Genome Wide Analysis for Growth at Two Growth Stages in A New Fast-Growing Common Carp Strain (Cyprinus carpio L.).


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
29 04 2020
Historique:
received: 12 06 2019
accepted: 08 04 2020
entrez: 1 5 2020
pubmed: 1 5 2020
medline: 7 1 2021
Statut: epublish

Résumé

In order to identify candidate genes or loci associated with growth performance of the newly established common carp strain, Xinlong, we conducted a genome-wide association analysis using 2b-RAD technology on 123 individuals. We constructed two sets of libraries associated with growth-related parameters (weight, length, width and depth) measured at two different grow-out stages. Among the 413,059 SNPs identified using SOAP SNP calling, 147,131 were tested for GWAS after quality filtering. Finally, 39 overlapping SNPs, assigned to four genomic locations, were associated with growth traits in two stages. These loci were assigned to functional classes related to immune response, response to stress, neurogenesis, cholesterol metabolism and development, and proliferation and differentiation of cells. By overlapping results of Plink and EMMAX analyses, we identified three genes: TOX, PLK2 and CD163 (both methods P < 0.05). Our study results could be used for marker-assisted selection to further improve the growth of the Xinlong strain, and illustrate that largely different sets of genes drive the growth of carp in the early and late grow-out stages.

Identifiants

pubmed: 32350307
doi: 10.1038/s41598-020-64037-w
pii: 10.1038/s41598-020-64037-w
pmc: PMC7190712
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

