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Development of microsatellite markers using next-generation sequencing for the fish Colossoma macropomum

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Abstract

Tambaqui (Colossoma macropomum) is a fish species from the Amazon and Orinoco Rivers, with favorable characteristics to the cultivation system and great market acceptance in South America. However, the construction of a genetic map for the genetic improvement of this species is limited by the low number of molecular markers currently described. Thus, this study aimed to validate gene-associated and anonymous (non-genic) microsatellites obtained by next generation sequencing (RNA-seq and whole genome shotgun—WGS, respectively), for future construction of a genetic map and search for quantitative trait loci (QTL) in this species. In the RNA-seq data, the observed and expected heterozygosity (Ho and He) ranged from 0.09 to 0.73, and 0.09 to 0.85, respectively. In the WGS data, Ho and He ranged from 0.33 to 0.95, and 0.28 to 0.92, respectively. In general, the evaluation of 200 markers resulted in 45 polymorphic loci, of which 14 were gene-associated (RNA-Seq) and 31 were anonymous (WGS). Moreover, some markers were related to genes of the immune system, biological regulation/control and biogenesis. This study contributes to increase the number of molecular markers available for genetic studies in C. macropomum, which will allow the development of breeding programs assisted by molecular markers.

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References

  1. Eigenmann CH (1915) The Serrasalminae and Mylinae. Ann Carnegie Mus 9:226–271

    Google Scholar 

  2. Britski HA (1977) Sobre o gênero Colossoma (Pisces, Characidae). Ciência e Cultura 29:810

    Google Scholar 

  3. Gomes LC, Simões LN, Araújo-Lima CARM (2010) Tambaqui (Colossoma macropomum). In: Baldisserotto B, Gomes LC (eds) Espécies nativas para piscicultura no Brasil, 2nd ed. Editora UFSM, Santa Maria, pp 175–204

    Google Scholar 

  4. Hashimoto DT, Senhorini JA, Foresti F, Porto-Foresti F (2012) Interspecific fish hybrids in Brazil: management of genetic resources for sustainable use. Rev Aquacult 4:108–118

    Article  Google Scholar 

  5. IBGE (2015) Instituto Brasileiro de Geografia e Estatística. Rio de Janeiro Produção da Pecuária Municipal, vol 43

  6. Valladão GMR, Gallani SU, Pilarski F (2016) South American fish for continental aquaculture. Rev Aquacult 0:1–19

    Google Scholar 

  7. Souza AP (2001) Biologia molecular aplicada ao melhoramento. In: Nass LL, Valois ACC, Mello IS, Valadares-Inglis MC (eds) Recursos genéticos e melhoramento de plantas. Fundação MT, Rondonópolis, pp 939–965

    Google Scholar 

  8. Santos MCF, Hrbek T, Farias IP (2009) Microsatellite markers for the tambaqui (Serrasalmidae, Characiformes), an economically important keystone species of the Amazon River floodplain. Mol Ecol Res 9:874–876

    Article  CAS  Google Scholar 

  9. Hamoy IG, Cidade FW, Barbosa MS, Gonçalves EC, Santos D (2010) Isolation and characterization of tri and tetranucleotide microsatellite markers for the tambaqui (Colossoma macropomum, Serrasalmidae, Characiformes). Conserv Genet Resour 3:33–36

    Article  Google Scholar 

  10. Santana GX, Santos CHA, Sousa CFS, Nascimento PRM, Paula-Silva MN, Sousa ACB, Campos T, Almeida-Val VMF (2012) Isolation of novel microsatellite markers for tambaqui (Colossoma macropomum, Cuvier 1818), an importante freshwater fish of the Amazon. Conserv Genet Resour 4:197–200

    Article  Google Scholar 

  11. Bouza C, Hermida M, Pardo BG et al (2007) A microsatellite genetic map of the turbot (Scophthalmus maximus). Genetics 177:2457–2467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ruan X, Wang W, Kong J, Yu F, Huang X (2010) Genetic linkage mapping of turbot (Scophthalmus maximus L.) using microsatellite markers and its application in QTL analysis. Aquaculture 308(3):89–100

    Article  CAS  Google Scholar 

  13. Billotte N, Lagoda PJL, Risterucci AM, Baurens FC (1999) Microsatellite-enriched libraries: applied methodology for the development of SSR markers in tropical crops. Fruits 54:277–288

