Skip to main content
SpringerLink
Log in

A genetic linkage map and comparative genome analysis of common carp (Cyprinus carpio L.) using microsatellites and SNPs

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

A genetic linkage map is a powerful research tool for mapping traits of interest and is essential to understanding genome evolution. The aim of this study is to provide an expanded genetic linkage map of common carp to effectively carry out quantitative trait loci analysis and conduct comparative mapping analysis between lineages. Here, we constructed a genetic linkage map of common carp (Cyprinus carpio L.) using microsatellite and single-nucleotide polymorphism (SNP) markers in a 159 sibling family. A total of 246 microsatellites and 306 SNP polymorphic markers were genotyped in this family. Linkage analysis using JoinMap 4.0 organized 427 markers (186 microsatellites and 241 SNPs) to 50 linkage groups, ranging in size from 1.4 to 130.1 cM. Each group contained 2–30 markers. The linkage map covered a genetic distance of 2,039.2 cM and the average interval for markers within the linkage groups was approximately 6.4 cM. In addition, comparative genome analysis within five model teleost fish revealed a high percentage (74.7%) of conserved loci corresponding to zebrafish chromosomes. In most cases, each zebrafish chromosome comprised two common carp linkage groups. The comparative analysis also revealed independent chromosome rearrangements in common carp and zebrafish. The linkage map will be of great assistance in mapping genes of interest and serve as a reference to approach comparative mapping and enable further insights into the comprehensive investigations of genome evolution of common carp.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aliah RS, Takagi M, Dong S, Taniguchi N (1999) Isolation and inheritance of microsatellite markers in the common carp Cyprinus carpio. Fish Sci 65:235–239

    CAS  Google Scholar 

  • Ball AD, Stapley J, Dawson DA, Birkhead TR, Burke T, Slate J (2010) A comparison of SNPs and microsatellites as linkage mapping markers: lessons from the zebra finch (Taeniopygia guttata). BMC Genomics 11:218

    Article  PubMed  Google Scholar 

  • Balon EK (1995) Origin and domestication of the wild carp, Cyprinus carpio: from Roman gourmets to the swimming flowers. Aquaculture 129:3–48

    Article  Google Scholar 

  • Bourque G, Pevzner PA, Tesler G (2004) Reconstructing the genomic architecture of ancestral mammals: lessons from human, mouse, and rat genomes. Genome Res 14:507–516

    Article  PubMed  CAS  Google Scholar 

  • Bouza C, Hermida M, Pardo BG, Fernandez C, Fortes GG, Castro J, Sanchez L, Presa P, Perez M, Sanjuan A (2007) A microsatellite genetic map of the turbot (Scophthalmus maximus). Genetics 177:2457–2467

    Article  PubMed  CAS  Google Scholar 

  • Castaño-Sánchez C, Fuji K, Ozaki A, Hasegawa O, Sakamoto T, Morishima K, Nakayama I, Fujiwara A, Masaoka T, Okamoto N (2010) A second generation genetic linkage map of Japanese flounder (Paralichthys olivaceus). BMC Genomics 11:554

    Article  PubMed  Google Scholar 

  • Chakravarti A, Lasher LK, Reefer JE (1991) A maximum likelihood method for estimating genome length using genetic linkage data. Genetics 128:175–182

    PubMed  CAS  Google Scholar 

  • Cheng L, Liu L, Yu X, Wang D, Tong J (2009) A linkage map of common carp (Cyprinus carpio) based on AFLP and microsatellite markers. Anim Genet 41:191–198

    Article  PubMed  Google Scholar 

  • Chistiakov D, Hellemans B, Haley C, Law A, Tsigenopoulos C, Kotoulas G, Bertotto D, Libertini A, Volckaert F (2005) A microsatellite linkage map of the European sea bass Dicentrarchus labrax L. Genetics 170:1821–1826

    Article  PubMed  CAS  Google Scholar 

  • Chistiakov D, Tsigenopoulos C, Lagnel J, Guo YM, Hellemans B, Haley C, Volckaert F, Kotoulas G (2008) A combined AFLP and microsatellite linkage map and pilot comparative genomic analysis of European sea bass Dicentrarchus labrax L. Anim Genet 39:623–634

