Skip to main content

Advertisement

Log in

Characterization of novel genotyping-by-sequencing (GBS)-based simple sequence repeats (SSRs) and their application for population genomics of Capoeta aculeata (Valenciennes, 1844)

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Background

The species Capoeta aculeata (Valenciennes, 1844) is one of the most important freshwater species endemic to Iran. However, the investigation of the population genetic structure of this species is limited by the low number of molecular markers currently described.

Methods and results

In this study, we implemented next generation sequencing technology to identify polymorphic microsatellite markers and investigate the population genetic structure of C. aculeata sampled from three geographical sites in Iran. We characterized and developed 36 novel polymorphic microsatellite markers and these loci were examined in 120 individuals from three populations occurring in the Zagros basin. The average number of alleles per locus varied from 1.7 to 16 (average = 7.89). The results showed that, the polymorphism information content (PIC) of these simple sequence repeat (SSR) loci varied from 0.254 to 0.888. The observed heterozygosity (HO) per locus ranged from 0.170 to 0.881, while the expected heterozygosity (HE) per locus was from 0.170 to 0.881. Among these SSR loci, 20 loci deviated significantly from the Hardy–Weinberg equilibrium after Bonferroni correction (p < 0.05).

Conclusions

These microsatellite markers could provide a valuable tool for future population and conservation genetics studies of C. aculeate and other closely related species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The datasets generated are available from the corresponding author upon request.

References

  1. Zareian H, Esmaeili HR, Freyhof J (2016) Capoeta anamisensis, a new species from the Minab and Hasan Langhi River drainages in Iran (Teleostei: Cyprinidae). Zootaxa 4083:126–142

    Article  Google Scholar 

  2. Bektas Y, Turan D, Aksu I, Ciftci Y, Eroglu O, Kalayci G, Belduz AO (2017) Molecular phylogeny of the genus Capoeta (Teleostei: Cyprinidae) in Anatolia. Turkey Biochem Syst Ecol 70:80–94

    Article  CAS  Google Scholar 

  3. Freyhof J, Esmaeili HR, Sayyadzadeh G, Geiger M (2014) Review of the crested loaches of the genus Paracobitis from Iran and Iraq with the description of four new species (Teleostei:Nemacheilidae). Ichthyol Explor Fresh 25(1):11–38

    Google Scholar 

  4. Nazari S, Paknejad H, Jalali A, Khorshidi Z (2021) Molecular genetic divergence of five genera of cypriniform fish in Iran assessed by DNA barcoding. Iran J Fish Sci 20(3):628–645

    Google Scholar 

  5. Parmaksız A, Eksi E (2017) Genetic diversity of the cyprinid fish Capoeta trutta (Heckel, 1843) populations from Euphrates and Tigris rivers in Turkey based on mtDNA COI sequences. Indian J Fish 64(1):18–22

    Article  Google Scholar 

  6. Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203

    Article  CAS  Google Scholar 

  7. Zane L, Bargelloni L, Patarnello T (2002) Strategies for microsatellite isolation: a review. Mol Ecol 11:1–16

    Article  CAS  Google Scholar 

  8. Chang Y, Feng Z, Yu J, Ding J (2009) Genetic variability analysis in five populations of the sea cucumber Stichopus (Apostichopus) japonicus from China, Russia, South Korea and Japan as revealed by microsatellite markers. Mar Ecol 30:455–461

    Article  CAS  Google Scholar 

  9. Xue D, Zhang T, Liu J (2014) Microsatellite evidence for high frequency of multiple paternity in the marine gastropod Rapana venosa. PLoS ONE. https://doi.org/10.1371/journal.pone.0086508

    Article  PubMed  PubMed Central  Google Scholar 

  10. Montanari S, Perchepied L, Renault D, Frijters L, Velasco R, Horner M, Gardiner SE, Chagné D, Bus VGM, Durel CE, Malnoy M (2016) A QTL detected in an inter specific pear population confers stable fire blight resistance across different environments and genetic backgrounds. Mol Breeding 36:1–16

    Article  CAS  Google Scholar 

  11. Jia SW, Liu P, Li J, Li JT, Pan LQ (2013) Isolation and characterization of polymorphic microsatellite loci in the ridgetail white prawn Exopalaemon carinicauda. Genet Mol Res 12:2816–2820

    Article  CAS  Google Scholar 

  12. Perina A, Gonzlez-Tizn AM, Vizcano A, Gonzlez-Ortegn E, Martnez-Lage A (2016) Isolation and characterization of 20 polymorphic microsatellite loci in Palaemon serratus and cross-amplification in Palaemon species by 454 pyrosequencing. Conserv Genet Resour 8:169–196