7259

Références

Tsai, H. Y. et al. Genome wide association and genomic prediction for growth traits in juvenile farmed Atlantic salmon using a high density SNP array. BMC Genomics. 16, (2015).
Gutierrez, A. P., Yáñez, J. M., Fukui, S., Swift, B. & Davidson, W. S. Genome-wide association study (GWAS) for growth rate and age at sexual maturation in Atlantic salmon (Salmo salar). PLoS One. 10, e0119730–e0119730 (2015).
pubmed: 25757012 pmcid: 4355585 doi: 10.1371/journal.pone.0119730
Gonzalez-Pena, D. et al. Genome-wide association study for identifying loci that affect fillet yield, carcass, and body weight traits in Rainbow Trout (Oncorhynchus mykiss). Front. Genet. 7, 203 (2016).
pubmed: 27920797 pmcid: 5118429 doi: 10.3389/fgene.2016.00203
Geng, X. et al. A Genome-wide association study identifies multiple regions associated with head size in Catfish. G3 (Bethesda). 6, 3389–3398 (2016).
pubmed: 27558670 pmcid: 5068958 doi: 10.1534/g3.116.032201
Chen, L. et al. Genetic mapping of head size related traits in common carp (Cyprinus carpio). Front. Genet. 9, 448 (2018).
pubmed: 30356829 pmcid: 6190898 doi: 10.3389/fgene.2018.00448
Korte, A. & Farlow, A. The advantages and limitations of trait analysis with GWAS: a review. Plant Methods. 9, 29 (2013).
pubmed: 23876160 pmcid: 3750305 doi: 10.1186/1746-4811-9-29
Xu, J. et al. Development and evaluation of the first high-throughput SNP array for common carp (Cyprinus carpio). BMC Genomics. 15, 307 (2014).
pubmed: 24762296 pmcid: 4234440 doi: 10.1186/1471-2164-15-307
Wang, S., Meyer, E., McKay, J. K. & Matz, M. V. 2b-RAD: a simple and flexible method for genome-wide genotyping. Nat. Methods. 9, 808–810 (2012).
pubmed: 22609625 doi: 10.1038/nmeth.2023
Pecoraro, C. et al. Methodological assessment of 2b-RAD genotyping technique for population structure inferences in yellowfin tuna (Thunnus albacares). Mar. Genomics. 25, 43–48 (2016).
pubmed: 26711352 doi: 10.1016/j.margen.2015.12.002
Seetharam, A. S. & Stuart, G. W. Whole genome phylogeny for 21 Drosophila species using predicted 2b-RAD fragments. PeerJ. 1, e226 (2013).
pubmed: 24432193 pmcid: 3883493 doi: 10.7717/peerj.226
Fu, B., Liu, H., Yu, X. & Tong, J. A high-density genetic map and growth related QTL mapping in bighead carp (Hypophthalmichthys nobilis). Sci. Rep. 6, 28679 (2016).
pubmed: 27345016 pmcid: 4921863 doi: 10.1038/srep28679
Palaiokostas, C. et al. Mapping and validation of the major sex-determining region in Nile tilapia (Oreochromis niloticus L.) Using RAD sequencing. PLoS One. 8, e68389 (2013).
pubmed: 23874606 pmcid: 3708939 doi: 10.1371/journal.pone.0068389
Casal, C. M. V. Global documentation of fish introductions: the growing crisis and recommendations for action. Biol. Invasions. 8, 3–11 (2006).
doi: 10.1007/s10530-005-0231-3
FAO. FAO Yearbook: Fisheries and Aquaculture Statistics. (Food and Agriculture Organization of the United Nations, 2015).
AFFAB. China Fishery Statistics Yearbook. Fisheries and Fishery Administration Bureau of the Ministry of Agriculture. (China Agriculture Press Chinese Agricultural Press, 2017).
Su, S. Y., Zhang, C. F., Dong, Z. J., Xu, P. & Yuan, X. H. The breeding gain of Huanghe carp (Cyprinus carpio hacmalopterus Temminck et Schlegel) new strain G3- The effect of higher carbohydrate diet on growth and fatty acid profile of huanghe carp new strain. J. Yangzhou Univ. 39, 63–66 (2018).
Chengfeng, Z., Shengyan, S., Jian, Z., Wenbin, Z. & Zaijie, D. Growth analysis of Huanghe carp during two grow-out stages. Acta Hydrobiol. Sin. 722–727 (2013).
Su, S. et al. Combined QTL and genome scan analyses with the help of 2b-RAD identify growth-associated genetic markers in a new fast-growing carp strain. Frontiers in Genetics. 9, 592 (2018).
pubmed: 30581452 pmcid: 6293859 doi: 10.3389/fgene.2018.00592
Xu, P. et al. Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nat. Genet. 46, 1212–1219 (2014).
pubmed: 25240282 doi: 10.1038/ng.3098
Ng, C. T., Mendoza, J. L., Garcia, K. C. & Oldstone, M. B. Alpha and beta type 1 interferon signaling: passage for diverse biologic outcomes. Cell. 164(3), 349–352 (2016).
pubmed: 26824652 pmcid: 4733246 doi: 10.1016/j.cell.2015.12.027
Liu, T., Jiang, W., Han, D. & Yu, L. DNAJC25 is downregulated in hepatocellular carcinoma and is a novel tumor suppressor gene. Oncol. Lett. 4(6), 1274–1280 (2012).
pubmed: 23205125 pmcid: 3506724 doi: 10.3892/ol.2012.903
Guha, P. et al. IPMK mediates activation of ULK signaling and transcriptional regulation of autophagy linked to liver inflammation and regeneration. Cell. Rep. 26(10), 2692–2703.e7 (2019).
pubmed: 30840891 pmcid: 6494083 doi: 10.1016/j.celrep.2019.02.013
Skon-Hegg, C. et al. LACC1 regulates TNF and IL-17 in mouse models of arthritis and inflammation. J. Immunol. 202(1), 183–193 (2019).
pubmed: 30510070 doi: 10.4049/jimmunol.1800636
Contu, L., Carare, R.O. & Hawkes, C. A. Knockout of apolipoprotein A-I decreases parenchymal and vascular β-amyloid pathology in the Tg2576 mouse model of Alzheimer’s disease. Neuropathol. Appl. Neurobiol. (2019).
Lobbardi, R. et al. TOX regulates growth, DNA repair, and genomic instability in T-cell acute lymphoblastic leukemia. Cancer. Discov. 7, 1336–1353 (2017).
pubmed: 28974511 pmcid: 5683427 doi: 10.1158/2159-8290.CD-17-0267
