Abstract
Common carp (Cyprinus carpio L.) is cultured worldwide and is a major contributor to the world’s aquaculture production. The common carp has a complex tetraploidized genome, which may historically experience additional whole genome duplication than most other Cyprinids. Fine maps for female and male carp were constructed using a mapping panel containing one F1 family with 190 progeny. A total of 1,025 polymorphic markers were used to construct genetic maps. For the female map, 559 microsatellite markers in 50 linkage groups cover 3,468 cM of the genome. For the male map, 383 markers in 49 linkage groups cover 1,811 cM of the genome. The consensus map was constructed by integrating the new map with two published linkage maps, containing 732 markers and spanning 3,278 cM in 50 linkage groups. The number of consensus linkage groups corresponds to the number of common carp chromosomes. A significant difference on sex recombinant rate was observed that the ratio of female and male recombination rates was 4.2:1. Comparative analysis was performed between linkage map of common carp and genome of zebrafish (Danio rerio), which revealed clear 2:1 relationship of common carp linkage groups and zebrafish chromosomes. The results provided evidence that common carp did experienced a specific whole genome duplication event comparing with most other Cyprinids. The consensus linkage map provides an important tool for genetic and genome study of common carp and facilitates genetic selection and breeding for common carp industry.
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References
Cheng L, Liu L, Yu X, Wang D, Tong J (2010) A linkage map of common carp (Cyprinus carpio) based on AFLP and microsatellite markers. Anim Genet 41:191–198
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 Bioinforma 7:S2
Crooijmans R, Poel J, Groenen M, Bierbooms V, Komen J (1997) Microsatellite markers in common carp (Cyprinus carpio L.). Anim Genet 28:129–134
Danzmann RG, Davidson EA, Ferguson MM, Gharbi K, Koop BF, Hoyheim B, Lien S, Lubieniecki KP, Moghadam HK, Park J, Phillips RB, Davidson WS (2008) Distribution of ancestral proto-Actinopterygian chromosome arms within the genomes of 4R-derivative salmonid fishes (Rainbow trout and Atlantic salmon). BMC genomics 9:557
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
David L, Blum S, Feldman MW, Lavi U, Hillel J (2003) Recent duplication of the common carp (Cyprinus carpio L.) genome as revealed by analyses of microsatellite loci. Mol Biol Evol 20:1425–1434
Hale MC, Xu P, Scardina J, Wheeler PA, Thorgaard GH, Nichols KM (2011) Differential gene expression in male and female rainbow trout embryos prior to the onset of gross morphological differentiation of the gonads. BMC Genomics 12:404
Hyten DL, Choi IY, Song Q, Specht JE, Carter TE Jr, Shoemaker RC, Hwang EY, Matukumalli LK, Cregan PB (2010) A high density integrated genetic linkage map of soybean and the development of a 1536 universal soy linkage panel for quantitative trait locus mapping. Crop Sci 50:960–969
Ji P, Liu G, Xu J, Wang X, Li J, Zhao Z, Zhang X, Zhang Y, Xu P, Sun X (2012) Characterization of common carp transcriptome: sequencing, de novo assembly, annotation and comparative genomics. PLoS One 7:e35152
Kohlmann K, Gross R, Murakaeva A, Kersten P (2003) Genetic variability and structure of common carp (Cyprinus carpio) populations throughout the distribution range inferred from allozyme, microsatellite and mitochondrial DNA markers. Aquat Living Resour 16:421–431
Kucuktas H, Wang S, Li P, He C, Xu P, Sha Z, Liu H, Jiang Y, Baoprasertkul P, Somridhivej B, Wang Y, Abernathy J, Guo X, Liu L, Muir W, Liu Z (2009) Construction of genetic linkage maps and comparative genome analysis of catfish using gene-associated markers. Genetics 181:1649–1660
Li Y, Xu P, Zhao Z, Wang J, Zhang Y, Sun XW (2011) Construction and characterization of the BAC library for common carp Cyprinus carpio L. and establishment of microsynteny with zebrafish Danio rerio. Mar Biotechnol (NY) 13:706–712
Li H, Liu X, Zhang G (2012) Development and linkage analysis of 104 new microsatellite markers for bay scallop (Argopecten irradians). Mar Biotechnol (NY) 14:1–9
Lien S, Gidskehaug L, Moen T, Hayes BJ, Berg PR, Davidson WS, Omholt SW, Kent MP (2011) A dense SNP-based linkage map for Atlantic salmon (Salmo salar) reveals extended chromosome homeologies and striking differences in sex-specific recombination patterns. BMC genomics 12:615
Liu H, Jiang Y, Wang S, Ninwichian P, Somridhivej B, Xu P, Abernathy J, Kucuktas H, Liu Z (2009a) Comparative analysis of catfish BAC end sequences with the zebrafish genome. BMC Genomics 10:592
Liu JH, Zhang Y, Chang YM, Liang LQ, Lu CY, Zhang XF, Xu MJ, Sun XW (2009b) Mapping QTLs related to head length, eye diameter and eye cross of common carp (Cyprinus carpio L.). Yi Chuan 31:508–514
Liu S, Rexroad CE 3rd, Couch CR, Cordes JF, Reece KS, Sullivan CVA (2011) Microsatellite linkage map of striped bass (Morone saxatilis) reveals conserved synteny with the three-spined stickleback (Gasterosteus aculeatus). Mar Biotechnol (NY) 14:237–244
