Early fish domestication affects methylation of key genes involved in the rapid onset of the farmed phenotype

References

• Price EO. Domestication defined Price, EO. In: Animal domestication and behavior. New York: CABI Publishing; 2002. p. 10–12. ISBN: 0-85199-597-7.
   Google Scholar
• de Mestral LG, Herbinger CM. Reduction in antipredator response detected between first and second generations of endangered juvenile Atlantic salmon Salmo salar in a captive breeding and rearing programme. J Fish Biol. 2013;83(5):1268–1286.
   Google Scholar
• Trut L, Oskina I, Kharlamova A. Animal evolution during domestication: the domesticated fox as a model. BioEssays. 2009;31(3):349–360.
   Google Scholar
• Agnvall B, Bélteky J, Katajamaa R, et al. Is evolution of domestication driven by tameness? A selective review with focus on chickens. Appl Anim Behav Sci. 2018;205:227–233.
   Google Scholar
• Wilkins AS, Wrangham RW, Fitch WT. The “domestication syndrome” in mammals: a unified explanation based on neural crest cell behavior and genetics. Genetics. 2014;197(3):795–808.
   Google Scholar
• Chen X, Wang J, Qian L, et al. Domestication drive the changes of immune and digestive system of Eurasian perch (Perca fluviatilis). PLoS One. 2017;12(3):e0172903–e0172903.
   Google Scholar
• Rauw WM, Kanis E, Noordhuizen-Stassen EN, et al. Undesirable side effects of selection for high production efficiency in farm animals: a review. Livest Prod Sci. 1998;56(1):15–33.
   Google Scholar
• Selechnik D, Richardson, MF, Shine, R et al, et al. Bottleneck revisited: increased adaptive variation despite reduced overall genetic diversity in a rapidly adapting invader. Front Genet. 2019;10:1221.
   Google Scholar
• Christie MR, Marine ML, Fox SE, et al. A single generation of domestication heritably alters the expression of hundreds of genes. Nat Commun. 2016;7:10676.
   Google Scholar
• Christie MR, Marine ML, French RA, et al. Genetic adaptation to captivity can occur in a single generation. Proc Natl Acad Sci USA. 2012;109(1):238–242.
   Google Scholar
• Schmitz RJ, Schultz MD, Lewsey MG, et al. Transgenerational epigenetic instability is a source of novel methylation variants. Science. 2011;334(6054):369–373.
   Google Scholar
• Hu J, Barrett RDH. Epigenetics in natural animal populations. J Evol Biol. 2017;30(9):1612–1632.
   Google Scholar
• Feil R, Fraga MF. Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet. 2012;13:97.
   Google Scholar
• Tian F, Zhan F, VanderKraats ND, et al. DNMT gene expression and methylome in Marek’s disease resistant and susceptible chickens prior to and following infection by MDV. Epigenetics. 2013;8(4):431–444.
   Google Scholar
• Hu Y, Xu H, Li Z, et al. Comparison of the genome-wide DNA methylation profiles between fast-growing and slow-growing broilers. PLoS One. 2013;8(2):e56411.
   Google Scholar
• Adam A-C, Lie KK, Whatmore P, et al. Profiling DNA methylation patterns of zebrafish liver associated with parental high dietary arachidonic acid. PLoS One. 2019;14(8):e0220934.
   Google Scholar
• Pértille F, Brantsæter M, Nordgreen J, et al. DNA methylation profiles in red blood cells of adult hens correlate with their rearing conditions. J Exp Biol. 2017;220(19):3579.
   Google Scholar
• Gavery MR, Nichols KM, Goetz GW, et al. Characterization of genetic and epigenetic variation in sperm and red blood cells from adult hatchery and natural-origin steelhead. Oncorhynchus mykiss G3 (Bethesda). 2018;8(11):3723–3736.
   Google Scholar
• Gavery MR, Roberts SB. Epigenetic considerations in aquaculture. PeerJ. 2017;12(5):e4147.
   Google Scholar
• Diana JS. Aquaculture production and biodiversity conservation. BioScience. 2009;59(1):27–38.
   Google Scholar
• Teletchea F, Fontaine P. Levels of domestication in fish: implications for the sustainable future of aquaculture. Fish Fish. 2014;15(2):181–195.
   Google Scholar
• Wang D, Han S, Peng R, et al. DUSP28 contributes to human hepatocellular carcinoma via regulation of the p38 MAPK signaling. Int J Oncol. 2014;45(6):2596–2604.
