Detection of a Cis eQTL Controlling BMCO1 Gene Expression Leads to the Identification of a QTG for Chicken Breast Meat Color

Elisabeth Le Bihan-Duval,Benoît Graulet,Olivier Demeure,Frédérique Pitel,Cécile Duby,Michel J Duclos,Sandrine Lagarrigue,Catherine M Beaumont,Estelle Godet,Javad Nadaf,Larry A Cogburn,Cécile Berri,Sophie Y Leroux

doi:10.1371/journal.pone.0014825

Abstract

Classical quantitative trait loci (QTL) analysis and gene expression QTL (eQTL) were combined to identify the causal gene (or QTG) underlying a highly significant QTL controlling the variation of breast meat color in a F2 cross between divergent high-growth (HG) and low-growth (LG) chicken lines. Within this meat quality QTL, BCMO1 (Accession number GenBank: AJ271386), encoding the β-carotene 15, 15′-monooxygenase, a key enzyme in the conversion of β-carotene into colorless retinal, was a good functional candidate. Analysis of the abundance of BCMO1 mRNA in breast muscle of the HG x LG F2 population allowed for the identification of a strong cis eQTL. Moreover, reevaluation of the color QTL taking BCMO1 mRNA levels as a covariate indicated that BCMO1 mRNA levels entirely explained the variations in meat color. Two fully-linked single nucleotide polymorphisms (SNP) located within the proximal promoter of BCMO1 gene were identified. Haplotype substitution resulted in a marked difference in BCMO1 promoter activity in vitro. The association study in the F2 population revealed a three-fold difference in BCMO1 expression leading to a difference of 1 standard deviation in yellow color between the homozygous birds at this haplotype. This difference in meat yellow color was fully consistent with the difference in carotenoid content (i.e. lutein and zeaxanthin) evidenced between the two alternative haplotypes. A significant association between the haplotype, the level of BCMO1 expression and the yellow color of the meat was also recovered in an unrelated commercial broiler population. The mutation could be of economic importance for poultry production by making possible a gene-assisted selection for color, a determining aspect of meat quality. Moreover, this natural genetic diversity constitutes a new model for the study of β-carotene metabolism which may act upon diverse biological processes as precursor of the vitamin A.

Highlights

For more than half of a century, commercial poultry breeding programs have focused mainly on improvements of two major production traits, growth rate and feed efficiency, in meat-type chickens
Our study supports the conclusion that BCMO1 is the gene underlying the chicken meat color quantitative trait loci (QTL) on GGA11, through a cis expression QTL (eQTL) controlling its expression
If no results were obtained for the first mutation, the second mutation alters a Vitamin D receptor (VDR), a DR5 binding site detected only with the A allele

Summary

Introduction

For more than half of a century, commercial poultry breeding programs have focused mainly on improvements of two major production traits, growth rate and feed efficiency, in meat-type (broiler) chickens. Different experimental lines of chickens have been created to increase our understanding of genetic control over other important production traits, including meat quality. Our unique model is a population of meat-type chickens that was divergently selected for high (HG) or low growth (LG) rate, based on a difference in body weight (BW) at both 8 and 36 weeks of age [1]. The HG and LG broiler lines have been extensively studied to understand the physiological and genetic basis of marked differences in growth rate and skeletal muscle development [4,5].

Methods

Results

Conclusion