Abstract
The genetic determination of eggshell coloration has not been determined in birds. Here we report that the blue eggshell is caused by an EAV-HP insertion that promotes the expression of SLCO1B3 gene in the uterus (shell gland) of the oviduct in chicken. In this study, the genetic map location of the blue eggshell gene was refined by linkage analysis in an F2 chicken population, and four candidate genes within the refined interval were subsequently tested for their expression levels in the shell gland of the uterus from blue-shelled and non-blue-shelled hens. SLCO1B3 gene was found to be the only one expressed in the uterus of blue-shelled hens but not in that of non-blue-shelled hens. Results from a pyrosequencing analysis showed that only the allele of SLCO1B3 from blue-shelled chickens was expressed in the uterus of heterozygous hens (O*LC/O*N). SLCO1B3 gene belongs to the organic anion transporting polypeptide (OATP) family; and the OATPs, functioning as membrane transporters, have been reported for the transportation of amphipathic organic compounds, including bile salt in mammals. We subsequently resequenced the whole genomic region of SLCO1B3 and discovered an EAV-HP insertion in the 5′ flanking region of SLCO1B3. The EAV-HP insertion was found closely associated with blue eggshell phenotype following complete Mendelian segregation. In situ hybridization also demonstrated that the blue eggshell is associated with ectopic expression of SLCO1B3 in shell glands of uterus. Our finding strongly suggests that the EAV-HP insertion is the causative mutation for the blue eggshell phenotype. The insertion was also found in another Chinese blue-shelled breed and an American blue-shelled breed. In addition, we found that the insertion site in the blue-shelled chickens from Araucana is different from that in Chinese breeds, which implied independent integration events in the blue-shelled chickens from the two continents, providing a parallel evolutionary example at the molecular level.
Highlights
Avian eggshell coloration is the result of crypsis or mimetism and plays important roles in filtering solar radiation and strengthening the eggshell [1]
The eggshell color of birds is of wide interest, but the molecular basis remained unknown until our discovery, reported here
We identified that blue eggshell in chickens from different geographical regions is caused by a,4.2 kb EAV-HP insertion in the 59 flanking region of SLCO1B3
Summary
Avian eggshell coloration is the result of crypsis or mimetism and plays important roles in filtering solar radiation and strengthening the eggshell [1]. Blue eggshell color has been proposed as post-mating signals of female phenotypic quality to their mates and is related to fitness of the offspring due to the antioxidant of biliverdin, a predominant pigment for blue eggs [2,3]. Protoporphyrin-IX, biliverdin, and biliverdin zinc chelate are the main pigments of the eggshell [10] and several blue egg laying breeds have been reported worldwide [11,12]. The Araucana, an indigenous breed from Chile, was the first chicken breed described to lay blue eggs [8], and has been frequently used in genetic studies of the blue eggshell phenotype. The blue eggshell phenotype has not been fixed in these three breeds which still produce brown eggs at low frequency
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