Abstract

The superior performance of hybrids to parents, termed heterosis, has been widely utilized in animal and plant breeding programs, but the molecular mechanism underlying heterosis remains an enigma. RNA-Seq provides a novel way to investigate heterosis at the transcriptome-wide level, because gene expression functions as an intermediate phenotype that contributes to observable traits. Here we compared embryonic gene expression between chicken hybrids and their inbred parental lines to identify inheritance patterns of gene expression. Inbred Fayoumi and Leghorn were crossed reciprocally to obtain F1 fertile eggs. RNA-Seq was carried out using 24 brain and liver samples taken from day 12 embryos, and the differentially expressed (DE) genes were identified by pairwise comparison among the hybrids, parental lines, and mid-parent expression values. Our results indicated the expression levels of the majority of the genes in the F1 cross are not significantly different from the mid-parental values, suggesting additivity as the predominant gene expression pattern in the F1. The second and third prevalent gene expression patterns are dominance and over-dominance. Additionally, we found only 7–20% of the DE genes exhibit allele-specific expression in the F1, suggesting that trans regulation is the main driver for differential gene expression and thus contributes to heterosis effect in the F1 crosses.

Highlights

  • Crossbreeding for heterosis has tremendously improved agricultural production in recent centuries by taking advantage of non-additive genetic effects and producing progeny that exhibit greater qualities than both parents

  • Epistasis [5,6] have long been proposed to explain the mechanistic bases of heterosis, which emphasize the effect of advantageous alleles, heterozygosity, and interaction of genes for multigenic traits, respectively

  • When comparing gene expression between F1 crosses and the inbred parental lines, we found additivity was the predominant gene expression pattern and dominance and over-dominance were the second and third, respectively

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Summary

Introduction

Crossbreeding for heterosis has tremendously improved agricultural production in recent centuries by taking advantage of non-additive genetic effects and producing progeny that exhibit greater qualities than both parents. Heterosis has been intensively exploited by breeders to obtain desirable agronomic traits, laborious research effort is needed to identify varieties that result in useful heterosis when crossed. Identification of such plant or animal varieties may be facilitated by understanding the molecular basis of heterosis. Epistasis [5,6] have long been proposed to explain the mechanistic bases of heterosis, which emphasize the effect of advantageous alleles, heterozygosity, and interaction of genes for multigenic traits, respectively. Due to technological limitations, these hypotheses have remained overly unexamined up until the advent of genome-wide methods for polymorphisms and gene expression analysis. Variation in gene expression, such as differential gene expression between parents and hybrids and allele-specific expression (ASE)

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