Skip to main content

Advertisement

SpringerLink
Log in

Cross-priming of microsatellite loci in subfamily cyprininae (family Cyprinidae): their utility in finding markers for population genetic analysis in three Indian major carps

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

This study is aimed to identify polymorphic microsatellite markers and establish their potential for population genetics studies in three carp (family cyprinidae; subfamily cyprininae) species, Labeo rohita, Catla catla and Cirrhinus mrigala through use of cyprinid primers. These species have high commercial value and knowledge of genetic variation is important for management of farmed and wild populations. We tested 108 microsatellite primers from 11 species belonging to three different cyprinid subfamilies, Cyprininae, Barbinae and Leuciscinae out of which 63 primers (58.33 %) successfully amplified orthologous loci in three focal species. Forty-two loci generated from 29 primers were polymorphic in these three carp species. Sequencing of amplified product confirmed the presence of SSRs in these 42 loci and orthologous nature of the loci. To validate potential of these 42 polymorphic loci in determining the genetic variation, we analyzed 486 samples of three focal species collected from Indus, Ganges and Brahmaputra river systems. Results indicated significant genetic variation, with mean number of alleles per locus ranging from 6.80 to 14.40 and observed heterozygosity ranging from 0.50 to 0.74 in the three focal species. Highly significant (P < 0.00001) allelic homogeneity values revealed that the identified loci can be efficiently used in population genetics analysis of these carp species. Further, thirty-two loci from 19 primers were useful for genotyping in more than one species. The data from the present study was compiled with cross-species amplification data from previous results on eight species of subfamily cyprininae to compare cross-transferability of microsatellite loci. It was revealed that out of 226 heterologous loci amplified, 152 loci that originated from 77 loci exhibited polymorphism and 45 primers were of multispecies utility, common for 2–7 species.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Thai BT, Burridge CP, Austin CM (2007) Genetic diversity of common carp (Cyprinus carpio L.) in Vietnam using four microsatellite loci. Aquaculture 269:174–186

    Article  CAS  Google Scholar 

  2. Abbas K, Zhou X, Li Y, Gao Z, Wang W (2010) Microsatellite diversity and population genetic structure of yellowcheek, Elopichthys bambusa (Cyprinidae) in the Yangtze River. Biochem Syst Ecol 38:806–812

    Article  CAS  Google Scholar 

  3. Jarne P, Lagoda PJL (1996) Microsatellites, from molecules to populations and back. Trends Ecol Evol 11:424–429

    Article  CAS  PubMed  Google Scholar 

  4. Gopalakrishnan A, Muneer PMA, Musammilu KK, Lal KK, Kapoor D, Mohindra V (2006) Primers from order Osteoglossiform and Siluriform detect polymorphic microsatellite loci in sun-catfish, Horabagrus brachysoma (Teleostei: Bagridae). J Appl Ichthyol 22(5):456–458

    Article  CAS  Google Scholar 

  5. Kim KS, Min MS, An JH, Lee H (2004) Cross-species amplification of Bovidae microsatellites and low diversity of the endangered Korean goral. J Heredity 95(6):521–525

    Article  CAS  Google Scholar 

  6. Nguyen TT, Genini S, Bui LC, Voegeli P, Stranzinger G, Renard JP, Maillard JC, Nguyen BX (2007) Genomic conservation of cattle microsatellite loci in wild gaur (Bos gaurus) and current genetic status of this species in Vietnam. BMC Genet 8:77. doi:10.1186/1471-2156-8-77

    Article  PubMed Central  PubMed  Google Scholar 

  7. Maudet C, Pereira AB, Zeyl E, Nagash H, Kence A, Özüt D, Duval MPB, Boolormaa S, Coltman DW, Taberlet P, Luikart G (2004) A standard set of polymorphic microsatellites for threatened mountain ungulates (Caprini, Artiodactyla). Mol Ecol Notes 4:49–55

    Article  CAS  Google Scholar 

  8. Jan C, Dawson DA, Altringham JD, Burke T, Butlin RK (2012) Development of conserved microsatellite markers of high cross-species utility in bat species (Vespertilionidae, Chiroptera, Mammalia). Mol Ecol Resour 12:532–548