    Article  PubMed  CAS  Google Scholar 

  • Christoffels A, Bartfai R, Srinivasan H, Komen H, Orban L (2006) Comparative genomics in cyprinids: common carp ESTs help the annotation of the zebrafish genome. BMC Bioinform 7(Suppl 5):S2

    Article  Google Scholar 

  • Cnaani A, Zilberman N, Tinman S, Hulata G, Ron M (2004) Genome-scan analysis for quantitative trait loci in an F 2 tilapia hybrid. Mol Genet Genomics 272:162–172

    Article  PubMed  CAS  Google Scholar 

  • Comber SC, Smith C (2004) Polyploidy in fishes: patterns and processes. Biol J Linn Soc 82:431–442

    Article  Google Scholar 

  • Crooijmans R, Poel JJ, Groenen MAM, Bierbooms VAF, Komen J (1997) Microsatellite markers in common carp (Cyprinus carpio L.). Anim Genet 28:129–134

    Article  CAS  Google Scholar 

  • David L, Rajasekaran P, Fang J, Hillel J, Lavi U (2001) Polymorphism in ornamental and common carp strains (Cyprinus carpio L.) as revealed by AFLP analysis and a new set of microsatellite markers. Mol Genet Genomics 266:353–362

    Article  PubMed  CAS  Google Scholar 

  • Eichler EE, Sankoff D (2003) Structural dynamics of eukaryotic chromosome evolution. Science 301:793–797

    Article  PubMed  CAS  Google Scholar 

  • Elena S, Rafaella F, Bruno L, Luca B, Antonios M, Fabrice S, Matina T, Tomaso P, Francis G, Georgios K (2007) A gene-based radiation hybrid map of the gilthead sea bream Sparus aurata refines and exploits conserved synteny with Tetraodon nigroviridis. BMC Genomics 8:44

    Article  Google Scholar 

  • Ellwood SR, Phan HTT, Jordan M, Hane J, Torres AM, Avila CM, Cruz-Izquierdo S, Oliver RP (2008) Construction of a comparative genetic map in faba bean(Vicia faba L.) conservation of genome structure with Lens culinaris. BMC Genomics 9:380

    Google Scholar 

  • Evans DM, Cardon LR (2004) Guidelines for genotyping in genomewide linkage studies: single-nucleotide-polymorphism maps versus microsatellite maps. Am J Hum Genet 75:687–692

    Article  PubMed  CAS  Google Scholar 

  • Fan J, Gunderson KL, Bibikova M, Yeakley JM, Chen J, Wickham Garcia E, Lebruska LL, Laurent M, Shen R, Barker D (2006) Illumina Universal Bead Arrays. In: Alan K, Brian O (eds) Methods in enzymology. Academic Press, New York, pp 57–73

  • Ferris SD, Whitt GS (1977) The evolution of duplicate gene expression in the carp (Cyprinus carpio). Cell Mol Life Sci 33:1299–1301

    Article  CAS  Google Scholar 

  • Fishman L, Kelly AJ, Morgan E, Willis JH (2001) A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics 159:1701–1716

    PubMed  CAS  Google Scholar 

  • Friedman R, Hughes AL (2001) Pattern and timing of gene duplication in animal genomes. Genome Res 11:1842–1847

    Article  PubMed  CAS  Google Scholar 

  • Gebhardt C, Walkemeier B, Henselewski H, Barakat A, Delseny M, Stüber K (2003) Comparative mapping between potato (Solanum tuberosum) and Arabidopsis thaliana reveals structurally conserved domains and ancient duplications in the potato genome. Plant J 34:529–541

    Article  PubMed  CAS  Google Scholar 

  • Gilbey J, Verspoor E, McLay A, Houlihan D (2004) A microsatellite linkage map for Atlantic salmon (Salmo salar). Anim Genet 35:98–105

    Article  PubMed  CAS  Google Scholar 

  • Guryev V, Koudijs MJ, Berezikov E, Johnson SL, Plasterk RHA, van Eeden FJM, Cuppen E (2006) Genetic variation in the zebrafish. Genome Res 16:491–497

    Article  PubMed  CAS  Google Scholar 

  • Hou N, Li DY, Li Y, Lu CY, Sun XW, Liang LQ (2008) Development of 10 tri- and tetranucleotide microsatellite loci for population studies in the common carp (Cyprinus carpio L.). Mol Ecol Resour 8:1357–1359

