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Copy Number Variations in Tilapia Genomes

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Abstract

Discovering the nature and pattern of genome variation is fundamental in understanding phenotypic diversity among populations. Although several millions of single nucleotide polymorphisms (SNPs) have been discovered in tilapia, the genome-wide characterization of larger structural variants, such as copy number variation (CNV) regions has not been carried out yet. We conducted a genome-wide scan for CNVs in 47 individuals from three tilapia populations. Based on 254 Gb of high-quality paired-end sequencing reads, we identified 4642 distinct high-confidence CNVs. These CNVs account for 1.9% (12.411 Mb) of the used Nile tilapia reference genome. A total of 1100 predicted CNVs were found overlapping with exon regions of protein genes. Further association analysis based on linear model regression found 85 CNVs ranging between 300 and 27,000 base pairs significantly associated to population types (R 2 > 0.9 and P > 0.001). Our study sheds first insights on genome-wide CNVs in tilapia. These CNVs among and within tilapia populations may have functional effects on phenotypes and specific adaptation to particular environments.

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References

  • Alkan C, Kidd JM, Marques-Bonet T, Aksay G, Antonacci F, Hormozdiari F, Kitzman JO, Baker C, Malig M, Mutlu O, Sahinalp SC, Gibbs RA, Eichler EE (2009) Personalized copy number and segmental duplication maps using next-generation sequencing. Nat Genet 41:1061–1067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alvarez CE, Akey JM (2012) Copy number variation in the domestic dog. Mamm Genome 23:144–163

    Article  PubMed  Google Scholar 

  • Beckmann JS, Estivill X, Antonarakis SE (2007) Copy number variants and genetic traits: closer to the resolution of phenotypic to genotypic variability. Nat Rev Genet 8:639–646

    Article  CAS  PubMed  Google Scholar 

  • Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berglund J, Nevalainen EM, Molin AM, Perloski M, Consortium L, Andre C, Zody MC, Sharpe T, Hitte C, Lindblad-Toh K, Lohi H, Webster MT (2012) Novel origins of copy number variation in the dog genome. Genome Biol 13:R73

    Article  PubMed  PubMed Central  Google Scholar 

  • Blackburn A, Almeida M, Dean A, Curran JE, Johnson MP, Moses EK, Abraham LJ, Carless MA, Dyer TD, Kumar S, Almasy L, Mahaney MC, Comuzzie A, Williams-Blangero S, Blangero J, Lehman DM, Goring HH (2015) Effects of copy number variable regions on local gene expression in white blood cells of Mexican Americans. Eur J Hum Genet 23:1229–1235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown KH, Dobrinski KP, Lee AS, Gokcumen O, Mills RE, Shi X, Chong WW, Chen JY, Yoo P, David S, Peterson SM, Raj T, Choy KW, Stranger BE, Williamson RE, Zon LI, Freeman JL, Lee C (2012) Extensive genetic diversity and substructuring among zebrafish strains revealed through copy number variant analysis. Proc Natl Acad Sci U S A 109:529–534

    Article  CAS  PubMed  Google Scholar 

  • Cingolani P, Platts A, Wang Le L, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 6:80–92

    Article  CAS  Google Scholar 

  • Conrad DF, Pinto D, Redon R, Feuk L, Gokcumen O, Zhang Y, Aerts J, Andrews TD, Barnes C, Campbell P, Fitzgerald T, Hu M, Ihm CH, Kristiansson K, Macarthur DG, Macdonald JR, Onyiah I, Pang AW, Robson S, Stirrups K, Valsesia A, Walter K, Wei J, Wellcome Trust Case Control C, Tyler-Smith C, Carter NP, Lee C, Scherer SW, Hurles ME (2010) Origins and functional impact of copy number variation in the human genome. Nature 464:704–712

    Article  CAS  PubMed  Google Scholar 

  • Oliveira CA, Ribeiro RP, Yoshida GM, Kunita NM, Rizzato GS, De Oliveira SN, Dos Santos AI, Nguyen NH (2016) Correlated changes in body shape after five generations of selection to improve growth rate in a breeding program for Nile tilapia Oreochromis niloticus in Brazil. J Appl Genet 57:487–493