   Google Scholar
• Segalés J, Perdiguero E, Muñoz-Cánoves P. Regulation of muscle stem cell functions: a focus on the p38 MAPK signaling pathway. Front Cell Dev Biol. 2016;4(91). DOI:10.3389/fcell.2016.00091
   Google Scholar
• Solomon AM, Bouloux PMG. Modifying muscle mass - the endocrine perspective. J Endocrinol. 2006;191(2):349–360.
   Google Scholar
• Jing E, O’Neill BT, Rardin MJ, et al. Sirt3 regulates metabolic flexibility of skeletal muscle through reversible enzymatic deacetylation. Diabetes. 2013;62(10):3404–3417.
   Google Scholar
• Palacios OM, Carmona JJ, Michan S, et al. Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1alpha in skeletal muscle. Aging (Albany Ny). 2009;1(9):771–783.
   Google Scholar
• Simo-Mirabet P, Perera E, Calduch-Giner JA, et al. Co-expression analysis of sirtuins and related metabolic biomarkers in juveniles of gilthead sea bream (Sparus aurata) with differences in growth performance. Front Physiol. 2018;9:608.
   Google Scholar
• Honda T, Inui M. PDZRN3 regulates differentiation of myoblasts into myotubes through transcriptional and posttranslational control of Id2. J Cell Physiol. 2019;234(3):2963–2972.
   Google Scholar
• Guiraud A, Couturier N, Buchman V, et al. Sh3kbp1 involvement during skeletal muscle fibers formation: a new candidate for centronuclear myopathies. Neuromuscul Disord. 2017;27:S248.
   Google Scholar
• Zhang W, Tong H, Zhang Z, et al. Transcription factor EGR1 promotes differentiation of bovine skeletal muscle satellite cells by regulating MyoG gene expression. J Cell Physiol. 2018;233(1):350–362.
   Google Scholar
• Edgett BA, Foster WS, Hankinson PB, et al. Dissociation of increases in PGC-1α and its regulators from exercise intensity and muscle activation following acute exercise. PLoS One. 2013;8(8):e71623.
   Google Scholar
• Feng Y, Desjardins CA, Cooper O, et al. EGR1 functions as a potent repressor of MEF2 transcriptional activity. PLoS One. 2015;10(5):e0131619.
   Google Scholar
• Wang Y, Ma C, Sun Y, et al. Dynamic transcriptome and DNA methylome analyses on longissimus dorsi to identify genes underlying intramuscular fat content in pigs. BMC Genomics. 2017;18(1). DOI:10.1186/s12864-017-4201-9
   Google Scholar
• Busanello A, Battistelli C, Carbone M, et al. MyoD regulates p57kip2 expression by interacting with a distant cis-element and modifying a higher order chromatin structure. Nucleic Acids Res. 2012;40(17):8266–8275.
   Google Scholar
• Guan M, Li W, Xu L, et al. Metformin improves epithelial-to-mesenchymal transition induced by TGF-β1 in renal tubular epithelial NRK-52E cells via inhibiting Egr-1. J Diabetes Res. 2018;2018:1–8.
   Google Scholar
• Aromataris EC, Rychkov GY. ClC-1 chloride channel: matching its properties to a role in skeletal muscle. Clin Exp Pharmacol Physiol. 2006;33(11):1118–1123.
   Google Scholar
• Shang Y, Xu X, Duan X, et al. Hsp70 and Hsp90 oppositely regulate TGF-β signaling through CHIP/Stub1. Biochem Biophys Res Commun. 2014;446(1):387–392.
   Google Scholar
• Taylor AW. Review of the activation of TGF-beta in immunity. J Leukoc Biol. 2009;85(1):29–33.
   Google Scholar
• Kim J, Lee J. Role of transforming growth factor-β in muscle damage and regeneration: focused on eccentric muscle contraction. J Exerc Rehabil. 2017;13(6):621–626.
   Google Scholar
• Mendias CL, Gumucio JP, Davis ME, et al. Transforming growth factor-beta induces skeletal muscle atrophy and fibrosis through the induction of atrogin-1 and scleraxis. Muscle Nerve. 2012;45(1):55–59.
   Google Scholar
• Schabort EJ, van der Merwe M, Loos B, et al. TGF-beta’s delay skeletal muscle progenitor cell differentiation in an isoform-independent manner. Exp Cell Res. 2009;315(3):373–384.
   Google Scholar
• Miyazono K, Olofsson A, Colosetti P, et al. A role of the latent TGF-beta 1-binding protein in the assembly and secretion of TGF-beta 1. Embo J. 1991;10(5):1091–1101.
   Google Scholar
• Delaney K, Kasprzycka P, Ciemerych MA, et al. The role of TGF-β1 during skeletal muscle regeneration. Cell Biol Int. 2017;41(7):706–715.