Yang, H. et al. CD163 knockout pigs are fully resistant to highly pathogenic porcine reproductive and respiratory syndrome virus. Antiviral Res. 151, 63–70 (2018).
pubmed: 29337166 doi: 10.1016/j.antiviral.2018.01.004
Kumanogoh, A. et al. Nonredundant roles of Sema4Ain the immune system: defective T cell priming and Th1/Th2 regulation in Sema4A-deficient mice. Immunity. 22(3), 305–316 (2005).
pubmed: 15780988 doi: 10.1016/j.immuni.2005.01.014
Spiegel, S., Maczis, M. A., Maceyka, M. & Milstien, S. New insights into functions of the sphingosine-1-phosphate transporter SPNS2. J. Lipid. Res. 60(3), 484–489 (2019).
pubmed: 30655317 pmcid: 6399492 doi: 10.1194/jlr.S091959
De la Serna, I. L., Carlson, K. A. & Imbalzano, A. N. Mammalian SWI/SNF complexes promote MyoD-mediated muscle differentiation. Nat.Genet. 27, 187–190 (2001).
pubmed: 11175787 doi: 10.1038/84826
Tanneberger, K. et al. Structural and functional characterization of the Wnt inhibitor APC membrane recruitment 1(Amer1). J Biol Chem. 286(22), 19204–19214 (2011).
pubmed: 21498506 pmcid: 3103299 doi: 10.1074/jbc.M111.224881
Sakamoto, K., Wehde, B. L., Rädler, P. D., Triplett, A. A. & Wagner, K. U. Generation of Janus kinase 1 (JAK1) conditional knockout mice. Genesis. 54(11), 582–588 (2016).
pubmed: 27671227 pmcid: 6988131 doi: 10.1002/dvg.22982
Wang, R. J. et al. The impact of NudCD1 on renal carcinoma cell proliferation, migration, and invasion. Eur. Rev. Med. Pharmacol. Sci. 22(3), 671–677 (2018).
pubmed: 29461594
Vasileva, A. et al. The DNA damage checkpoint protein RAD9A is essential for male meiosis in the mouse. J. Cell. Sci. 126(Pt 17), 3927–3938 (2013).
pubmed: 23788429 pmcid: 3757332 doi: 10.1242/jcs.126763
Wang, F. et al. Hormone-sensitive lipase deficiency alters gene expression and cholesterol content of mouse testis. Reproduction. 153(2), 175–185 (2017).
pubmed: 27920259 doi: 10.1530/REP-16-0484 pmcid: 27920259
Hu, A. et al. PIP4K2A regulates intracellular cholesterol transport through modulating PI(4,5)P2 homeostasis. J. Lipid. Res. 59(3), 507–514 (2018).
pubmed: 29353240 pmcid: 5832930 doi: 10.1194/jlr.M082149
Kuehnle, K. et al. Age-dependent increase in desmosterol restores DRM formation and membrane-related functions in cholesterol-free DHCR24-/- mice. Neurochem. Res. 34(6), 1167–1182 (2009).
pubmed: 19115107 doi: 10.1007/s11064-008-9893-4 pmcid: 19115107
Saharan, M. et al. Enhanced long-term potentiation in vivo in dentate gyrus of NELL2-deficient mice. Neuroreport 15(3), 417–420 (2004).
doi: 10.1097/00001756-200403010-00007
Dean, B. J., Erdogan, B., Gamse, J. T. & Wu, S. Y. Dbx1b defines the dorsal habenular progenitor domain in the zebrafish epithalamus. Neural. Dev. 9, 20 (2014).
pubmed: 25212830 pmcid: 4164515 doi: 10.1186/1749-8104-9-20
Díaz, E. SynDIG1 regulation of excitatory synapse maturation. J. Physiol. 590(1), 33–38 (2012).
pubmed: 21878521 doi: 10.1113/jphysiol.2011.213884 pmcid: 21878521
Sistig, T. et al. Mtss1 promotes maturation and maintenance of cerebellar neurons via splice variant-specific effects. Brain. Struct. Funct. 222(6), 2787–2805 (2017).
pubmed: 28214917 doi: 10.1007/s00429-017-1372-8
Berger, C., Helmprobst, F., Chapouton, P., Lillesaar, C. & Stigloher, C. Sept8a and sept8b mRNA expression in the developing and adult zebrafish. Gene Expr Patterns. 25-26, 8–21 (2017).
pubmed: 28414113 doi: 10.1016/j.gep.2017.04.002
Born, G. et al. Genetic targeting of NRXN2 in mice unveils role in excitatory cortical synapse function and social behaviors. Front. Synaptic. Neurosci. 7, 3 (2015).
pubmed: 25745399 pmcid: 4333794 doi: 10.3389/fnsyn.2015.00003
Maeta, K. et al. Comprehensive behavioral analysis of mice deficient in Rapgef2 and Rapgef6, a subfamily of guanine nucleotide exchange factors for Rap small GTPases possessing the Ras/Rap-associating domain. Mol. Brain. 11(1), 27 (2018).
pubmed: 29747665 pmcid: 5946393 doi: 10.1186/s13041-018-0370-y
Ghosh, A. S. et al. DLK induces developmental neuronal degeneration via selective regulation of proapoptotic JNK activity. J. Cell. Biol. 194(5), 751–64 (2011).
pubmed: 21893599 pmcid: 3171129 doi: 10.1083/jcb.201103153
Cambiaghi, T. D. et al. Evolutionarily conserved IMPACT impairs various stress responses that require GCN1 for activating the eIF2 kinase GCN2. Biochem Biophys Res Commun. 443(2), 592–597 (2014).
pubmed: 24333428 doi: 10.1016/j.bbrc.2013.12.021
Maul, S. et al. Genetics of resilience: Implications from genome-wide association studies and candidate genes of the stress response system in posttraumatic stress disorder and depression. Am. J. Med. Genet. B. Neuropsychiatr. Genet. (2019).
Cizmecioglu, O., Warnke, S., Arnold, M., Duensing, S. & Hoffmann, I. Plk2 regulated centriole duplication is dependent on its localization to the centrioles and a functional polo-box domain. Cell. Cycle. 7, 3548–3555 (2008).
pubmed: 19001868 doi: 10.4161/cc.7.22.7071
Visscher, P. M., Brown, M. A., McCarthy, M. I. & Yang, J. Five years of GWAS discovery. Am. J. Hum. Genet. 90, 7–24 (2012).
pubmed: 22243964 pmcid: 22243964 doi: 10.1016/j.ajhg.2011.11.029
Goddard, M. E. & Hayes, B. J. Mapping genes for complex traits in domestic animals and their use in breeding programmes. Nat. Rev. Genet. 10, 381–391 (2009).