    Article  Google Scholar 

  13. Gandomkar H, Shekarabi SPH, Abdolhay HA, Nazari S, Mehrjan MS (2020) Genetic structure of the Capoeta aculeata populations inferred from microsatellite DNA loci. Biodiversitas 21:4565–4570. https://doi.org/10.13057/biodiv/d211014

    Article  Google Scholar 

  14. Dutta N, Singh RK, Mohindra V, Pathak A, Kumar R, Sah P, Mandal S, Kaur G, Lal KK (2019) Microsatellite marker set for genetic diversity assessment of primitive Chitala chitala (Hamilton, 1822) derived through SMRT sequencing technology. Mol Biol Rep 46(1):41–49

  15. Qiu B, Fang S, Ikhwanuddin M, Wong L, Ma H (2020) Genome survey and development of polymorphic microsatellite loci for Sillago sihama based on Illumina sequencing technology. Mol Biol Rep 47(4):3011–3017

  16. Feng N, Ma H, Ma C et al (2014) Characterization of 40 single nucleotide polymorphism (SNP) via T m-shift assay in the mud crab (Scylla paramamosain). Mol Biol Rep 41:5467–5471. https://doi.org/10.1007/s11033-014-3420-2

    Article  CAS  PubMed  Google Scholar 

  17. Xiao M, Hu Q, Zhao Y, Bao F, Cui F, Zheng R (2018) Development of 36 SNP markers in Ophiocephalus argus Cantor base on high throughput sequencing. Conserv Genet Resour 10(1):35–38. https://doi.org/10.1007/s12686-017-0757-6

    Article  Google Scholar 

  18. Khoshkholgh M, Nazari S (2020) Characterization of single nucleotide polymorphism markers for the narrow-clawed crayfish Pontastacus leptodactylus (Eschscholtz, 1823) based on RAD sequencing. Conserv Genet Resour. https://doi.org/10.1007/s12686-020-01154-8

    Article  Google Scholar 

  19. Ewers-Saucedo C, Zardus JD, Wares JP (2016) Microsatellite loci discovery from next-generation sequencing data and loci characterization in the epizoic barnacle Chelonibia testudinaria (Linnaeus, 1758). PeerJ. https://doi.org/10.7717/peerj.2019

    Article  PubMed  PubMed Central  Google Scholar 

  20. Wei N, Bemmels JB, Dick CW (2014) The effects of read length, quality and quantity on microsatellite discovery and primer development: from Illumina to PacBio. Mol Ecol Resour 14:953–965

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  22. Zhou J, Zhou B, Li Q et al (2017) Isolation and characterization of 33 EST-SNP markers in Schizothorax prenanti. Conserv Genet Resour 10:205–207. https://doi.org/10.1007/s12686-017-0799-9

    Article  Google Scholar 

  23. Yu L, Bai J, Cao T et al (2014) Genetic variability and relationships among six grass carp Ctenopharyngodon idella populations in China estimated using EST-SNP markers. Fish Sci 80:475–481. https://doi.org/10.1007/s12562-014-0709-y

    Article  CAS  Google Scholar 

  24. Luo H, Ye H, Xiao S-J et al (2016) Development of SNP markers associated with immune-related genes of Schizothorax prenanti. Conserv Genet Resour 8:223–226. https://doi.org/10.1007/s12686-016-0539-6

    Article  Google Scholar 

  25. Peng X, Zhao L, Liu J, Guo X (2018) Development of SNP markers for Xenocypris argentea based on transcriptomics. Conserv Genet Resour 10(4):679–684. https://doi.org/10.1007/s12686-017-0900-4

    Article  Google Scholar 

  26. Nazari S, Jafari V, Pourkazemi M, Kolangi Miandare H, Abdolhay H (2016) Association between myostatin gene (MSTN-1) polymorphism and growth traits in domesticated rainbow trout (Oncorhynchus mykiss). Agri Gene 1:109–115

    Article  Google Scholar 

  27. Khoshkholgh M, Nazari S (2019) The genetic diversity and differentiation of narrow-clawed crayfish Pontastacus leptodactylus (Eschscholtz, 1823) (Decapoda: Astacidea: Astacidae) in the Caspian Sea Basin, Iran as determined with mitochondrial and microsatellite DNA markers. J Crust Biol 39(2):112–120