  • El-Sayed A (2006) Environmental requirements in tilapia culture. CABI Publishing, Oxfordshire

  • Fakhro KA, Yousri NA, Rodriguez-Flores JL, Robay A, Staudt MR, Agosto-Perez F, Salit J, Malek JA, Suhre K, Jayyousi A, Zirie M, Stadler D, Mezey JG, Crystal RG (2015) Copy number variations in the genome of the Qatari population. BMC Genomics 16:834

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghosh S, Qu Z, Das PJ, Fang E, Juras R, Cothran EG, Mcdonell S, Kenney DG, Lear TL, Adelson DL, Chowdhary BP, Raudsepp T (2014) Copy number variation in the horse genome. PLoS Genet 10:e1004712

    Article  PubMed  PubMed Central  Google Scholar 

  • Green BW (2006) Tilapia fingerling production systems. Food Products Press, Binghamton

    Google Scholar 

  • Hastings PJ, Lupski JR, Rosenberg SM, Ira G (2009) Mechanisms of change in gene copy number. Nat Rev Genet 10:551–564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henrichsen CN, Vinckenbosch N, Zollner S, Chaignat E, Pradervand S, Schutz F, Ruedi M, Kaessmann H, Reymond A (2009) Segmental copy number variation shapes tissue transcriptomes. Nat Genet 41:424–429

    Article  CAS  PubMed  Google Scholar 

  • Hou Y, Liu GE, Bickhart DM, Cardone MF, Wang K, Kim ES, Matukumalli LK, Ventura M, Song J, Vanraden PM, Sonstegard TS, Van Tassell CP (2011) Genomic characteristics of cattle copy number variations. BMC Genomics 12:127

    Article  PubMed  PubMed Central  Google Scholar 

  • Iskow RC, Gokcumen O, Lee C (2012) Exploring the role of copy number variants in human adaptation. Trends Genet 28:245–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang L, Jiang J, Yang J, Liu X, Wang J, Wang H, Ding X, Liu J, Zhang Q (2013) Genome-wide detection of copy number variations using high-density SNP genotyping platforms in Holsteins. BMC Genomics 14:131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kato M, Kawaguchi T, Ishikawa S, Umeda T, Nakamichi R, Shapero MH, Jones KW, Nakamura Y, Aburatani H, Tsunoda T (2010) Population-genetic nature of copy number variations in the human genome. Hum Mol Genet 19:761–773

    Article  CAS  PubMed  Google Scholar 

  • Kijas JW, Barendse W, Barris W, Harrison B, Mcculloch R, Mcwilliam S, Whan V (2011) Analysis of copy number variants in the cattle genome. Gene 482:73–77

    Article  CAS  PubMed  Google Scholar 

  • Klambauer G, Schwarzbauer K, Mayr A, Clevert DA, Mitterecker A, Bodenhofer U, Hochreiter S (2012) cn.MOPS: mixture of Poissons for discovering copy number variations in next-generation sequencing data with a low false discovery rate. Nucleic Acids Res 40:e69

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing, S (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Li P, Guo M, Wang C, Liu X, Zou Q (2015) An overview of SNP interactions in genome-wide association studies. Brief Funct Genomics 14:143–155

    Article  PubMed  Google Scholar 

  • Liu F, Sun F, Xia JH, Li J, Fu GH, Lin G, Tu RJ, Wan ZY, Quek D, Yue GH (2014) A genome scan revealed significant associations of growth traits with a major QTL and GHR2 in tilapia. Sci Rep 4:7256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu GE, Bickhart DM (2012) Copy number variation in the cattle genome. Funct Integr Genomics 12:609–624

