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Red Carotenoid Coloration in the Zebra Finch Is Controlled by a Cytochrome P450 Gene Cluster.


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Authors

Mundy, Nicholas I 
Stapley, Jessica 
Bennison, Clair 
Tucker, Rachel 
Twyman, Hanlu 

Abstract

Bright-red colors in vertebrates are commonly involved in sexual, social, and interspecific signaling [1-8] and are largely produced by ketocarotenoid pigments. In land birds, ketocarotenoids such as astaxanthin are usually metabolically derived via ketolation of dietary yellow carotenoids [9, 10]. However, the molecular basis of this gene-environment mechanism has remained obscure. Here we use the yellowbeak mutation in the zebra finch (Taeniopygia guttata) to investigate the genetic basis of red coloration. Wild-type ketocarotenoids were absent in the beak and tarsus of yellowbeak birds. The yellowbeak mutation mapped to chromosome 8, close to a cluster of cytochrome P450 loci (CYP2J2-like) that are candidates for carotenoid ketolases. The wild-type zebra finch genome was found to have three intact genes in this cluster: CYP2J19A, CYP2J19B, and CYP2J40. In yellowbeak, there are multiple mutations: loss of a complete CYP2J19 gene, a modified remaining CYP2J19 gene (CYP2J19(yb)), and a non-synonymous SNP in CYP2J40. In wild-type birds, CYP2J19 loci are expressed in ketocarotenoid-containing tissues: CYP2J19A only in the retina and CYP2J19B in the beak and tarsus and to a variable extent in the retina. In contrast, expression of CYP2J19(yb) is barely detectable in the beak of yellowbeak birds. CYP2J40 has broad tissue expression and shows no differences between wild-type and yellowbeak. Our results indicate that CYP2J19 genes are strong candidates for the carotenoid ketolase and imply that ketolation occurs in the integument in zebra finches. Since cytochrome P450 enzymes include key detoxification enzymes, our results raise the intriguing possibility that red coloration may be an honest signal of detoxification ability.

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Keywords

Animals, Avian Proteins, Beak, Cytochrome P-450 Enzyme System, Female, Finches, Male, Pigmentation, Pigments, Biological, Retina, Tarsus, Animal

Journal Title

Curr Biol

Conference Name

Journal ISSN

0960-9822
1879-0445

Volume Title

26

Publisher

Elsevier BV
Sponsorship
We thank the BBSRC (grant numbers BB/E017509/1 and BB/I02185X/1 to J. Sl., T. B, T. R. B), the EC Marie Curie International Outgoing Fellowship scheme (project 253300 to J. St.), the NERC Biomolecular Analysis Facility (NBAF961 to N.M., J. Sl.) and Murray Edwards College, Cambridge (N. M.) for funding. We thank Simon Griffith for wild zebra finch samples.