    Article  PubMed  CAS  Google Scholar 

  • Hubert S, Hedgecock D (2004) Linkage maps of microsatellite DNA markers for the Pacific oyster Crassostrea gigas. Genetics 168:351–362

    Article  PubMed  CAS  Google Scholar 

  • Hulata G (1995) A review of genetic improvement of the common carp (cyprinus carpio L.) and other cyprinids by crossbreeding, hybridization and selection. Aquaculture 129:143–155

    Article  Google Scholar 

  • Kalo P, Seres A, Taylor S, Jakab J, Kevei Z, Kereszt A, Endre G, Ellis THN, Kiss G (2004) Comparative mapping between Medicago sativa and Pisum sativum. Mol Genet Genomics 272:235–246

    Article  PubMed  CAS  Google Scholar 

  • Kocher TD, Lee WJ, Sobolewska H, Penman D, McAndrew B (1998) A genetic linkage map of a cichlid fish, the tilapia (Oreochromis niloticus). Genetics 148:1225–1232

    PubMed  CAS  Google Scholar 

  • Kosambi D (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Article  Google Scholar 

  • Kucuktas H, Wang S, Li P, He C, Xu P, Sha Z, Liu H, Jiang Y, Baoprasertkul P, Somridhivej B (2009) Construction of genetic linkage maps and comparative genome analysis of catfish using gene-associated markers. Genetics 181:1649–1660

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    PubMed  CAS  Google Scholar 

  • Larhammar D, Risinger C (1994) Molecular genetic aspects of tetraploidy in the common carp Cyprinus carpio. Mol Phylogenet Evol 3:59–68

    Article  PubMed  CAS  Google Scholar 

  • Lee BY, Lee WJ, Streelman JT, Carleton KL, Howe AE, Hulata G, Slettan A, Stern JE, Terai Y, Kocher TD (2005) A second generation genetic linkage map of tilapia (Oreochromis spp.). Genetics 170:237–244

    Article  PubMed  CAS  Google Scholar 

  • Li Y, He W, Ding L, Li Y, Liang LQ, Lei QQ (2009) Construction and identification of cDNA library from common carp(Cyprinus carpio Linnaeus) brain. J Fish Sci China 16:147–155

    CAS  Google Scholar 

  • Li Y, Xu P, Zhao ZX, Wang J, Zhang Y, Sun XW (2010) Construction and characterization of the BAC library for common carp Cyprinus Carpio L. and establishment of microsynteny with Zebrafish Danio Rerio. Mar Biotechnol 13:706–712

    Article  PubMed  Google Scholar 

  • Lincoln SE, Lander ES (1992) Systematic detection of errors in genetic linkage data. Genomics 14:604–610

    Article  PubMed  CAS  Google Scholar 

  • Liu Z, Karsi A, Li P, Cao D, Dunham R (2003) An AFLP-based genetic linkage map of channel catfish (Ictalurus punctatus) constructed by using an interspecific hybrid resource family. Genetics 165:687–694

    PubMed  CAS  Google Scholar 

  • Lu CY, Mao RX, Li O, Geng LW, Sun XW, Liang LQ (2009) Characterization of Polymorphic tri-and tetranucleotide repeat microsatellite loci in common carp (Cyprinus carpio). J Agric Biotechnol 17:979–987

    CAS  Google Scholar 

  • Maliepaard C, Jansen J, Van Ooijen J (1997) Linkage analysis in a full-sib family of an outbreeding plant species: overview and consequences for applications. Genet Res 70:237–250

    Article  Google Scholar 

  • Moen T, Hoyheim B, Munck H, Gomez‐Raya L (2004) A linkage map of Atlantic salmon (Salmo salar) reveals an uncommonly large difference in recombination rate between the sexes. Anim Genet 35:81–92

    Article  PubMed  CAS  Google Scholar 

  • Moen T, Hayes B, Baranski M, Berg P, Kjglum S, Koop B, Davidson W, Omholt S, Lien S (2008) A linkage map of the Atlantic salmon (Salmo salar) based on EST-derived SNP markers. BMC Genomics 9:223

    Article  PubMed  Google Scholar 

  • Nakamura K, Ozaki A, Akutsu T, Iwai K, Sakamoto T, Yoshizaki G, Okamoto N (2001) Genetic mapping of the dominant albino locus in rainbow trout (Oncorhynchus mykiss). Mol Genet Genomics 265:687–693

