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      Major gene expression changes and epigenetic remodelling in Nile tilapia muscle after just one generation of domestication

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          ABSTRACT

          The historically recent domestication of fishes has been essential to meet the protein demands of a growing human population. Selection for traits of interest during domestication is a complex process whose epigenetic basis is poorly understood. Cytosine hydroxymethylation is increasingly recognized as an important DNA modification involved in epigenetic regulation. In the present study, we investigated if hydroxymethylation plays a role in fish domestication and demonstrated for the first time at a genome-wide level and single nucleotide resolution that the muscle hydroxymethylome changes after a single generation of Nile tilapia ( Oreochromis niloticus, Linnaeus) domestication. The overall decrease in hydroxymethylcytosine levels was accompanied by the downregulation of 2015 genes in fish reared in captivity compared to their wild progenitors. In contrast, several myogenic and metabolic genes that can affect growth potential were upregulated. There were 126 differentially hydroxymethylated cytosines between groups, which were not due to genetic variation; they were associated with genes involved in immune-, growth- and neuronal-related pathways. Taken together, our data unveil a new role for DNA hydroxymethylation in epigenetic regulation of fish domestication with impact in aquaculture and implications in artificial selection, environmental adaptation and genome evolution.

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          Most cited references43

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine.

            In contrast to 5-methylcytosine (5-mC), which has been studied extensively, little is known about 5-hydroxymethylcytosine (5-hmC), a recently identified epigenetic modification present in substantial amounts in certain mammalian cell types. Here we present a method for determining the genome-wide distribution of 5-hmC. We use the T4 bacteriophage β-glucosyltransferase to transfer an engineered glucose moiety containing an azide group onto the hydroxyl group of 5-hmC. The azide group can be chemically modified with biotin for detection, affinity enrichment and sequencing of 5-hmC-containing DNA fragments in mammalian genomes. Using this method, we demonstrate that 5-hmC is present in human cell lines beyond those previously recognized. We also find a gene expression level-dependent enrichment of intragenic 5-hmC in mouse cerebellum and an age-dependent acquisition of this modification in specific gene bodies linked to neurodegenerative disorders.
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              Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild.

              Captive breeding is used to supplement populations of many species that are declining in the wild. The suitability of and long-term species survival from such programs remain largely untested, however. We measured lifetime reproductive success of the first two generations of steelhead trout that were reared in captivity and bred in the wild after they were released. By reconstructing a three-generation pedigree with microsatellite markers, we show that genetic effects of domestication reduce subsequent reproductive capabilities by approximately 40% per captive-reared generation when fish are moved to natural environments. These results suggest that even a few generations of domestication may have negative effects on natural reproduction in the wild and that the repeated use of captive-reared parents to supplement wild populations should be carefully reconsidered.
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                Author and article information

                Journal
                Epigenetics
                Epigenetics
                Epigenetics
                Taylor & Francis
                1559-2294
                1559-2308
                7 April 2020
                2020
                7 April 2020
                : 15
                : 10
                : 1052-1067
                Affiliations
                [a ]Faculty of Biosciences and Aquaculture, Nord University; , Bodø, Norway
                [b ]Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology; , Trondheim, Norway
                [c ]Department of Computer Science, Norwegian University of Science and Technology; , Trondheim, Norway
                [d ]Bioinformatics Core facility-BioCore, Norwegian University of Science and Technology; , Trondheim, Norway
                [e ]K.G. Jebsen Center for Genetic Epidemiology, Norwegian University of Science and Technology; , Trondheim, Norway
                [f ]The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh; , Midlothian, UK
                Author notes
                CONTACT Jorge M. O. Fernandes jorge.m.fernandes@ 123456nord.no Nord University; Bodø8049, Norway
                Author information
                https://orcid.org/0000-0003-2560-5447
                https://orcid.org/0000-0001-7040-0892
                https://orcid.org/0000-0002-9616-5912
                https://orcid.org/0000-0002-2550-1640
                Article
                1748914
                10.1080/15592294.2020.1748914
                7116051
                32264748
                b41b9325-1854-4320-a17d-523639049cb0
                © 2020 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License ( http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way.

                History
                Page count
                Figures: 5, Tables: 1, References: 65, Pages: 16
                Categories
                Research Article
                Research Paper

                Genetics
                domestication,epigenetics,dna hydroxymethylation,muscle growth,oreochromis niloticus
                Genetics
                domestication, epigenetics, dna hydroxymethylation, muscle growth, oreochromis niloticus

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