pubmed: 19448663 doi: 10.1038/nrg2575
Matukumalli, L. K. et al. Development and characterization of a high density SNP genotyping assay for cattle. PLoS One. 4, e5350 (2009).
pubmed: 19390634 pmcid: 2669730 doi: 10.1371/journal.pone.0005350
Gidskehaug, L., Kent, M., Hayes, B. J. & Lien, S. Genotype calling and mapping of multisite variants using an Atlantic salmon iSelect SNP array. Bioinformatics. 27, 303–310 (2011).
pubmed: 21149341 doi: 10.1093/bioinformatics/btq673
Peng, W. et al. An ultra-high density linkage map and QTL mapping for sex and growth-related traits of common carp (Cyprinus carpio). Sci Rep. 6, (2016).
Mauch, D. H. et al. CNS synaptogenesis promoted by glia-derived cholesterol. Science. 294, 1354–1357 (2001).
pubmed: 11701931 doi: 10.1126/science.294.5545.1354
Gomes, I. et al. GPR171 is a hypothalamic G protein-coupled receptor for BigLEN, a neuropeptide involved in feeding. Proc. Natl. Acad. Sci. USA 110, 16211–16216 (2013).
pubmed: 24043826 doi: 10.1073/pnas.1312938110
Bakos, J., Zatkova, M., Bacova, Z. & Ostatnikova, D. The role of hypothalamic neuropeptides in neurogeneis and neuritogenesis. Neual. plasticity. 2016, 3276383 (2016).
Brunner, L. et al. Leptin is a physiologically important regulator of food intake. Int. J. Obes. Relat. Metab. Disord. 21, 1152 (1997).
pubmed: 9426383 doi: 10.1038/sj.ijo.0800529
Muraoka, O. et al. Leptin-induced transactivation of NPY gene promoter mediated by JAK1, JAK2 and STAT3 in the neural cell lines. Neurochem. Int. 42(7), 591–601 (2003).
pubmed: 12590942 doi: 10.1016/S0197-0186(02)00160-2
Chaffey, N. et al. Molecular Biology of the Cell. 4th edn. Ann. Bot. 91, 401 (2003).
pmcid: 4244961 doi: 10.1093/aob/mcg023 pubmed: 4244961
Archambault, V. & Glover, D. M. Polo-like kinases: conservation and divergence in their functions and regulation. Nat. Rev. Mol. Cell Biol. 10, 265–275 (2009).
pubmed: 19305416 doi: 10.1038/nrm2653
Ma, S., Charron, J. & Erikson, R. L. Role of Plk2 (Snk) in mouse development and cell proliferation. Mol. Cell. Biol. 23, 6936–6943 (2003).
pubmed: 12972611 pmcid: 193943 doi: 10.1128/MCB.23.19.6936-6943.2003
Park, W. B. et al. The rs196952262 Polymorphism of the AGPAT5 gene is associated with meat quality in berkshire pigs. Korean. J. Food. Sci. An. 37, 926 (2017).
Wei, X., Zhang, J., Sun, X., Zhao, F. & Zhang, J. Correlation analysis between the polymorphism of AGPAT5 gene and meat quality traits in German Simmental cattle. Hei. Anim. Sci. Vet. Med. 9, 12 (2013).
Clair, S. L. S., Belisle, S. L., Jaimes, F. B. L., Li, Z. & Parks, B. 1892-P: Hepatic Agpat5 Regulates Plasma Insulin in Obesity. Diabetes. 68, 1892-p (2019).
doi: 10.2337/db19-1892-P
Agarwal, A. K. et al. AGPAT2 is mutated in congenital generalized lipodystrophy linked to chromosome 9q34. Nat. Genet. 31, 21–23 (2002).
pubmed: 11967537 doi: 10.1038/ng880
Wang, C. H. & Li, S. F. Genetic effects and genotype x environment interactions for growth-related traits in common carp, Cyprinus carpio L. Aquaculture. 272, 267–272 (2007).
doi: 10.1016/j.aquaculture.2007.07.011
Ponzoni, R. W., Hamzah, A., Tan, S. & Kamaruzzaman, N. Genetic parameters and response to selection for live weight in the GIFT strain of Nile tilapia (Oreochromis niloticus). Aquaculture. 247, 203–210 (2005).
doi: 10.1016/j.aquaculture.2005.02.020
Velisek, J., Svobodova, Z., Piackova, V., Groch, L. & Nepejchalova, L. Effects of clove oil anaesthesia on common carp (Cyprinus carpio L.). Vet Med. 50, 269–275 (2005).
doi: 10.17221/5623-VETMED
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A. & Cresko, W. A. Stacks: an analysis tool set for population genomics. Mol. Ecol. 22, 3124–3140 (2013).
pubmed: 23701397 pmcid: 3936987 doi: 10.1111/mec.12354
Jiao, W. et al. High-resolution linkage and quantitative trait locus mapping aided by genome survey sequencing: building up an integrative genomic framework for a bivalve mollusc. DNA Res. 21, 85–101 (2014).
pubmed: 24107803 doi: 10.1093/dnares/dst043
Zhang, J., Kobert, K., Flouri, T. & Stamatakis, A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics. 30, 614–620 (2014).
pubmed: 24142950 doi: 10.1093/bioinformatics/btt593
Li, R. et al. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics. 25, 1966–1967 (2009).
pubmed: 19497933 doi: 10.1093/bioinformatics/btp336 pmcid: 19497933
Fu, X. et al. RADtyping: An Integrated Package for Accurate De Novo Codominant and Dominant RAD Genotyping in Mapping Populations. PloS. One. 8, e79960 (2013).
pubmed: 24278224 pmcid: 3836964 doi: 10.1371/journal.pone.0079960
Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).
pubmed: 17701901 pmcid: 17701901 doi: 10.1086/519795
Kang, H. M. et al. Variance component model to account for sample structure in genome-wide association studies. Nat. Genet. 42, 348–354 (2010).
pubmed: 20208533 pmcid: 3092069 doi: 10.1038/ng.548
Turner, S.D. Qqman: an R package for visualizing GWAS results using Q-Q and manhattan plots. BioRxiv.005165
Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly. 6, 80–92 (2012).
pubmed: 22728672 pmcid: 3679285 doi: 10.4161/fly.19695
Shin, J. H. et al. The International HapMap Consortium. A haplotype map of the human genome. Nature. 437, 1299–1320 (2005).
doi: 10.1038/nature04226

