3,675
Views
26
CrossRef citations to date
0
Altmetric
Research Paper

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

ORCID Icon, , , ORCID Icon, ORCID Icon & ORCID Icon
Pages 1052-1067 | Received 28 Oct 2019, Accepted 25 Mar 2020, Published online: 07 Apr 2020

References

  • Diamond J. Evolution, consequences and future of plant and animal domestication. Nature. 2002;418:700–707.
  • Larson G, Fuller DQ. The evolution of animal domestication. Annu Rev Ecol Evol Syst. 2014;45:115–136.
  • Makinen H, Vasemagi A, McGinnity P, et al. Population genomic analyses of early-phase Atlantic Salmon (Salmo salar) domestication/captive breeding. Evol Appl. 2015;8:93–107.
  • Lopez ME, Neira R, Yanez JM. Applications in the search for genomic selection signatures in fish. Front Genet. 2014;5:458.
  • Roberge C, Einum S, Guderley H, et al. Rapid parallel evolutionary changes of gene transcription profiles in farmed Atlantic salmon. Mol Ecol. 2006;15:9–20.
  • Sauvage C, Derome N, Normandeau E, et al. Fast transcriptional responses to domestication in the brook charr Salvelinus fontinalis. Genetics. 2010;185:105–112.
  • Gjerdem T, Robinson N. Advances by selective breeding for aquatic species: A review. Agri Sci. 2014;5:1152–1158.
  • Thodesen J, Grisdale-Helland B, Helland SJ, et al. Feed intake, growth and feed utilization of offspring from wild and selected Atlantic salmon (Salmo salar). Aquaculture. 1999;180:237–246.
  • Bentsen HB, Gjerde B, Eknath AE, et al. Genetic improvement of farmed tilapias: response to five generations of selection for increased body weight at harvest in Oreochromis niloticus and the further impact of the project. Aquaculture. 2017;468:206–217.
  • Tahiliani M, Koh KP, Shen Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 2009;324:930–935.
  • Greco CM, Kunderfranco P, Rubino M, et al. DNA hydroxymethylation controls cardiomyocyte gene expression in development and hypertrophy. Nat Commun. 2016;7:12418.
  • Sun F, Abreu-Rodriguez I, Ye S, et al. TET1 is an important transcriptional activator of TNFalpha expression in macrophages. PLoS One. 2019;14:e0218551.
  • Pan Z, Zhang M, Ma T, et al. Hydroxymethylation of microRNA-365-3p regulates nociceptive behaviors via Kcnh2. J Neurosci. 2016;36:2769–2781.
  • Wu H, D’Alessio AC, Ito S, et al. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev. 2011;25:679–684.
  • Song CX, Szulwach KE, Fu Y, et al. Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat Biotechnol. 2011;29:68–72.
  • Runemark A, Brydegaard M, Svensson EI. Does relaxed predation drive phenotypic divergence among insular populations? J Evol Biol. 2014;27:1676–1690. DOI:10.1111/jeb.12421
  • Vasemägi A, Nilsson J, McGinnity P, et al. Screen for footprints of selection during domesticatin/captive breeding of Atlantic salmon. Comp Funct Genom. 2012;2012:628204.
  • Christie MR, Marine ML, French RA, et al. Genetic adaptation to captivity can occur in a single generation. Proc Natl Acad Sci U S A. 2012;109:238–242.
  • Araki H, Cooper B, Blouin MS. Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science. 2007;318:100–103.
  • 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.
  • Devlin RH, Sakhrani D, White S, et al. Effects of domestication and growth hormone transgenesis on mRNA profiles in rainbow trout (Oncorhynchus mykiss). J Anim Sci. 2013;91:5247–5258.
  • Devlin RH, Sakhrani D, Tymchuk WE, et al. Domestication and growth hormone transgenesis cause similar changes in gene expression in coho salmon (Oncorhynchus kisutch). Proc Natl Acad Sci U S A. 2009;106:3047–3052.
  • Haase D, Rieger JK, Witten A, et al. Specific gene expression responses to parasite genotypes reveal redundancy of innate immunity in vertebrates. PLoS One. 2014;9:e108001.
  • Lio CJ, Rao A. TET Enzymes and 5hmC in adaptive and innate immune systems. Front Immunol. 2019;10:210.
  • Tsumagari K, Baribault C, Terragni J, et al. Early de novo DNA methylation and prolonged demethylation in the muscle lineage. Epigenetics. 2013;8:317–332.
  • Uren Webster TM, Rodriguez-Barreto D, Martin SAM, et al. Contrasting effects of acute and chronic stress on the transcriptome, epigenome, and immune response of Atlantic salmon. Epigenetics. 2018;13:1191–1207.
  • Sveen LR, Timmerhaus G, Krasnov A, et al. High fish density delays wound healing in Atlantic salmon (Salmo salar). Sci Rep. 2018;8:16907.
  • Tymchuk WE, Beckman B, Devlin RH. Altered expression of growth hormone/insulin-like growth factor I axis hormones in domesticated fish. Endocrinology. 2009;150:1809–1816.
  • Hassin S, Monbrison D, Hanin Y, et al. Domestication of the white grouper, Epinephelus aeneus 1. Growth and reproduction. Aquaculture. 1997;156:305–316.
  • Johnsson JI, Petersson E, Jönsson E, et al. Domestication and growth hormone alter antipredator behaviour and growth patterns in juvenile brown trout, Salmo trutta. Can J Fish Aquat Sci. 1996;53:1546–1554.
  • Fleming IA, Agustsson T, Finstad B, et al. Effects of domestication on growth physiology and endocrinology of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci. 2002;59:1323–1330.