    Article  Google Scholar 

  28. Wang S, Liu P, Lv J, Li Y, Cheng T, Zhang L (2016) Serial sequencing of iso-length rad tags for cost-efficient genome-wide profiling of genetic and epigenetic variations. Nat Protoc 11(11):2189–2200. https://doi.org/10.1038/nprot.2016.133

    Article  CAS  PubMed  Google Scholar 

  29. Bian L, Liu C, Liu G, Chen S, Zhang L, Ge J, Li F, Tan J (2018) SNP discovery in spotted halibut (Verasper variegatus) using restriction site-associated DNA sequencing (RAD-seq). Conserv Genet Resour 10(3):409–413

  30. Andrews S (2016) FastQC: a quality control tool for high throughput sequence data. Version 0.11.5. Babraham Institute, Cambridge, UK. http://www.bioinformatics.babraham.ac.uk/projects/fastqc

  31. Martin M (2011) Sequencing reads. EMBnet J 17:10–12

    Article  Google Scholar 

  32. Catchen JP, Hohenlohe SB, Amores A, Cresko W (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22(11):3124–3140

    Article  Google Scholar 

  33. Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. J Bioinform 22(13):1658–1659

  34. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  Google Scholar 

  35. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics 25:1754–1760

    Article  CAS  Google Scholar 

  36. Miller MP (1997) Tools for population genetic analyses (TFPGA) v 1.3: a windows program for the analysis of allozyme and molecular genetic data. Northern Arizona University, Flagstaff

    Google Scholar 

  37. Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  38. Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Resour 4(3):535–538

    Article  Google Scholar 

  39. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  CAS  Google Scholar 

  40. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research_an update. Bioinformatics 28:2537–2539

    Article  CAS  Google Scholar 

  41. Excoffier L (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform. https://doi.org/10.1143/JJAP.34.L418

    Article  Google Scholar 

  42. Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for windows and linux. Mol Ecol Resour 8:103–106

    Article  Google Scholar 

  43. Ling LP, Adibah AB, Tan SG et al (2013) Isolation by the 5′ anchored PCR technique and characterization of eighteen microsatellite loci in horseshoe crab (Tachypleus gigas). J Genet 92:101–104. https://doi.org/10.1007/s12041-011-0115-5

    Article  Google Scholar 

  44. Ariede RB, Freitas MV, Hata ME, Matrochirico-Filho VA, Utsunomia R, Mendonça FF et al (2018) Development of microsatellite markers using next-generation sequencing for the fish Colossoma macropomum. Mol Biol Rep 45:9–18. https://doi.org/10.1007/s11033-017-4134-z

    Article  CAS  PubMed  Google Scholar 

  45. Han Z, Xiao S, Li W, Ye K, Wang ZY (2018) The identification of growth, immune related genes and marker discovery through transcriptome in the yellow drum (Nibea albiflora). Genes Genomics 40:881–891. https://doi.org/10.1007/s13258-018-0697-x

    Article  CAS  PubMed  Google Scholar 

  46. Bazsalovicsová E, Koleniˇcová A, Králová-Hromadová I, Minárik G, Šoltys K, Kuchta R, Štefka J (2018) Development of microsatellite loci in zoonotic tapeworm Dibothriocephalus latus (Linnaeus, 1758), Lühe, 1899 (syn. Diphyllobothrium latum) using microsatellite library screening. Mol Biochem Parasitol 225:1–3

    Article  Google Scholar 

  47. Gravley MC, Pierson BJ, Sage GK, Ramey AM, Talbot SL (2018) DNA microsatellite markers for northern fulmar (Fulmaris glacialis) and cross-species amplification in select seabird species, Alaska 2018. U.S. Geological Survey data release. https://doi.org/10.5066/P9KWA9VZ

  48. Patel A, Das P, Barat A, Meher PK, Jayasankar P (2010) Utility of cross-species amplification of 34 rohu microsatellite loci in Labeo bata, and their transferability in six other species of the cyprinidae family. Aquac Res 41:590–593

    Article  CAS  Google Scholar 

  49. Gao Z, Luo W, Liu H, Zeng C, Liu X, Yi S, Wang W (2012) Transcriptome analysis and SSR/SNP markers information of the blunt snout bream (Megalobrama amblycephala). PLoS ONE. https://doi.org/10.1371/journal.pone.0042637

    Article  PubMed  PubMed Central  Google Scholar 

  50. Fitch AJ, Leeworthy G, Li X, Bowman W, Turner L, Gardner MG (2013) Isolation and characterisation of eighteen microsatellite markers from the sea cucumber Holothuria scabra (Echinodermata: Holothuriidae). Aust J Zool 60:368–371

    Article  Google Scholar 

  51. Norrell AE, Crawley D, Jones KL, Saillant EA (2014) Development and characterization of eighty-four microsatellite markers for the red snapper (Lutjanus campechanus) using Illumina paired-end sequencing. Aquaculture 430:128–132

    Article  CAS  Google Scholar 

  52. Fan S, Wang J, Huang G, Liu B, Yu D (2015) Identification of twenty novel polymorphic microsatellite DNA markers from transcripts of the pearl oyster Pinctada fucata using next-generation sequencing approach. J Genet 94:82–85

    Article  Google Scholar 

  53. Rodrigues MDN, Moreira CGÁ, Gutierrez HJP, Almeida DB, Junoir D, Moreira HLM (2015) Development of microsatellite markers for use in breeding catfish, Rhamdia sp. Afr J Biotechnol 14:400–411

    Article  Google Scholar 

  54. Yu JN, Kim SK, Sagong J, Ryu SH, Chae B (2019) Identification of microsatellite markers and their application in yellow catfish (Pseudobagrus fulvidraco Richardson, 1846) population genetics of Korea. J Genet 98:2–7

    Article  Google Scholar 

  55. Nazari S, Pourkazemi M, Khoshkholgh MR (2019) Analysis of the genetic structure of the Persian sturgeon (Acipenser persicus) populations: comparison of control region sequencing and PCR-RFLP analysis of mitochondrial DNA. Iran J Fish Sci 19(6):3201–3220

    Google Scholar 

  56. Peyran C, Planes S, Tolou N, Iwankow G, Boissin E (2020) Development of 26 highly polymorphic microsatellite markers for the highly endangered fan mussel Pinna nobilis and cross-species amplification. Mol Biol Rep 4:2551–2559

    Article  Google Scholar 

  57. Pathak RU, Mamillapalli A, Rangaraj N, Kumar RP, Vasanthi D, Mishra K, Mishra RK (2013) AAGAG repeat RNA is an essential component of nuclear matrix in Drosophila. RNA Biol 10(4):564–571

    Article  CAS  Google Scholar 

  58. Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O, Lepoittevin C, Malausa T, Revardel E, Salin F, Petit RJ (2011) Current trends in microsatellite genotyping. Mol Ecol Resour 11:591–611

    Article  CAS  Google Scholar 

  59. Ma H, Zou X, Ji X, Ma C, Lu J, Jiang W, Xia L, Li S, Liu Y, Gong Y, Ma L (2013) Discovery and characterization of a first set of polymorphic microsatellite markers in red crab (Charybdis feriatus). J Genet 92:e113–e115

    PubMed  Google Scholar 

  60. Zalapa JE, Cuevas H, Zhu H, Steffan S, Senalik D, Zeldin E, McCown B, Harbut R, Simon P (2012) Using next-generation sequencing approaches to isolate simple sequence repeat (SSR) loci in the plant sciences. Am J Bot 99:193–208

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Research Fund for the department of Fisheries of the Islamic Azad University of Tehran, Iran.

Author information

Authors and Affiliations

Authors

Contributions

HG made the literature, sample collection, material preparation. SPHS has major contribution to the preliminary study design and interpretation of data. The first draft of the manuscript was written by HAA. SN designed the experiment, institutional support and supervision of the preliminary experiment and made the data analysis. MSM has significant contributions to the laboratory work and interpretation of the results. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Seyed Pezhman Hosseini Shekarabi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The main research project researcher of this work was approved for animal ethics by Iranian Fisheries Sciences Research Institute (IFSRI) for scientific purposes development, Iran. All applicable guidelines for the care and use of animals were followed by the authors. The experiment was approved for Animal Welfare by the Institutional Animal Welfare Committee of Agricultural Research, Education and Extension Organization (AREEO), Iran.

Informed consent

This research does not involve humans and therefore informed consents are not applicable.

Consent to participate (ethics)

Informed consent was obtained from all individual participants included in the study.

Consent to publish (ethics)

The participant has consented to the submission of the report to the journal.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gandomkar, H., Shekarabi, S.P.H., Abdolhay, H.A. et al. Characterization of novel genotyping-by-sequencing (GBS)-based simple sequence repeats (SSRs) and their application for population genomics of Capoeta aculeata (Valenciennes, 1844). Mol Biol Rep 48, 6471–6480 (2021). https://doi.org/10.1007/s11033-021-06653-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-021-06653-x

Keywords

Navigation