Auteurs

Shengyan Su (S)

Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture; Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, 214081, PR China. susy@ffrc.cn.
Wuxi Fisheries College, Nanjing Agricultural University, Wuxi, 214081, PR China. susy@ffrc.cn.

Bouzoualegh Raouf (B)

Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture; Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, 214081, PR China.
Wuxi Fisheries College, Nanjing Agricultural University, Wuxi, 214081, PR China.

Xinjin He (X)

Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture; Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, 214081, PR China.
College of Animal science, Shanxi Agricultural University, Taigu, PR China.

Nana Cai (N)

Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture; Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, 214081, PR China.

Xinyuan Li (X)

Wuxi Fisheries College, Nanjing Agricultural University, Wuxi, 214081, PR China.

Juhua Yu (J)

Wuxi Fisheries College, Nanjing Agricultural University, Wuxi, 214081, PR China.

JianLin Li (J)

Wuxi Fisheries College, Nanjing Agricultural University, Wuxi, 214081, PR China.

Fan Yu (F)

Wuxi Fisheries College, Nanjing Agricultural University, Wuxi, 214081, PR China.

Meiyao Wang (M)

Wuxi Fisheries College, Nanjing Agricultural University, Wuxi, 214081, PR China.

Yongkai Tang (Y)

Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture; Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, 214081, PR China. tangyk@ffrc.cn.
Wuxi Fisheries College, Nanjing Agricultural University, Wuxi, 214081, PR China. tangyk@ffrc.cn.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH