The evolution and functional divergence of the beta-carotene oxygenase gene family in teleost fish—Exemplified by Atlantic salmon |
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Authors: | Hanna Helgeland,Simen Rø d Sandve,Jacob Seilø Torgersen,Mari Kyllesø Halle,Hilde Sundvold,Stig Omholt,Dag Inge Vå ge |
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Affiliation: | 1. Centre for Integrative Genetics (CIGENE), Dept. of Animal and Aquacultural Sciences, Norwegian University of Life Sciences (UMB), P.O. Box 5003, N-1432 As, Norway;2. Centre for Integrative Genetics (CIGENE), Dept. of Plant and Environmental Sciences, Norwegian University of Life Sciences (UMB), P.O. Box 5003, N-1432 As, Norway;3. Nofima AS, PO Box 5010, N-1432 Ås, Norway |
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Abstract: | In mammals, two carotenoid cleaving oxygenases are known; beta-carotene 15,15′-monooxygenase (BCMO1) and beta-carotene 9′,10′-oxygenase (BCO2). BCMO1 is a key enzyme in vitamin A synthesis by symmetrically cleaving beta-carotene into 2 molecules of all-trans-retinal, while BCO2 is responsible for asymmetric cleavage of a broader range of carotenoids. Here, we show that the Atlantic salmon beta-carotene oxygenase (bco) gene family contains 5 members, three bco2 and two bcmo1 paralogs. Using public sequence databases, multiple bco genes were also found in several additional teleost species. Phylogenetic analysis indicates that bco2a and bco2b originate from the teleost fish specific genome duplication (FSGD or 3R), while the third and more distant paralog, bco2 like, might stem from a prior duplication event in the teleost lineage. The two bcmo1 paralogs (bcmo1 and bcmo1 like) appear to be the result of an ancient duplication event that took place before the divergence of ray-finned (Actinopterygii) and lobe-finned fish (Sarcopterygii), with subsequent nonfunctionalization and loss of one Sarcopterygii paralog. Gene expression analysis of the bcmo1 and bco2 paralogs in Atlantic salmon reveals regulatory divergence with tissue specific expression profiles, suggesting that the beta-carotene oxygenase subtypes have evolved functional divergences. We suggest that teleost fish have evolved and maintained an extended repertoire of beta-carotene oxygenases compared to the investigated Sarcopterygii species, and hypothesize that the main driver behind this functional divergence is the exposure to a diverse set of carotenoids in the aquatic environment. |
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Keywords: | aa, amino acid(s) ANOVA, analysis of variance BCMO1, beta-carotene 15,15&prime -monooxygenase bco, beta-carotene oxygenase BCO2, beta-carotene 9&prime ,10&prime -oxygenase bp, base pair(s) cDNA, DNA complementary to RNA ef1a, elongation factor 1-alpha EST, expressed sequence tag FSGD, fish-specific genome duplication ICSASG, International Collaboration to Sequence the Atlantic Salmon Genome MAFFT, Multiple Alignment using Fast Fourier Transform MEGA, Molecular Evolutionary Genetics Analysis ML, maximum likelihood MYA, million years ago NCBI, National Center for Biotechnology Information NIVA, Norwegian Institute for Water Research PCR, polymerase chain reaction qRT-PCR, quantitative real-time PCR RPE65, retinal pigment epithelium-specific 65 kDa protein |
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