    Article  CAS  PubMed  Google Scholar 

  9. Mohindra V, Mishra A, Palanichamy M, Ponniah AG (2001) Cross-species amplification of Catla catla microsatellite locus in Labeo rohita. Indian J Fish 48:103–108

    Google Scholar 

  10. Lal KK, Chauhan T, Mandal A, Singh RK, Khulbe L, Ponniah AG, Mohindra V (2004) Identification of microsatellite DNA markers or population structure analysis in Indian major carp, Cirrhinus mrigala (Hamilton–Buchanan, 1882). J Appl Ichthyol 20:87–91

    Article  CAS  Google Scholar 

  11. Tong J, Yu X, Liao X (2005) Characterization of a highly conserved microsatellite marker with utility potentials in cyprinid fishes. J Appl Ichthyol 21:232–235

    Article  CAS  Google Scholar 

  12. Chauhan T, Lal KK, Mohindra V, Singh RK, Punia P, Gopalakrishnan A, Sharma PC, Lakra WS (2007) Evaluating genetic differentiation in wild populations of the Indian major carp, Cirrhinus mrigala (Hamilton–Buchanan, 1882): evidence from allozyme and microsatellite markers. Aquaculture 269:135–149

    Article  CAS  Google Scholar 

  13. Peakall R, Gilmore S, Keys W, Morgante M, Rafalski A (1998) Cross-species amplification of soybean (Glycine max) simple sequence repeats (SSRs) within the genus and other legume genera: implications for the transferability of SSRs in plants. Mol Biol Evol 15(10):1275–1287

    Article  CAS  PubMed  Google Scholar 

  14. Anmarkrud JA, Kleven O, Bachmann L, Lifjeld JT (2008) Microsatellite evolution: mutations, sequence variation, and homoplasy in the hypervariable avian microsatellite locus HrU10. BMC Evol Biol. doi:10.1186/1471-2148-8-138

    PubMed Central  PubMed  Google Scholar 

  15. Estoup A, Jarne P, Cornuet JM (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetic analysis. Mol Ecol 11(9):1591–1604

    Article  CAS  PubMed  Google Scholar 

  16. Hua YG, Kovacs B, Orban L (2010) A new problem with cross-species amplification of microsatellites: generation of non-homologous products. Zool Res 31(2):131–140

    Article  Google Scholar 

  17. FAO (2006–2014) Fisheries and aquaculture software. FishStat Plus: Universal software for fishery statistical time series. FAO Fisheries and Aquaculture Department. Rome. http://www.fao.org/fishery/statistics/software/fishstat/en. Accessed 17 Jan 2014

  18. Penman DJ, Gupta MV, Dey MM (2005) Carp genetic resources for aquaculture in Asia. World Fish Center technical report, vol. 65, pp. 152

  19. Salgueiro P, Carvalho G, Pereira MJC, Coelho MM (2003) Microsatellite analysis of genetic population structure of the endangered cyprinid Anaecypris hispanica in Portugal: implications for conservation. Biol Conserv 109(1):47–56

    Article  Google Scholar 

  20. Luhariya RK, Lal KK, Singh RK, Mohindra V, Punia P, Chauhan UK, Gupta A, Lakra WS (2011) Genetic divergence in wild population of Labeo rohita (Hamilton, 1822) from nine Indian rivers, analyzed through mtDNA cytochrome b region. Mol Biol Rep 39(4):3659–3665

    Article  PubMed  Google Scholar 

  21. Das R, Mohindra V, Singh RK, Lal KK, Punia P, Masih P, Mishra RM, Lakra WS (2012) Intraspecific genetic diversity in wild Catla catla (Hamilton, 1822) populations assessed through MtDNA cytochrome b sequences. J Appl Ichthyol 28:280–283

    Article  Google Scholar 

  22. Ruzzante DE, Taggart C, Cook D, Goddard S (1996) Genetic differentiation between inshore and offshore Atlantic cod (Gadus morhua) off Newfoundland: microsatellite DNA variation and antifreeze level. Can J Fish Aquat Sci 53:634–645

    Article  Google Scholar 

  23. Das P, Barat A, Meher PK, Ray PP, Majumdar D (2005) Isolation and characterization of polymorphic microsatellites in Labeo rohita and their cross-species amplification in related species. Mol Ecol Notes 5:231–233

