Evolution of cis- and trans-regulatory divergence in the chicken genome between two contrasting breeds analyzed using three tissue types at one-day-old

Qiong Wang,Zhihua Jiang,Xiang Zhou,Yuan Wang,Zebin Zhang,Junying Li,Lujiang Qu,Yaxiong Jia,Ning Yang,Changsheng Nie

doi:10.1186/s12864-019-6342-5

Abstract

BackgroundGene expression variation is a key underlying factor influencing phenotypic variation, and can occur via cis- or trans-regulation. To understand the role of cis- and trans-regulatory variation on population divergence in chicken, we developed reciprocal crosses of two chicken breeds, White Leghorn and Cornish Game, which exhibit major differences in body size and reproductive traits, and used them to determine the degree of cis versus trans variation in the brain, liver, and muscle tissue of male and female 1-day-old specimens.ResultsWe provided an overview of how transcriptomes are regulated in hybrid progenies of two contrasting breeds based on allele specific expression analysis. Compared with cis-regulatory divergence, trans-acting genes were more extensive in the chicken genome. In addition, considerable compensatory cis- and trans-regulatory changes exist in the chicken genome. Most importantly, stronger purifying selection was observed on genes regulated by trans-variations than in genes regulated by the cis elements.ConclusionsWe present a pipeline to explore allele-specific expression in hybrid progenies of inbred lines without a specific reference genome. Our research is the first study to describe the regulatory divergence between two contrasting breeds. The results suggest that artificial selection associated with domestication in chicken could have acted more on trans-regulatory divergence than on cis-regulatory divergence.

Highlights

Gene expression variation is a key underlying factor influencing phenotypic variation, and can occur via cis- or trans-regulation
We picked singlenucleotide polymorphisms (SNPs) that were homozygous in each parental bird but different from each other in the same cross, resulting in two heterozygous SNP lists with 1.4 million heterozygous SNPs on average for the two reciprocal crosses, individually, to identify the allele-specific RNA-Seq reads of the offspring in the following steps
Our results suggest that trans-regulatory divergence genes were subjected to high selective constraint in the course of chicken domestication and could have been under stronger artificial selection, which is consistent with the findings of similar studies in mice [11] that reported that trans-regulated genes exhibited greater sequence conservation based on the computed Genomic Evolutionary Profiling scores for each exon

Summary

Introduction

Gene expression variation is a key underlying factor influencing phenotypic variation, and can occur via cis- or trans-regulation. Numerous transcriptional regulatory factors, which can be classified into cis-regulatory elements and trans-regulatory factors, regulate gene expression [1]. Cis-regulatory elements, such as promoters, enhancers, and silencers, are regions of non-coding DNA, which regulate the transcription of nearby genes. Trans-regulatory factors regulate (or modify) the expression of distant genes by combining with their target sequences [1, 2]. Cis- and trans-regulatory elements are thought to vary based on key genetic and evolutionary properties [5, 6]. Cis-regulatory elements regulate gene expression in an allele-specific manner. Cis-regulatory variation heterozygotes express allelic imbalances at the transcriptional and translational levels. Beneficial cis-regulatory variants are more likely to be enriched to fixation in the course of

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