Abstract
Understanding the evolutionary forces that influence patterns of gene expression variation will provide insights into the mechanisms of evolutionary change and the molecular basis of phenotypic diversity. To date, studies of gene expression evolution have primarily been made by analyzing how gene expression levels vary within and between species. However, the fundamental unit of heritable variation in transcript abundance is the underlying regulatory allele, and as a result it is necessary to understand gene expression evolution at the level of DNA sequence variation. Here we describe the evolutionary forces shaping patterns of genetic variation for 1206 cis-regulatory QTL identified in a cross between two divergent strains of Saccharomyces cerevisiae. We demonstrate that purifying selection against mildly deleterious alleles is the dominant force governing cis-regulatory evolution in S. cerevisiae and estimate the strength of selection. We also find that essential genes and genes with larger codon bias are subject to slightly stronger cis-regulatory constraint and that positive selection has played a role in the evolution of major trans-acting QTL.
Highlights
Gene expression is the primary intermediate between information encoded by the genome and higher order phenotypes, and as a result expression variation is thought to be an important source of phenotypic diversity
To study the evolutionary forces acting on regulatory polymorphisms, we took advantage of a large, well-studied data set of gene expression QTL discovered between the S. cerevisiae laboratory strain BY4716 (BY, isogenic to S288C) and the wild vineyard strain RM11-1a (RM) [11,20,21,22,23,24]
We refer to genes whose expression levels show linkage coincident with their own location as cis-acting QTL and, there appears to be a minor role for local trans-acting polymorphisms at these loci, we refer to the causative polymorphisms at these loci as cis-acting regulatory polymorphisms
Summary
Gene expression is the primary intermediate between information encoded by the genome and higher order phenotypes, and as a result expression variation is thought to be an important source of phenotypic diversity. A powerful paradigm to emerge in studies of gene expression variation has been the combination of microarray technology and genetic mapping, allowing many gene expression QTL to be identified [11,12,13,14,15,16,17,18,19]. Because these QTL point to regulatory polymorphisms that are the underlying units of heritable variation in transcript abundance, understanding the forces governing their evolution can provide detailed insights into gene expression diversity within populations and divergence between species. We made use of the known ancestral history of S288C to identify a key recent departure from mutation-purifying selection-drift equilibrium in the regulatory program of laboratory yeast
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