    Article  CAS  Google Scholar 

  24. Patel A, Das P, Swain SK, Meher PK, Jayasankar P, Sarangi N (2009) Development of 21 new microsatellite markers in Labeo rohita (rohu). Anim Genet 40:253–254

    Article  CAS  PubMed  Google Scholar 

  25. Patel A, Das P, Barat A, Meher PK, Pallipuram J (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. Aquacult Res 41:590–593

    Article  CAS  Google Scholar 

  26. Naish KA, Skibinski DOF (1998) Tetranucleotide microsatellite loci for Indian major carp. J Fish Biol 53:886–889

    Article  CAS  Google Scholar 

  27. Crooijmans RPMA, Bierbooms VAF, Komen J, Poe JJVD, Groenen MAM (1997) Microsatellite markers in common carp (Cyprinus carpio L.). Anim Genet 8:129–134

    Article  Google Scholar 

  28. Yue GH, Ho MY, Orban L, Komen J (2004) Microsatellites within genes and ESTs of common carp and their applicability in silver crucian carp. Aquaculture 234:85–98

    Article  CAS  Google Scholar 

  29. McConnell SKJ, Skibinski DOF, Mair GC (2001) Microsatellite markers from a commercially important south-east Asian cyprinid, the silver barb (Barbodes gonionotus Bleeker). Mol Ecol Notes 1(3):135–136

    Article  CAS  Google Scholar 

  30. Chenuil A, Galtier N, Berrebi P (1999) A test of the hypothesis of an autopolyploid vs. allopolyploid origin for a tetraploid lineage: application to the genus Barbus (Cyprinidae). Heredity 82:373–380

    Article  PubMed  Google Scholar 

  31. Dimsoski P, Gregory PT, Mark JB (2000) Microsatellite characterization in central stoneroller Campostoma anomalum (Pisces: Cyprinidae). Mol Ecol 9:2187–2189

    Article  CAS  PubMed  Google Scholar 

  32. Bessert ML, Orti G (2003) Microsatellite loci for paternity analysis in the fathead minnow, Pimephales promelas (Teleostei: Cyprinidae). Mol Ecol Notes 3(4):532–534

    Article  CAS  Google Scholar 

  33. Baerwald MR, May B (2004) Characterization of microsatellite loci for five members of the minnow family Cyprinidae found in the Sacramento: San Joaquin Delta and its tributaries. Mol Ecol Notes 4:385–390

    Article  CAS  Google Scholar 

  34. Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F (1997) GENETIX ver. 4.02, Genetics logicielsous windows pour Ia ge’ ne’ Tique des populations. http://www.univ-montp2.fr/~genetix/genetix.htm

  35. Raymond M, Rousset F (1995) GENEPOP (ver. 1.2): population genetics software for exact test and ecumenicism ver. 4.2. J Heredity 86:248–249. http://wbiomed.curtin.edu.au/genepop/

  36. 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

    PubMed Central  CAS  Google Scholar 

  37. Primmer CR, Moller AP, Ellegren H (1996) A wide-range survey of cross-species microsatellite amplification in birds. Mol Ecol 5:365–378

    Article  CAS  PubMed  Google Scholar 

  38. Gupta A, Lal KK, Punia P, Singh RK, Mohindra V, Sah RS, Kumar R, Luhariya RK, Dwivedi AK, Masih P, Mishra RM, Jena JK (2014) Characterization of polymorphic microsatellite markers and genetic diversity in wild bronze featherback, Notopterus notopterus (Pallas, 1769). Mol Biol Rep. doi:10.1007/s11033-013-2776-z

    PubMed Central  Google Scholar 

  39. Zardoya R, Doadrio I (1999) Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids. J Mol Evol 49:227–237

    Article  CAS  PubMed  Google Scholar 

  40. Wang X, Li J, He S (2007) Molecular evidence for the monophyly of east Asian groups of cyprinidae (Teleostei: Cypriniformes) derived from the nuclear recombination activating gene 2 sequences. Mol Phyl Evol 42:157–170

    Article  CAS  Google Scholar 

  41. Ellegren H, Moore S, Robinson N, Byrne K, Ward W, Sheldon BC (1997) Microsatellite evolution-A reciprocal study of repeat lengths at homologous loci in cattle and sheep. Mol Biol Evol 14(8):854–860

    Article  CAS  PubMed  Google Scholar 

  42. Singh RK, Lal KK, Mohindra V, Punia P, Lakra WS (2008) Cross species amplification of microsatellite loci in the cyprinid fish Labeo calbasu (Hamilton, 1822). Acta Zool Sin 54(5):937–940

    CAS  Google Scholar 

  43. Chaturvedi A, Mohindra V, Singh RK, Lal KK, Punia P, Bhaskar R, Mandal A, Narain L, Lakra WS (2011) Population genetic structure and phylogeography of cyprinid fish, Labeo dero (Hamilton, 1822) inferred from allozyme and microsatellite DNA marker analysis. Mol Biol Rep 38(5):3513–3529

    Article  CAS  PubMed  Google Scholar 

  44. Gopalakrishnan A, Musammilu KK, Basheer VS, John L, Padmakumar KG, Lal KK, Mohindra V, Punia P, Dinesh K, Manjebrayakath H, Ponniah AG, Lakra WS (2009) Low genetic differentiation in the populations of the Malabar Carp Labeo dussumieri as revealed by allozymes, microsatellites and RAPD. Asian Fish Sci 22:359–391

    Google Scholar 

  45. Sun Y, Lin HD, Tang WQ, Ju YM, Liu ZZ, Liu D, Yang JQ (2011) Polymorphic microsatellite loci isolated from the Squalidus argentatus using PCR-based isolation of microsatellite arrays (PIMA). Int J Mol Sci 12:5666–5671

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Singh RK, Lal KK, Mohindra V, Punia P, Sah RS, Kumar R, Gupta A, Das R, Lakra WS, Ayyappan S (2012) Genetic diversity of Indian major carp, Labeo calbasu (Hamilton, 1822) populations inferred from microsatellite loci. Biochem Syst Ecol 44:307–316

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  48. Musammilu KK, Muneer PMA, Gopalakrishnan A, Basheer VS, Gupta H, Mohindra V, Lal KK, Ponniah AG (2014) Identification and characterization of microsatellite markers for the population genetic structure in endemic red-tailed barb Gonoproktopterus curmuca. Mol Biol Rep. doi:10.1007/s11033-014-3164-z

    PubMed  Google Scholar 

Download references

Acknowledgments

The present work is part of a programme on Outreach Activity on Fish Genetic Stocks, funded by Indian Council of Agricultural Research (ICAR), New Delhi. The authors express their gratitude to Dr. S. Ayyappan, Director General, and ICAR for his guidance in undertaking this programme. The authors also thank Director, NBFGR, Lucknow for his support for execution of this work. Excellent technical co-operation from Mr. Rajesh Kumar and Mr. Sree Ram is duly acknowledged.

Author information

Authors and Affiliations

  1. National Bureau of Fish Genetic Resources (ICAR), Canal Ring Road, P.O. Dilkusha, Lucknow, 226 002, Uttar Pradesh, India

    Prachi Masih, Rupesh K. Luhariya, Rakhi Das, Arti Gupta, Vindhya Mohindra, Rajeev K. Singh, Rohit Srivastava, J. K. Jena & Kuldeep K. Lal

  2. School of Environmental Sciences, Awadhesh Pratap Singh University, Rewa, 486 003, Madhya Pradesh, India

    U. K. Chauhan

Authors
  1. Prachi Masih
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rupesh K. Luhariya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rakhi Das
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arti Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vindhya Mohindra
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rajeev K. Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rohit Srivastava
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. U. K. Chauhan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. J. K. Jena
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Kuldeep K. Lal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kuldeep K. Lal.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 232 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Masih, P., Luhariya, R.K., Das, R. et al. Cross-priming of microsatellite loci in subfamily cyprininae (family Cyprinidae): their utility in finding markers for population genetic analysis in three Indian major carps. Mol Biol Rep 41, 5187–5197 (2014). https://doi.org/10.1007/s11033-014-3386-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-014-3386-0

Keywords

Search

Navigation