A mechanism for red coloration in vertebrates

Red coloration is a salient feature of the natural world. Many vertebrates produce red color by converting dietary yellow carotenoids into red ketocarotenoids via an unknown mechanism. Here, we show that two enzymes, cytochrome P450 2J19 (CYP2J19) and 3-hydroxybutyrate dehydrogenase 1-like (BDH1L),...

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Published in:Current biology Vol. 32; no. 19; pp. 4201 - 4214.e12
Main Authors: Toomey, Matthew B., Marques, Cristiana I., Araújo, Pedro M., Huang, Delai, Zhong, Siqiong, Liu, Yu, Schreiner, Gretchen D., Myers, Connie A., Pereira, Paulo, Afonso, Sandra, Andrade, Pedro, Gazda, Małgorzata A., Lopes, Ricardo J., Viegas, Ivan, Koch, Rebecca E., Haynes, Maureen E., Smith, Dustin J., Ogawa, Yohey, Murphy, Daniel, Kopec, Rachel E., Parichy, David M., Carneiro, Miguel, Corbo, Joseph C.
Format: Journal Article
Language:English
Published: England Elsevier Inc 10-10-2022
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Summary:Red coloration is a salient feature of the natural world. Many vertebrates produce red color by converting dietary yellow carotenoids into red ketocarotenoids via an unknown mechanism. Here, we show that two enzymes, cytochrome P450 2J19 (CYP2J19) and 3-hydroxybutyrate dehydrogenase 1-like (BDH1L), are sufficient to catalyze this conversion. In birds, both enzymes are expressed at the sites of ketocarotenoid biosynthesis (feather follicles and red cone photoreceptors), and genetic evidence implicates these enzymes in yellow/red color variation in feathers. In fish, the homologs of CYP2J19 and BDH1L are required for ketocarotenoid production, and we show that these enzymes are sufficient to produce ketocarotenoids in cell culture and when ectopically expressed in fish skin. Finally, we demonstrate that the red-cone-enriched tetratricopeptide repeat protein 39B (TTC39B) enhances ketocarotenoid production when co-expressed with CYP2J19 and BDH1L. The discovery of this mechanism of ketocarotenoid biosynthesis has major implications for understanding the evolution of color diversity in vertebrates. [Display omitted] •Avian CYP2J19 and BDH1L together convert dietary carotenoids into ketocarotenoids•TTC39B enhances the production of ketocarotenoids by CYP2J19 and BDH1L•BDH1L alone converts dietary carotenoids into ε,ε-carotenoids•Homologs of CYP2J19 and BDH1L mediate ketocarotenoid biosynthesis in fish Red ketocarotenoid-based coloration is an important signal for many vertebrates. Toomey et al. describe a two-step enzymatic mechanism that mediates the production of ketocarotenoids in birds and fish. This work opens new avenues for understanding the evolution and function of red coloration in vertebrates.
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Lead Contact: Joseph C. Corbo
Twitter handles: @mbtoomey; @evolgenCIBIO; @CorboLab
M.B.T., M.C., and J.C.C. conceived the project. M.B.T., D.J.S., M.E.H., M.C., C.I.M., P.M.A., P.P., S.A., P.A., M.A.G., R.J.L., I.V., S.Z., R.E. Kopec, R.E. Koch, D.H., D.M.P., Y.L., G.D.S., C.A.M., Y.O., D.M., and J.C.C. performed the experiments and/or analyzed the data. M.B.T., M.C., and J.C.C. supervised and administered the project. M.B.T., M.C., R.E. Kopec, D.M.P., and J.C.C. acquired funding for the project. M.B.T., M.C., and J.C.C. wrote the manuscript with input from all authors.
Present address: Institut Pasteur, Université de Paris, CNRS UMR 3525, INSERM UA12, Comparative Functional Genomics group, F-75015 Paris, France.
AUTHOR CONTRIBUTIONS
ISSN:0960-9822
1879-0445
DOI:10.1016/j.cub.2022.08.013