Lu J, Peatman E, Yang Q, Wang S, Hu Z, Reecy J, Kucuktas H, Liu Z (2011) The catfish genome database cBARBEL: an informatic platform for genome biology of ictalurid catfish. Nucleic Acids Res 39:D815–D821
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
Moen T, Hayes B, Baranski M, Berg PR, Kjøglum S, Koop BF, Davidson WS, Omholt SW, Lien S (2008) A linkage map of the Atlantic salmon (Salmo salar) based on EST-derived SNP markers. BMC Genomics 9:223
Neilan BA, Wilton AN, Jacobs D (1997) A universal procedure for primer labelling of amplicons. Nucleic Acids Res 25:2938–2939
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386
Sakamoto T, Danzmann RG, Gharbi K, Howard P, Ozaki A, Khoo SK, Woram RA, Okamoto N, Ferguson MM, Holm LE, Guyomard R, Hoyheim B (2000) A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 155:1331–1345
Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234
Spiller M, Linde M, Hibrand-Saint Oyant L, Tsai CJ, Byrne DH, Smulders MJ, Foucher F, Debener T (2011) Towards a unified genetic map for diploid roses. Theor Appl Genet 122:489–500
Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: join map. Plant J 3:739–744
Sun X, Liang L (2004) A genetic linkage map of common carp (Cyprinus carpio L.) and mapping of a locus associated with cold tolerance. Aquaculture 238:165–172
Van De Peer Y, Maere S, Meyer A (2009) The evolutionary significance of ancient genome duplications. Nat Rev Genet 10:725–732
Van Ooijen J (2006) JoinMap 4. Software for the calculation of genetic linkage maps in experimental populations. Plant Research International, Wageningen
Vezzulli S, Troggio M, Coppola G, Jermakow A, Cartwright D, Zharkikh A, Stefanini M, Grando MS, Viola R, Adam-Blondon AF, Thomas M, This P, Velasco R (2008) A reference integrated map for cultivated grapevine (Vitis vinifera L.) from three crosses, based on 283 SSR and 501 SNP-based markers. Theor Appl Genet 117:499–511
Wan Y, Zhang Y, Ji P, Li Y, Xu P, Sun X (2012) Molecular characterization of CART, AgRP, and MC4R genes and their expression with fasting and re-feeding in common carp (Cyprinus carpio L.). Mol Biol Rep 39:2215–2223
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
Wang X, Zhang X, Li W, Zhang T, Li C, Sun X (2012) Mapping and genetic effect analysis on quantitative trait loci related to feed conversion ratio of common carp(Cyprinus carpio L.). Acta Hydrobiol Sinica 36:177–196
Xu P, Li J, Li Y, Cui R, Wang J, Wang J, Zhang Y, Zhao Z, Sun X (2011a) Genomic insight into the common carp (Cyprinus carpio) genome by sequencing analysis of BAC-end sequences. BMC Genomics 12:188
Xu P, McIntyre LM, Scardina J, Wheeler PA, Thorgaard GH, Nichols KM (2011b) Transcriptome profiling of embryonic development rate in rainbow trout advanced backcross introgression lines. Mar Biotechnol (NY) 13:215–231
Xu P, Wang J, Wang J, Cui R, Li Y, Zhao Z, Ji P, Zhang Y, Li J, Sun X (2011c) Generation of the first BAC-based physical map of the common carp genome. BMC Genomics 12:537
Zhan X, Fan F, You W, Yu J, Ke C (2012) Construction of an integrated map of Haliotis diversicolor using microsatellite markers. Mar Biotechnol (NY) 14:79–86
Zhang Y, Liang LQ, Chang YM, Hou N, Lu CY, Sun XW (2007) Mapping and genetic effect analysis of quantitative trait loci related to body size in common carp (Cyprinus carpio L.). Yi Chuan 29:1243–1248
Zhang Y, Liang L, Jiang P, Li D, Lu C, Sun X (2008a) Genome evolution trend of common carp (Cyprinus carpio L.) as revealed by the analysis of microsatellite loci in a gynogentic family. J Genet Genomics 35:97–103
Zhang YF, Zhang Y, Lu CY, Cao DC, Sun XW (2008b) Correlation analysis of microsatellite DNA markers with body weight, length and height of common carp (Cyprinus carpio L.). Yi Chuan 30:613–619
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 (NY) 13:376–392
Zheng X, Kuang Y, Zhang X, Lu C, Cao D, Li C, Sun X (2011) A genetic linkage map and comparative genome analysis of common carp (Cyprinus carpio L.) using microsatellites and SNPs. Mol Genet Genomics 286:261–277
Acknowledgments
The authors would like to thank Yu Chang, Tingting Sun, Yulan Xu, Sen Yin, Wei Liu, Binbin Yu, Baoyong Zhang, Zhiwu Jia, Xuanpeng Wang, Wensheng Li, Tianqi Zhang, Zhu Cao, Cui Liu, Zhiyuan Chu, Zhaojun Tan, Weihua Lv, and Qian Yu. This study was supported by the Key Project of Chinese National Programs for Fundamental Research and Development (2010CB126305), the National Department Public Benefit Research Foundation of China (200903045), the National High-tech R&D Program of China (2011AA100401), and the Introduction of Advanced Agricultural Science and Technology Key Project (“948” Project: 2011-G12).
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X. Zhang and Y. Zhang contributed equally.
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Zhang, X., Zhang, Y., Zheng, X. et al. A Consensus Linkage Map Provides Insights on Genome Character and Evolution in Common Carp (Cyprinus carpio L.). Mar Biotechnol 15, 275–312 (2013). https://doi.org/10.1007/s10126-012-9485-9
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DOI: https://doi.org/10.1007/s10126-012-9485-9