    Article  CAS  PubMed  Google Scholar 

  • Liu GE, Hou Y, Zhu B, Cardone MF, Jiang L, Cellamare A, Mitra A, Alexander LJ, Coutinho LL, Dell’aquila ME, Gasbarre LC, Lacalandra G, Li RW, Matukumalli LK, Nonneman D, Regitano LC, Smith TP, Song J, Sonstegard TS, Van Tassell CP, Ventura M, Eichler EE, Mcdaneld TG, Keele JW (2010) Analysis of copy number variations among diverse cattle breeds. Genome Res 20:693–703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Zhang L, Xu L, Ren H, Lu J, Zhang X, Zhang S, Zhou X, Wei C, Zhao F, Du L (2013) Analysis of copy number variations in the sheep genome using 50 K SNP BeadChip array. BMC Genomics 14:229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Locke ME, Milojevic M, Eitutis ST, Patel N, Wishart AE, Daley M, Hill KA (2015) Genomic copy number variation in Mus musculus. BMC Genomics 16:497

    Article  PubMed  PubMed Central  Google Scholar 

  • Maldonado Dos Santos JV, Valliyodan B, Joshi T, Khan SM, Liu Y, Wang J, Vuong TD, Oliveira MDF, Marcelino-Guimarães FC, Xu D, Nguyen HT, Abdelnoor RV (2016) Evaluation of genetic variation among Brazilian soybean cultivars through genome resequencing. BMC Genomics 17:1–18

    Article  Google Scholar 

  • Marsh DJ, Theodosopoulos G, Martin-Schulte K, Richardson AL, Philips J, Roher HD, Delbridge L, Robinson BG (2003) Genome-wide copy number imbalances identified in familial and sporadic medullary thyroid carcinoma. J Clin Endocrinol Metab 88:1866–1872

    Article  CAS  PubMed  Google Scholar 

  • Mccarthy MI, Abecasis GR, Cardon LR, Goldstein DB, Little J, Ioannidis JP, Hirschhorn JN (2008) Genome-wide association studies for complex traits: consensus, uncertainty and challenges. Nat Rev Genet 9:356–369

    Article  CAS  PubMed  Google Scholar 

  • Mckenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, Depristo MA (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mills RE, Walter K, Stewart C, Handsaker RE, Chen K, Alkan C, Abyzov A, Yoon SC, Ye K, Cheetham RK, Chinwalla A, Conrad DF, Fu Y, Grubert F, Hajirasouliha I, Hormozdiari F, Iakoucheva LM, Iqbal Z, Kang S, Kidd JM, Konkel MK, Korn J, Khurana E, Kura D, Lam HYK, Leng J, Li R, Li Y, Lin C-Y, Luo R, Mu XJ, Nemesh J, Peckham HE, Rausch T, Scally A, Shi X, Stromberg MP, Stütz AM, Urban AE, Walker JA, Wu J, Zhang Y, Zhang ZD, Batzer MA, Ding L, Marth GT, Mcvean G, Sebat J, Snyder M, Wang J, Ye K, Eichler EE, Gerstein MB, Hurles ME, Lee C, Mccarroll SA, Korbel JO, Genomes P (2011) Mapping copy number variation by population scale genome sequencing. Nature 470:59–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moro C, Cornette R, Vieaud A, Bruneau N, Gourichon D, Bed’hom B, Tixier-Boichard M (2015) Quantitative effect of a CNV on a morphological trait in chickens. PLoS One 10:e0118706

    Article  PubMed  PubMed Central  Google Scholar 

  • Nagao M, Asai A, Sugihara H, Oikawa S (2015) Transgenerational changes of metabolic phenotypes in two selectively bred mouse colonies for different susceptibilities to diet-induced glucose intolerance. Endocr J 62:371–378

    Article  CAS  PubMed  Google Scholar 

  • Nyamweya CS, Mlewa CM, Ngugi CC, Kaunda-Arara B (2010) Daily growth of young-of-the-year of the Baringo tilapia, Oreochromis niloticus baringoensis (Trewavas, 1983). Afr Zool 45:139–143