    Article  PubMed  CAS  Google Scholar 

  • Naruse K, Tanaka M, Mita K, Shima A, Postlethwait J, Mitani H (2004) A medaka gene map: the trace of ancestral vertebrate proto-chromosomes revealed by comparative gene mapping. Genome Res 14:820–828

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273

    Article  PubMed  CAS  Google Scholar 

  • Ohno S, Muramoto J, Christian L, Atkin NB (1967) Diploid-tetraploid relationship among old-world members of the fish family Cyprinidae. Chromosoma 23:1–9

    Article  Google Scholar 

  • Phillips RB, Amores A, Morasch MR, Wilson C, Postlethwait JH (2006) Assignment of zebrafish genetic linkage groups to chromosomes. Cytogenet Genome Res 114:155–162

    Article  PubMed  CAS  Google Scholar 

  • Rexroad C, Rodriguez M, Coulibaly I, Gharbi K, Danzmann R, DeKoning J, Phillips R, Palti Y (2005) Comparative mapping of expressed sequence tags containing microsatellites in rainbow trout (Oncorhynchus mykiss). BMC Genomics 6:54

    Article  PubMed  Google Scholar 

  • Rexroad CE, Palti Y, Gahr SA, Vallejo RL (2008) A second generation genetic map for rainbow trout (Oncorhynchus mykiss). BMC Genetics 9:74

    Article  PubMed  Google Scholar 

  • Richards S, Liu Y, Bettencourt BR, Hradecky P, Letovsky S, Nielsen R, Thornton K, Hubisz MJ, Chen R, Meisel RP (2005) Comparative genome sequencing of Drosophila pseudoobscura: chromosomal, gene, and cis-element evolution. Genome Res 15:1–18

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sankoff D (2003) Rearrangements and chromosomal evolution. Curr Opin Genet Dev 13:583–587

    Article  PubMed  CAS  Google Scholar 

  • Sarropoulou E, Nousdili D, Magoulas A, Kotoulas G (2008) Linking the genomes of nonmodel teleosts through comparative genomics. Mar Biotechnol 10:227–233

    Article  PubMed  CAS  Google Scholar 

  • Soltis DE, Soltis PS (1999) Polyploidy: recurrent formation and genome evolution. Trends Ecol Evol 14:348–352

    Article  PubMed  Google Scholar 

  • Steinke D, Salzburger W, Meyer A (2006) Novel relationships among ten fish model species revealed based on a phylogenomic analysis using ESTs. J Mol Evol 62:772–784

    Article  PubMed  CAS  Google Scholar 

  • Sun XW, Liang LQ (2004) A genetic linkage map of common carp (Cyprinus carpio L.) and mapping of a locus associated with cold tolerance. Aquaculture 238:165–172

    Article  CAS  Google Scholar 

  • Sun XW, Jia ZY, Wei DW, Lu CY, Liang LQ (2005) Comparison between magnetic beads enriched and small inserted fragment library. J Fish Sci China 12:126–132

    CAS  Google Scholar 

  • Tanck MWT, Palstra AP, Weerd M, Leffering CP, Poel JJ, Bovenhuis H, Komen J (2001) Segregation of microsatellite alleles and residual heterozygosity at single loci in homozygous androgenetic common carp (Cyprinus carpio L.). Genome 44:743–751

    PubMed  CAS  Google Scholar 

  • Tang J, Vosman B, Voorrips RE, Van Der Linden CG, Leunissen JAM (2006) QualitySNP: a pipeline for detecting single nucleotide polymorphisms and insertions/deletions in EST data from diploid and polyploid species. BMC Bioinform 7:438

    Article  Google Scholar 

  • Taylor JS, Van de Peer Y, Braasch I, Meyer A (2001) Comparative genomics provides evidence for an ancient genome duplication event in fish. Philos Trans R Soc B 356:1661–1679

    Article  CAS  Google Scholar 

  • Van Ooijen J (2006) JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations. In: Kyazma BV (ed) Wageningen, Netherlands

  • 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 34:275–306

    Article  PubMed  CAS  Google Scholar 

  • Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

  • Wang DG, Fan JB, Siao CJ, Berno A, Young P, Sapolsky R, Ghandour G, Perkins N, Winchester E, Spencer J (1998) Large-scale identification, mapping, and genotyping of single-nucleotide polymorphisms in the human genome. Science 280:1077–1082