   Google Scholar
• Cao J, Wei C, Liu D, et al. DNA methylation landscape of body size variation in sheep. Sci Rep. 2015;5:13950.
   Google Scholar
• Yu EM, Ma -L-L, Ji H, et al. Smad4-dependent regulation of type I collagen expression in the muscle of grass carp fed with faba bean. Gene. 2019;685:32–41.
   Google Scholar
• Paris ND, Soroka A, Klose A, et al. Smad4 restricts differentiation to promote expansion of satellite cell derived progenitors during skeletal muscle regeneration. eLife. 2016;5:e19484.
   Google Scholar
• Fu M, Zhang J, Lin Y, et al. Early stimulation and late inhibition of peroxisome proliferator-activated receptor γ (PPARγ) gene expression by transformino growth factor β in human aortic smooth muscle cells: role of early growth-response factor-1 (Egr-1), activator protein 1 (AP1) and Smads. Biochem J. 2003;370(3):1019–1025.
   Google Scholar
• Gu AD, Zhang S, Wang Y, et al. A critical role for transcription factor Smad4 in T cell function that is independent of transforming growth factor β receptor signaling. Immunity. 2015;42(1):68–79.
   Google Scholar
• Huang Y, Zhang H, Shao Z, et al. Suppression of endothelin-1-induced cardiac myocyte hypertrophy by PPAR agonists: role of diacylglycerol kinase zeta. Cardiovasc Res. 2011;90(2):267–275.
   Google Scholar
• Shah TM, Patel NV, Patel AB, et al. A genome-wide approach to screen for genetic variants in broilers (Gallus gallus) with divergent feed conversion ratio. Mol Genet Genomics. 2016;291(4):1715–1725.
   Google Scholar
• Paziewska A, Dabrowska M, Goryca K, et al. DNA methylation status is more reliable than gene expression at detecting cancer in prostate biopsy. Br J Cancer. 2014;111(4):781–789.
   Google Scholar
• Evangelisti C, Tazzari PL, Riccio M, et al. Nuclear diacylglycerol kinase-ζ is a negative regulator of cell cycle progression in C2C12 mouse myoblasts. FASEB J. 2007;21(12):3297–3307.
   Google Scholar
• You JS, Lincoln HC, Kim C-R, et al. The role of diacylglycerol kinase ζ and phosphatidic acid in the mechanical activation of mammalian target of rapamycin (mTOR) signaling and skeletal muscle hypertrophy. J Biol Chem. 2014;289(3):1551–1563.
   Google Scholar
• Miao Y, Yang J, Xu Z, et al. RNA sequencing identifies upregulated kyphoscoliosis peptidase and phosphatidic acid signaling pathways in muscle hypertrophy generated by transgenic expression of myostatin propeptide. Int J Mol Sci. 2015;16(4):7976–7994.
   Google Scholar
• Zhong XP, Hainey EA, Olenchock BA, et al. Enhanced T cell responses due to diacylglycerol kinase ζ deficiency. Nat Immunol. 2003;4(9):882–890.
   Google Scholar
• Rincón E, Gharbi SI, Santos-Mendoza T, et al. Diacylglycerol kinase ζ: at the crossroads of lipid signaling and protein complex organization. Prog Lipid Res. 2012;51(1):1–10.
   Google Scholar
• Marino JS, Tausch BJ, Dearth CL, et al. β2-Integrins contribute to skeletal muscle hypertrophy in mice. Am J Physiol Cell Physiol. 2008;295(4):C1026–1036.
   Google Scholar
• Fagerholm SC, Guenther C, Llort Asens M, et al. Beta2-integrins and interacting proteins in leukocyte trafficking, immune suppression, and immunodeficiency disease. Front Immunol. 2019;10(254). DOI:10.3389/fimmu.2019.00254
   Google Scholar
• Li H, Malhotra S, Kumar A. Nuclear factor-kappa B signaling in skeletal muscle atrophy. J Mol Med. 2008;86(10):1113–1126.
   Google Scholar
• Lawrence T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol. 2009;1(6):a001651.
   Google Scholar
• Matthews SP, McMillan SJ, Colbert JD, et al. Cystatin F ensures eosinophil survival by regulating granule biogenesis. Immunity. 2016;44(4):795–806.
   Google Scholar
• Hamilton G, Colbert JD, Schuettelkopf AW, et al. Cystatin F is a cathepsin C-directed protease inhibitor regulated by proteolysis. EMBO J. 2008;27(3):499–508.
   Google Scholar
• Park S, Lee S, Lee C-G, et al. Capicua deficiency induces autoimmunity and promotes follicular helper T cell differentiation via derepression of ETV5. Nat Commun. 2017;8:16037.