    Article  Google Scholar 

  • Orozco LD, Cokus SJ, Ghazalpour A, Ingram-Drake L, Wang S, Van Nas A, Che N, Araujo JA, Pellegrini M, Lusis AJ (2009) Copy number variation influences gene expression and metabolic traits in mice. Hum Mol Genet 18:4118–4129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel RK, Jain M (2012) NGS QC toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 7:e30619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paudel Y, Madsen O, Megens HJ, Frantz LA, Bosse M, Bastiaansen JW, Crooijmans RP, Groenen MA (2013) Evolutionary dynamics of copy number variation in pig genomes in the context of adaptation and domestication. BMC Genomics 14:449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinto D, Darvishi K, Shi X, Rajan D, Rigler D, Fitzgerald T, Lionel AC, Thiruvahindrapuram B, Macdonald JR, Mills R, Prasad A, Noonan K, Gribble S, Prigmore E, Donahoe PK, Smith RS, Park JH, Hurles ME, Carter NP, Lee C, Scherer SW, Feuk L (2011) Comprehensive assessment of array-based platforms and calling algorithms for detection of copy number variants. Nat Biotechnol 29:512–520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinto D, Marshall C, Feuk L, Scherer SW (2007) Copy-number variation in control population cohorts. Hum Mol Genet 16 Spec No. 2:R168–R173

  • Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Redon R, Ishikawa S, Fitch KR, Feuk L, Perry GH, Andrews TD, Fiegler H, Shapero MH, Carson AR, Chen W, Cho EK, Dallaire S, Freeman JL, Gonzalez JR, Gratacos M, Huang J, Kalaitzopoulos D, Komura D, Macdonald JR, Marshall CR, Mei R, Montgomery L, Nishimura K, Okamura K, Shen F, Somerville MJ, Tchinda J, Valsesia A, Woodwark C, Yang F, Zhang J, Zerjal T, Zhang J, Armengol L, Conrad DF, Estivill X, Tyler-Smith C, Carter NP, Aburatani H, Lee C, Jones KW, Scherer SW, Hurles ME (2006) Global variation in copy number in the human genome. Nature 444:444–454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rovelet-Lecrux A, Hannequin D, Raux G, Le Meur N, Laquerriere A, Vital A, Dumanchin C, Feuillette S, Brice A, Vercelletto M, Dubas F, Frebourg T, Campion D (2006) APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat Genet 38:24–26

    Article  CAS  PubMed  Google Scholar 

  • Sebat J, Lakshmi B, Malhotra D, Troge J, Lese-Martin C, Walsh T, Yamrom B, Yoon S, Krasnitz A, Kendall J, Leotta A, Pai D, Zhang R, Lee YH, Hicks J, Spence SJ, Lee AT, Puura K, Lehtimaki T, Ledbetter D, Gregersen PK, Bregman J, Sutcliffe JS, Jobanputra V, Chung W, Warburton D, King MC, Skuse D, Geschwind DH, Gilliam TC, Ye K, Wigler M (2007) Strong association of de novo copy number mutations with autism. Science 316:445–449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simon-Sanchez J, Scholz S, Matarin Mdel M, Fung HC, Hernandez D, Gibbs JR, Britton A, Hardy J, Singleton A (2008) Genomewide SNP assay reveals mutations underlying Parkinson disease. Hum Mutat 29:315–322

    Article  CAS  PubMed  Google Scholar 

  • Suresh AV, Lin CK (1992) Tilapia culture in saline waters: a review. Aquaculture 106:201–226

    Article  Google Scholar 

  • Tremmel R, Klein K, Winter S, Schaeffeler E, Zanger UM (2015) Gene copy number variation analysis reveals dosage-insensitive expression of CYP2E1. Pharmacogenomics J 16:551-558

  • Vignal A, Milan D, Sancristobal M, Eggen A (2002) A review on SNP and other types of molecular markers and their use in animal genetics. Genet Sel Evol 34:275–305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Jiang J, Fu W, Jiang L, Ding X, Liu JF, Zhang Q (2012) A genome-wide detection of copy number variations using SNP genotyping arrays in swine. BMC Genomics 13:273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weaver S, Dube S, Mir A, Qin J, Sun G, Ramakrishnan R, Jones RC, Livak KJ (2010) Taking qPCR to a higher level: analysis of CNV reveals the power of high throughput qPCR to enhance quantitative resolution. Methods 50:271–276

    Article  CAS  PubMed  Google Scholar 

  • Winchester L, Yau C, Ragoussis J (2009) Comparing CNV detection methods for SNP arrays. Brief Funct Genomic Proteomic 8:353–366