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Liao XN, Cheng L, Yu XM, Tong J (2007) Development of novel EST-SSR markers in common carp by data mining from public EST sequences. Aquaculture 271:558–574

    Article  CAS  Google Scholar 

  • Wang CM, Bai ZY, He XP, Lin G, Xia JH, Sun F, Lo LC, Feng F, Zhu ZY, Yue GH (2011) A high-resolution linkage map for comparative genome analysis and QTL fine mapping in Asian seabass, Lates calcarifer. BMC Genomics 12:174

    Article  PubMed  CAS  Google Scholar 

  • Wei DW, Lou YD, Sun XW, Shen JB (2001) Isolation of microsatellite markers in the common carp (Cyprinus carpio). Zool Res 22:238–241

    CAS  Google Scholar 

  • Wohlfarth G (1984) Common carp. In: Mason L (ed) Evolution of domesticated animals. Longman, Harlow, pp 375–380

    Google Scholar 

  • Wolfe KH (2001) Yesterday’s polyploids and the mystery of diploidization. Nat Rev Genet 2:333–341

    Article  PubMed  CAS  Google Scholar 

  • Woods IG, Wilson C, Friedlander B, Chang P, Reyes DK, Nix R, Kelly PD, Chu F, Postlethwait JH, Talbot WS (2005) The zebrafish gene map defines ancestral vertebrate chromosomes. Genome Res 15:1307–1314

    Article  PubMed  CAS  Google Scholar 

  • Xia JH, Liu F, Zhu ZY, Fu JJ, Feng JB, Li JL, Yue GH (2010) A consensus linkage map of the grass carp(Ctenopharyngodon idella) based on microsatellites and SNPs. BMC Genomics 11:135

    Article  PubMed  Google Scholar 

  • Xu P, Li J, Li Y, Cui R, Wang J, Zhang Y, Zhao Z, Sun X (2011) Genomic insight into the common carp (Cyprinus carpio) genome by sequencing analysis of BAC-end sequences. BMC Genomics 12:188

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Zhang X, Yang J, Sun X (2009) Exploitation of SNPs related to growth traits of common carp (Cyprinus crpio L.) based on EST sequences. Chinese J Fish 22:1–7

    Google Scholar 

  • Zhang Y, Xu P, Lu C, Kuang Y, Zhang X, Cao D, Li C, Chang Y, Hou N, Li H (2010) Genetic linkage mapping and analysis of muscle fiber-related QTLs in common carp (Cyprinus carpio L.). Mar Biotechnol 13:376–392

    Article  PubMed  Google Scholar 

  • Zimdahl H, Nyakatura G, Brandt P, Schulz H, Hummel O, Fartmann B, Brett D, Droege M, Monti J, Lee Y (2004) A SNP map of the rat genome generated from cDNA sequences. Science 303:807

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Dr Yi Zhou (Harvard Medical School, USA) for English editing and comments on a previous version of the manuscript. They also thank Xuanpeng Wang, Wensheng Li and Weihua Lv for experimental assistance. This study was supported by the National Program on Key Basic Research Project of China (No. 2010CB126305), the Special Fund for Agro-scientific Research in the Public Interest (No. 200903045) and the Central-Level Non-profit Scientific Research Institutes Special Funds (No. 201006).

Author information

Authors and Affiliations

  1. Heilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, No. 43 Songfa Road, Daoli District, Harbin, 150070, Heilongjiang, China

    Xianhu Zheng, Youyi Kuang, Xiaofeng Zhang, Cuiyun Lu, Dingchen Cao, Chao Li & Xiaowen Sun

  2. College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, 201306, China

    Xianhu Zheng

Authors
  1. Xianhu Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Youyi Kuang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaofeng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cuiyun Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dingchen Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaowen Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiaowen Sun.

Additional information

Communicated by J. Cerdá.

Xianhu Zheng and Youyi Kuang contributed equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zheng, X., Kuang, Y., Zhang, X. et al. A genetic linkage map and comparative genome analysis of common carp (Cyprinus carpio L.) using microsatellites and SNPs. Mol Genet Genomics 286, 261 (2011). https://doi.org/10.1007/s00438-011-0644-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00438-011-0644-x

Keywords

Search

Navigation