   Google Scholar
• Fu Y, Li J, Tang Q, et al. Integrated analysis of methylome, transcriptome and miRNAome of three pig breeds. Epigenomics. 2018;10(5):597–612.
   Google Scholar
• Ji X, Dadon DB, Abraham BJ, et al. Chromatin proteomic profiling reveals novel proteins associated with histone-marked genomic regions. Proc Natl Acad Sci USA. 2015;112(12):3841.
   Google Scholar
• Kleiner RE, Hang LE, Molloy KR, et al. A chemical proteomics approach to reveal direct protein-protein interactions in living cells. Cell Chem Biol. 2018;25(1):110–120.
   Google Scholar
• Xiong L, Darwanto A, Sharma S, et al. Mass spectrometric studies on epigenetic interaction networks in cell differentiation. J Biol Chem. 2011;286(15):13657–13668.
   Google Scholar
• Zhang Y, Yang X, Gui B, et al. Corepressor protein CDYL functions as a molecular bridge between polycomb repressor complex 2 and repressive chromatin mark trimethylated histone lysine 27. J Biol Chem. 2011;286(49):42414–42425.
   Google Scholar
• Adhikari A, Davie J. JARID2 and the PRC2 complex regulate skeletal muscle differentiation through regulation of canonical Wnt signaling. Epigenetics Chromatin. 2018;11(1):46.
   Google Scholar
• Dougherty JD, Reineke LC, Lloyd RE. mRNA decapping enzyme 1a (Dcp1a)-induced translational arrest through protein kinase R (PKR) activation requires the N-terminal enabled vasodilator-stimulated protein homology 1 (EVH1) domain. J Biol Chem. 2014;289(7):3936–3949.
   Google Scholar
• Hargarten JC, Williamson PR. Epigenetic regulation of autophagy: a path to the control of autoimmunity. Front Immunol. 2018;9:1864.
   Google Scholar
• Song H, Feng X, Zhang H, et al. METTL3 and ALKBH5 oppositely regulate m6 A modification of TFEB mRNA, which dictates the fate of hypoxia/reoxygenation-treated cardiomyocytes. Autophagy. 2019;15:1419–1437.
   Google Scholar
• Mansueto G, Armani A, Viscomi C, et al. Transcription factor EB controls metabolic flexibility during exercise. Cell Metab. 2017;25(1):182–196.
   Google Scholar
• Lu N, Li X, Yu J, et al. Curcumin attenuates lipopolysaccharide-induced hepatic lipid metabolism disorder by modification of m6 A RNA methylation in piglets. Lipids. 2018;53(1):53–63.
   Google Scholar
• Liu Y, Lear T, Iannone O, et al. The pro-apoptotic F-box protein Fbxl7 regulates mitochondrial function by mediating the ubiquitylation and proteasomal degradation of survivin. J Biol Chem. 2015;290:11843–11852.
   Google Scholar
• Bakula D, Müller, AJ, Zuleger, T et al . WIPI3 and WIPI4 β-propellers are scaffolds for LKB1-AMPK-TSC signalling circuits in the control of autophagy. Commun Biol. 2017;8:15637.
   Google Scholar
• Tang Z, Takahashi Y, Chen C, et al. Atg2A/B deficiency switches cytoprotective autophagy to non-canonical caspase-8 activation and apoptosis. Cell Death Differ. 2017;24(12):2127–2138.
   Google Scholar
• Demarchi F, Bertoli C, Copetti T, et al. Calpain as a novel regulator of autophagosome formation. Autophagy. 2007;3(3):235–237.
   Google Scholar
• Ye M, Xu M, Chen C, et al. Expression analyses of candidate genes related to meat quality traits in squabs from two breeds of meat-type pigeon. J Anim Physiol Anim Nutr. 2018;102(3):727–735.
   Google Scholar
• Cleveland BM, Weber GM. Effects of sex steroids on indices of protein turnover in rainbow trout (Oncorhynchus mykiss) white muscle. Gen Comp Endocrinol. 2011;174(2):132–142.
   Google Scholar
• Xia HG, Zhang L, Chen G, et al. Control of basal autophagy by calpain1 mediated cleavage of ATG5. Autophagy. 2010;6(1):61–66.
   Google Scholar
• Macqueen DJ, Meischke L, Manthri S, et al. Characterisation of capn1, capn2-like, capn3 and capn11 genes in Atlantic halibut (Hippoglossus hippoglossus L.): transcriptional regulation across tissues and in skeletal muscle at distinct nutritional states. Gene. 2010;453(1–2):45–58.