    Article  CAS  PubMed  Google Scholar 

  • Xia JH, Bai Z, Meng Z, Zhang Y, Wang L, Liu F, Jing W, Wan ZY, Li J, Lin H, Yue GH (2015) Signatures of selection in tilapia revealed by whole genome resequencing. Sci Rep 5:14168

    Article  CAS  PubMed  Google Scholar 

  • Xia JH, Wan ZY, Ng ZL, Wang L, Fu GH, Lin G, Liu F, Yue GH (2014) Genome-wide discovery and in silico mapping of gene-associated SNPs in Nile tilapia. Aquaculture 432:67–73

    Article  CAS  Google Scholar 

  • Xu L, Cole JB, Bickhart DM, Hou Y, Song J, Vanraden PM, Sonstegard TS, Van Tassell CP, Liu GE (2014) Genome wide CNV analysis reveals additional variants associated with milk production traits in Holsteins. BMC Genomics 15:683

    Article  PubMed  PubMed Central  Google Scholar 

  • Yalcin B, Wong K, Agam A, Goodson M, Keane TM, Gan X, Nellaker C, Goodstadt L, Nicod J, Bhomra A, Hernandez-Pliego P, Whitley H, Cleak J, Dutton R, Janowitz D, Mott R, Adams DJ, Flint J (2011) Sequence-based characterization of structural variation in the mouse genome. Nature 477:326–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan Y, Yang N, Cheng HH, Song J, Qu L (2015) Genome-wide identification of copy number variations between two chicken lines that differ in genetic resistance to Marek’s disease. BMC Genomics 16:843

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Mao L, Chen H, Bu F, Li G, Sun J, Li S, Sun H, Jiao C, Blakely R, Pan J, Cai R, Luo R, Van De Peer Y, Jacobsen E, Fei Z, Huang S (2015) Genome-wide mapping of structural variations reveals a copy number variant that determines reproductive morphology in cucumber. Plant Cell 27:1595–1604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 31572612); Natural Science Foundation of Guangdong Province, China (No. 2015A030313150); and the Special Program for Marine Fishery, Science, Technology and Industry Development Foundation of Guangdong Province (A201501A04). We would like to thank Mr. Baoqing Ye for editing English of this paper.

Author Contributions

JHX and GHY coordinated and supervised the project. BJL, LHL, ZNM, ZY, HRL, and GHY designed the research and performed experiments. JHX and BJL analyzed the data and wrote the paper. GHY finalized the paper.

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Authors and Affiliations

  1. State Key Laboratory of Biocontrol, Institute of Aquatic Economic Animals and Guangdong Provincial Key Laboratory for Aquatic Economic Animals, College of Life Sciences, Sun Yat-Sen University, Guangzhou, 510275, People’s Republic of China

    Bi Jun Li, Hong Lian Li, Zining Meng, Yong Zhang, Haoran Lin & Jun Hong Xia

  2. Molecular Population Genetics and Breeding Group, Temasek Life Sciences Laboratory, 1 Research Link, National University of Singapore, Singapore, 117604, Singapore

    Gen Hua Yue

  3. Department of Biological Sciences, National University of Singapore, Singapore, 117543, Singapore

    Gen Hua Yue

  4. School of Biological Sciences, Nanyang Technological University, 60 Nanyang Drive, Singapore, 637551, Singapore

    Gen Hua Yue

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  1. Bi Jun Li
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Correspondence to Gen Hua Yue or Jun Hong Xia.

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Electronic supplementary material

Supplementary Table S1

Summary for the CNVs identified in all 47 samples (XLSX 1386 kb)

Supplementary Table S2

Primer sequences for CNVs confirmation in this study (XLSX 10 kb)

Supplementary Table S3

The identified CNVs that significantly associated with the population types (XLSX 39 kb)

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Li, B.J., Li, H.L., Meng, Z. et al. Copy Number Variations in Tilapia Genomes. Mar Biotechnol 19, 11–21 (2017). https://doi.org/10.1007/s10126-017-9733-0

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