    CAS  Google Scholar 

  14. Seeb JE, Carvalho G, Hauser L (2011) Single-nucleotide polymorphism (SNP) discovery and applications of SNP genotyping in nonmodel organisms. Mol Ecol Res 11:1–8

    Article  Google Scholar 

  15. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nature 12(7):499–510

    CAS  Google Scholar 

  16. Carvalho DC, Rodríguez-Zárate CJ, Hammer MP, Beheregaray B (2011) Development of 21 microsatellite markers for the threatened Yarra pygmy perch (Nannoperca obscura) through 454 shot-gun pyrosequencing. Conserv Genet Resour 3:601–604

    Article  Google Scholar 

  17. Carvalho DC, Beheregaray LB (2011) Rapid development of microsatellites for the endangered Neotropical catfish Conorhynchus conirostris using a modest amount of 454 shot-gun pyrosequencing. Conserv Genet Resour 3:373–375

    Article  Google Scholar 

  18. Liu S, Zhou Z, Lu J (2011) Generation of genome-scale gene-associated SNPs in catfish for the construction of a high-density SNP array. BMC Genomics 12:53

    Article  CAS  Google Scholar 

  19. Ji P, Liu G, Xu J, Wang X, Li J, Zhao Z (2012) Characterization of common carp transcriptome: sequencing, de novo assembly, annotation and comparative genomics. PLoS ONE 7(4):e35152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Long Y, Li Q, Zhou B (2013) De novo assembly of Mud Loach (Misgurnus anguillicaudatus) skin transcriptome to identify putative genes involved in immunity and epidermal mucus secretion. PLoS ONE 8:e56998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Gross JB, Furter A, Carlson BM (2013) An integrated transcriptome-wide analysis of cave and surface dwelling Astyanax mexicanus. PLoS ONE 8:e55659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Margulies M, Egholm M, Altman WE et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437(7057):376–380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Faircloth BC (2008) Msatcommander: detection of microsatellite repeat arrays and automated, locus-specific primer design. Mol Ecol Research 8:92–94

    Article  CAS  Google Scholar 

  24. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    CAS  PubMed  Google Scholar 

  25. Conesa A, Götz S, García-Gómez JM (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  26. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  CAS  PubMed  Google Scholar 

  27. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  28. Excoffier L, Laval G, Schneider S (2005) ARLEQUIN ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    Article  CAS  Google Scholar 

  29. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  PubMed  Google Scholar 

  30. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  PubMed  Google Scholar 

  31. Kalinowsk ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1006–1099

    Google Scholar 

  32. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  33. Chapuis MP, Estoup A (2006) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24(3):621–631

    Article  PubMed  Google Scholar 

  34. Rico C, Cuesta JA, Drake P et al (2017) Null alleles are ubiquitous at microsatellite loci in the Wedge Clam (Donax trunculus). PeerJ 5:e3188

    Article  PubMed  PubMed Central  Google Scholar 

  35. Carvalho DC, Rodríguez-Zárate CJ, Hammer MP et al (2011) Development of 21 microsatellite markers for the threatened Yarra pygmy perch (Nannoperca obscura) through 454 shot-gun pyrosequencing. Conserv Genet Resour 3(4):601–604

    Article  Google Scholar 

  36. Chistiakov DA, Hellemans B, Volckaert FA (2006) Microsatellites and their genomic distribution, evolution, function and applications: a review with special reference to fish genetics. Aquaculture 255(1):1–29

    Article  CAS  Google Scholar 

  37. Mandal S, Jena JK, Singh RK et al (2016) De novo development and characterization of polymorphic microsatellite markers in a schilbid catfish, Silonia silondia (Hamilton, 1822) and their validation for population genetic studies. Mol Biol Rep 43(2):91–98

    Article  CAS  PubMed  Google Scholar 

  38. Zheng X, Kuang Y, Lü W et al (2014) Transcriptome-derived EST–SSR markers and their correlations with growth traits in crucian carp Carassius auratus. Fish Sci 80(5):977–984

    Article  CAS  Google Scholar 

  39. Papetti C, Harms L, Jürgens J et al (2016) Microsatellite markers for the notothenioid fish Lepidonotothen nudifrons and two congeneric species. BMC Res Notes 9:238