   Google Scholar
• Vélez EJ, Azizi S, Verheyden D, et al. Proteolytic systems’ expression during myogenesis and transcriptional regulation by amino acids in gilthead sea bream cultured muscle cells. PLoS One. 2017;12(12):e0187339.
   Google Scholar
• Vélez EJ, Azizi S, Lutfi E, et al. Moderate and sustained exercise modulates muscle proteolytic and myogenic markers in gilthead sea bream (Sparus aurata). Am J Physiol Regul Integr Comp Physiol. 2017;312(5):R643–R653.
   Google Scholar
• Meugnier E, Bossu C, Oliel M, et al. Changes in gene expression in skeletal muscle in response to fat overfeeding in lean men. Obesity. 2007;15(11):2583–2594.
   Google Scholar
• Tong T, Shen Y, Lee H-W, et al. Adenylyl cyclase 3 haploinsufficiency confers susceptibility to diet-induced obesity and insulin resistance in mice. Sci Rep. 2016;6:34179.
   Google Scholar
• Xu H, Du X, Liu G, et al. The pseudokinase MLKL regulates hepatic insulin sensitivity independently of inflammation. Mol Metab. 2019;23:14–23.
   Google Scholar
• Schneeberger M. Irx3, a new leader on obesity genetics. EBioMedicine. 2018;39:19–20.
   Google Scholar
• Corominas J, Ramayo-Caldas Y, Puig-Oliveras A, et al. Polymorphism in the ELOVL6 gene is associated with a major QTL effect on fatty acid composition in pigs. PLoS One. 2013;8(1):e53687–e53687.
   Google Scholar
• Matsuzaka T, Shimano H, Yahagi N, et al. Crucial role of a long-chain fatty acid elongase, Elovl6, in obesity-induced insulin resistance. Nat Med. 2007;13(10):1193–1202.
   Google Scholar
• Fujita M, Momose A, Ohtomo T, et al. Upregulation of fatty acyl-CoA thioesterases in the heart and skeletal muscle of rats fed a high-fat diet. Biol Pharm Bull. 2011;34(1):87–91.
   Google Scholar
• Le Luyer J, Laporte M, Beacham TD, et al. Parallel epigenetic modifications induced by hatchery rearing in a Pacific salmon. Proc Natl Acad Sci USA. 2017;114(49):12964–12969.
   Google Scholar
• Anastasiadi D, Piferrer F. Epimutations in developmental genes underlie the onset of domestication in farmed european sea bass. Mol Biol Evol. 2019;36(10):2252–2264.
   Google Scholar
• Podgorniak T, Brockmann S, Konstantinidis I, et al. Differences in the fast muscle methylome provide insight into sex-specific epigenetic regulation of growth in Nile tilapia during early stages of domestication. Epigenetics. 2019;14:818–836.
   Google Scholar
• Wan ZY, Xia JH, Lin G, et al. Genome-wide methylation analysis identified sexually dimorphic methylated regions in hybrid tilapia. Sci Rep. 2016;6:35903.
   Google Scholar
• Chen X, Wang Z, Tang S, et al. Genome-wide mapping of DNA methylation in Nile tilapia. Hydrobiologia. 2016;791(1):1–11.
   Google Scholar
• Blouin MS, Thuillier V, Cooper B, et al. No evidence for large differences in genomic methylation between wild and hatchery steelhead (Oncorhynchus mykiss). Can J Fish Aquat Sci. 2010;67(2):217–224.
   Google Scholar
• Visse M, Sild E, Kesler M, et al. Do Atlantic salmon parr trade growth against immunity? Mar Freshwater Behav Physiol. 2015;48(4):225–240.
   Google Scholar
• van der Most PJ, de Jong B, Parmentier HK, et al. Trade-off between growth and immune function: a meta-analysis of selection experiments. Funct Ecol. 2011;25(1):74–80.
   Google Scholar
• Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17(1):10–12.
   Google Scholar
• Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011;27(11):1571–1572.
   Google Scholar
• Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–359.
   Google Scholar
• Akalin A, Kormaksson M, Li S, et al. methylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biol. 2012;13(10):R87–R87.
   Google Scholar
• Krzywinski M, Schein J, Birol İ, et al. Circos: an information aesthetic for comparative genomics. Genome Res. 2009;19(9):1639–1645.
   Google Scholar
• Heinz S, Benner C, Spann N, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38(4):576–589.
   Google Scholar
• Rebhan M, Chalifa-Caspi V, Prilusky J, et al. GeneCards: integrating information about genes, proteins and diseases. Trends Genet. 1997;13(4):163.
   Google Scholar
• Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44–57.
   Google Scholar