  • Robison D, Rowland W. A potential model system for studying the genetics of domestication: behavioral variation among wild and domesticated strains of zebra danio (Danio rerio). Can J Fish Aquat Sci. 2005;62:2046–2054.
  • Ponzoni RW, Nguyen NH, Khaw HL, et al. Genetic improvement of Nile tilapia (Oreochromis niloticus) with special reference to the work conducted by the WorldFish Center with the GIFT strain. Rev Aquacult. 2011;3:27–41.
  • Tidball JG. Regulation of muscle growth and regeneration by the immune system. Nat Rev Immunol. 2017;17:165–178.
  • Nascimento AF, Trindade DM, Tonoli CC, et al. Structural insights into functional overlapping and differentiation among myosin V motors. J Biol Chem. 2013;288:34131–34145.
  • Sun Y, Bilan PJ, Liu Z, et al. Rab8A and Rab13 are activated by insulin and regulate GLUT4 translocation in muscle cells. Proc Natl Acad Sci U S A. 2010;107:19909–19914.
  • Ishikura S, Klip A. Muscle cells engage Rab8A and myosin Vb in insulin-dependent GLUT4 translocation. Am J Physiol Cell Physiol. 2008;295:C1016–25.
  • Hammer JA 3rd, Wagner W. Functions of class V myosins in neurons. J Biol Chem. 2013;288:28428–28434.
  • Altarejos JY, Montminy M. CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol. 2011;12:141–151.
  • Xu Y, Yu W, Xiong Y, et al. Molecular characterization and expression patterns of serine/arginine-rich specific kinase 3 (SPRK3) in porcine skeletal muscle. Mol Biol Rep. 2011;38:2903–2909.
  • Adam AC, Lie KK, Whatmore P, et al. Profiling DNA methylation patterns of zebrafish liver associated with parental high dietary arachidonic acid. PLoS One. 2019;14:e0220934.
  • Skjaerven KH, Jakt LM, Fernandes JMO, et al. Parental micronutrient deficiency distorts liver DNA methylation and expression of lipid genes associated with a fatty-liver-like phenotype in offspring. Sci Rep. 2018;8:3055.
  • Shock LS, Thakkar PV, Peterson EJ, et al. DNA methyltransferase 1, cytosine methylation, and cytosine hydroxymethylation in mammalian mitochondria. Proc Natl Acad Sci U S A. 2011;108:3630–3635.
  • Bellizzi D, D’Aquila P, Scafone T, et al. The control region of mitochondrial DNA shows an unusual CpG and non-CpG methylation pattern. DNA Res. 2013;20:537–547.
  • Potok ME, Nix DA, Parnell TJ, et al. Reprogramming the maternal zebrafish genome after fertilization to match the paternal methylation pattern. Cell. 2013;153:759–772.
  • Le Luyer J, Laporte M, Beacham TD, et al. Parallel epigenetic modifications induced by hatchery rearing in a Pacific salmon. Proc Natl Acad Sci U S A. 2017;114:12964–12969.
  • Anastasiadi D, Esteve-Codina A, Piferrer F. Consistent inverse correlation between DNA methylation of the first intron and gene expression across tissues and species. Epigenetics Chromatin. 2018;11:37.
  • Jiang L, Zhang J, Wang JJ, et al. Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos. Cell. 2013;153:773–784.
  • Simões LN, Lombardi DC, Gomide ATM, et al. Efficacy of clove oil as anesthetic in handling and transportation of Nile tilapia, Oreochromis niloticus (Actinopterygii: cichlidae) juveniles. Zoologia. 2011;28:285–290.
  • Illumina. Effects of index misassignment on multiplexing and downstream analysis. 2017.
  • Sun X, Chung TH, Tan D, et al. Practical guidelines and consideration of using RRHP for 5hmC detectionPractical guidelines and consideration of using RRHP for 5hmC detection. Epigenomics. 2016;8:225–235.
  • Petterson A, Chung TH, Tan D, et al. RRHP: a tag-based approach for 5-hydroxymethylcytosine mapping at single-site resolution. Genome Biol. 2014;15:456.
  • Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal. 2011;17:10–12.
  • Conte MA, Gammerdinger WJ, Bartie KL, et al. A high quality assembly of the Nile Tilapia (Oreochromis niloticus) genome reveals the structure of two sex determination regions. BMC Genomics. 2017;18:341.
  • Langmead B. Aligning short sequencing reads with Bowtie. Curr Protoc Bioinformatics. 2010;32:11.7.1–11.7.14.
  • Team RC. R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria; 2017.
  • 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;38:576–589.
  • Zhou Y, Zhou B, Pache L, et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun. 2019;10:1523.
  • Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120.
  • Dobin A, Davis CA, Schlesinger F, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21.
  • Anders S, Pyl PT, Huber W. HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31:166–169.
  • Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Series B. 1995;57:289–300.
  • Su A Dataset: GeneAtlas U133A, gcrma. 2019.
  • Jain A, Tuteja G. TissueEnrich: tissue-specific gene enrichment analysis. Bioinformatics. 2019;1966–1967. DOI:10.1093/bioinformatics/bty890
  • Davis S, Pettengill JB, Luo Y, et al. CFSAN SNP Pipeline: an automated method for constructing SNP matrices from next-generation sequence data. PeerJ Comput Sci. 2015;1:e20.