    Article  PubMed  PubMed Central  Google Scholar 

  40. Yue GH, Li Y, Orban L (2001) Characterization of microsatellites in the IGF-2 and GH genes of Asian seabass (Lates calcarifer). Mar Biotechnol 3:1–3

    Article  CAS  PubMed  Google Scholar 

  41. Yue GH, Orban L (2002) Microsatellites from genes show polymorphism in two related Oreochromis species. Mol Ecol Notes 2:99–100

    Article  CAS  Google Scholar 

  42. Yue GH, Ho MY, Orban L, Komen J (2003) Microsatellites within genes and ESTs of common carp and their applicability in silver crucian carp. Aquaculture 234:85–98

    Article  Google Scholar 

  43. Vasemägi A, Nilsson J, Primmer CR (2005) Expressed sequence tag-linked microsatellite as a source of gene-associated polymorphisms for detecting signatures of divergente selection in Atlantic salmon (Salmo salar L.). Mol Biol Evol 22(4):1067–1076

    Article  PubMed  Google Scholar 

  44. Stenvik J, Wesmajervi MS, Fjalestad KT, Damsgard B, Delghandi M (2006) Development of 25 gene-associated microsatellite markers of Atlantic cod (Gadus morhua L.). Mol Ecol Notes 6:1105–1107

    Article  CAS  Google Scholar 

  45. Almuly R, Poleg-Danin Y, Gorshkov S, Rapoport B, Soller M, Kashi Y, Funkenstein B (2005) Characterization of the 5′ flanking region of the growth hormone gene of the marine teleost, gilthead sea bream Sparus aurata: analysis of a polymorphic microsatellite in the proximal promoter. Fish Sci 71(3):479–490

    Article  CAS  Google Scholar 

  46. Drew RE, Settles ML, Churchill EJ, Williams SM, Balli S, Robison BD (2012) Brain transcriptome variation among behaviorally distinct strains of zebrafish (Danio rerio). BMC Genomics 13:323

    Article  CAS  Google Scholar 

  47. Sahlmann C, Sutherland BJG, Kortner TM, Koop BF, Krogdahl A, Bakke AM (2012) Early response of gene expression in the distal intestine of Atlantic salmon (Salmo salar L.) during the development of soybean meal induced enteritis. Fish Shellfish Immunol 34:599e609

    Google Scholar 

  48. Vasta GR, Nita-Lazar M, Giomarelli B et al (2011) Structural and functional diversity of the lectin repertoire in teleost fish: relevance to innate and adaptive immunity. Dev Comp Immunol 35(12):1388–1399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by grants from PROPE/UNESP (07/2015), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 446779/2014-8 and 305916/2015-7), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2014/03772-7), and CAPES. We thanks to Jonas da Paz Aguiar for providing samples of wild individuals from the Curuá-Uná River.

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Authors and Affiliations

  1. Centro de Aquicultura da Unesp, Universidade Estadual Paulista, Jaboticabal, SP, Brazil

    Raquel B. Ariede, Milena V. Freitas, Milene E. Hata, Vito A. Matrochirico-Filho, Fábio Porto-Foresti & Diogo T. Hashimoto

  2. Departamento de Morfologia, IBB, Universidade Estadual Paulista, Botucatu, SP, Brazil

    Ricardo Utsunomia & Fausto Foresti

  3. Instituto do Mar, Universidade Federal de São Paulo, UNIFESP, Santos, SP, Brazil

    Fernando F. Mendonça

  4. Departamento de Ciências Biológicas, FC, Universidade Estadual Paulista, Bauru, SP, Brazil

    Fábio Porto-Foresti

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  1. Raquel B. Ariede
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  2. Milena V. Freitas
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  9. Diogo T. Hashimoto
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Correspondence to Diogo T. Hashimoto.

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Ariede, R.B., Freitas, M.V., Hata, M.E. et al. Development of microsatellite markers using next-generation sequencing for the fish Colossoma macropomum . Mol Biol Rep 45, 9–18 (2018). https://doi.org/10.1007/s11033-017-4134-z

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  • DOI: https://doi.org/10.1007/s11033-017-4134-z

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