plasticity were more frequent in A. halleri

Summary

Introduction

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. We identified those genes whose basal expression differed from A thaliana in the same direction as the plastic reaction to dehydration observed in this outgroup species and called such genetic changes in “orthoplastic” (Fig. 2A).

Results

Conclusion