Skip to main content
Log in

Genetic Mapping and QTL Analysis of Growth Traits in the Large Yellow Croaker Larimichthys crocea

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Large yellow croaker (Larimichthys crocea) is an important maricultured species in China. A genetic linkage map of the large yellow croaker was constructed using type II microsatellites and expressed sequence tag (EST)-derived microsatellites in two half-sib families (two females and one male). A total of 289 microsatellite markers (contained 93 EST-SSRs) were integrated into 24 linkage groups, which agreed with the haploid chromosome number. The map spanned a length of 1,430.8 cm with an average interval of 5.4 cm, covering 83.9 % of the estimated genome size (1,704.8 cm). A total of seven quantitative trait locis (QTLs) were detected for growth traits on five linkage groups, including two 1 % and five 5 % chromosome-wide significant QTLs, and explained from 2.33 to 5.31 % of the trait variation. The identified QTLs can be applied in marker-assisted selection programs to improve the growth traits.

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

Similar content being viewed by others

References

  • An HS, Cho KC, Park JY (2005) Eleven new highly polymorphic microsatellite loci in the yellow croaker, Pseudosciaena crocea. Mol Ecol Notes 5:866–868

    Article  CAS  Google Scholar 

  • Andersson L, Georges M (2004) Domestic-animal genomics: deciphering the genetics of complex traits. Nat Rev Genet 5:202–212

    Article  CAS  PubMed  Google Scholar 

  • Baranski M, Rourke M, Loughnan S, Hayes B, Austin C, Robinson N (2008) Detection of QTL for growth rate in the blacklip abalone (Haliotis rubra Leach) using selective DNA pooling. Anim Genet 39:606–614

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  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 Central  CAS  PubMed  Google Scholar 

  • Chang YM, Ding L, Wang WW, He JG, Ling LQ, Lei QQ (2009) Isolation and characterization of 11 microsatellite markers for the large yellow croaker, Pseudosciaena crocea. Conserv Genet 10:1405–1408

    Article  CAS  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cnaani A, Hallerman EM, Ron M, Weller JI, Indelman M, Kashi Y, Gall GA, Hulata G (2003) Detection of a chromosomal region with two quantitative trait loci, affecting cold tolerance and fish size, in an F-2 tilapia hybrid. Aquaculture 223:117–128

    Article  CAS  Google Scholar 

  • Coimbra MR, Kobayashi K, Koretsugu S, Koretsugu S, Hasegawa O, Oharaa E, Ozakia A, Sakamotoa T, Narusec K, Okamoto N (2003) A genetic linkage map of the Japanese flounder, Paralichtys olivaceus. Aquaculture 220:203–218

    Article  CAS  Google Scholar 

  • Dekkers JCM, Hospital F (2002) Multifactoral genetics: the use of molecular genetics in the improvement of agricultural populations. Nat Rev Genet 3:22–32

    Article  CAS  PubMed  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Addison Wesley Longman, Harlow

    Google Scholar 

  • Faris JD, Laddomada B, Gill BS (1998) Molecular mapping of segregation distortion loci in Aegilops taushii. Genetics 149:319–327

    PubMed Central  CAS  PubMed  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 Central  CAS  PubMed  Google Scholar 

  • Fuji K, Kobayashi K, Hasegawa O, Coimbra M, Sakamoto T, Okamoto N (2006) Identification of a single major genetic locus controlling the resistance to lymphocystis disease in Japanese flounder (Paralichthys olivaceus). Aquaculture 254:203–210

    Article  CAS  Google Scholar 

  • Gates MA, Kim L, Egan ES, Cardozo T, Sirotkin HI, Dougan ST, Lashkari D, Abagyan R, Schier AF, Talbot WS (1999) A genetic linkage map for zebrafish: comparative analysis and localization of genes and expressed sequences. Genome Res 9:334–347

    CAS  PubMed  Google Scholar 

  • Gonen S, Lowe NR, Cezard T, Gharbi K, Bishop SC, Houston RD (2014) Linkage maps of the Atlantic salmon (Salmo salar) genome derived from RAD sequencing. BMC Genomics 15:166

    Article  PubMed Central  PubMed  Google Scholar 

  • Grandillo S, Tanksley SD (1996) Genetic analysis of RFLPs, GATA microsatellites and RAPDs in a cross between L. esculentum and L. pimpinellifolium. Theor Appl Genet 92:957–965

    Article  CAS  PubMed  Google Scholar 

  • Green P, Falls K, Crooks S (1990) Documentation for CRI-MAP version 2.4. Washington University School of Medicine. Saint Louis

  • Guo W, Wang ZY, Wang YL, Zhang ZP, Gui JF (2005) Isolation and characterization of six microsatellite markers in the large yellow croaker (Pseudosciaena crocea Richardson). Mol Ecol Notes 5(2):369–371

    Article  CAS  Google Scholar 

  • Guyomard R, Mauger S, Tabet-Canale K, Martineau S, Genet C (2006) A type I and type II microsatellite linkage map of Rainbow trout (Oncorhynchus mykiss) with presumptive coverage of all chromosome arms. BMC Genomics 7:302–315

    Article  PubMed Central  PubMed  Google Scholar 

  • Guyomard R, Mauger S, Martineau S, Tabet-Canale K, Quillet E (2007) Construction of a female microsatellite linkage map in rainbow trout (Oncorhynchus mykiss), a tetraploid species. Aquaculture 272:S264–S264

    Article  Google Scholar 

  • Guyomard R, Boussaha M, Krieg F, Hervet C, Quillet E (2012) A synthetic rainbow trout linkage map provides new insights into the salmonid whole genome duplication and the conservation of synteny among teleosts. BMC Genet 13:15

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hao J, Sun X, Liang L, Lu C (2006) Enrichment of large yellow croaker genome microsatellite markers using magnet beads. J Fish Sci China 13(5):762–766 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Hyne V, Kearsey MJ, Pike DJ, Snape JW (1995) QTL analysis: unreliability and bias in estimation procedures. Mol Breed 1:273–282

    Article  Google Scholar 

  • Kang JH, Kim WJ, Lee WJ (2008) Genetic linkage map of olive flounder, Paralichthys olivaceus. Int J Biol Sci 4(3):143–149

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Katagiri T, Kidd C, Tomasinoe E, Davis JT, Wishon C, Stern JE, Carleton KL, Howe AE, Kocher TD (2005) A BAC-based physical map of the Nile tilapia genome. BMC Genomics 6:89

    Article  PubMed Central  PubMed  Google Scholar 

  • Kelly PD, Chu F, Woods LG, Ngo-Hazelett P, Cardozo T, Huang H, Kimm F, Liao L, Yan YL, Zhou Y, Johnson SL, Abagyan R, Schier AF, Postlethwait JH, Talbot WS (2000) Genetic linkage mapping of zebrafish genes and ESTs. Genome Res 10:558–567

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kimura T, Yoshida K, Shimada A, Jindo T, Sakaizumi M, Mitani H, Naruse K, Takeda H, Inoko H, Tamiya G, Shinya M (2005) Genetic linkage map of medaka with polymerase chain reaction length polymorphisms. Gene 363:24–31

    Article  CAS  PubMed  Google Scholar 

  • Kosambi DD (1994) 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, 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(4):1649–1660

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Launey S, Hedgecock D (2001) High genetic load in the Pacific oyster Crassostrea gigas. Genetics 159:255–265

    PubMed Central  CAS  PubMed  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 Central  CAS  PubMed  Google Scholar 

  • Li Y, Cai M, Wang ZY, Guo W, Liu X, Wang X, Ning Y (2008) Microsatellite–centromere mapping in large yellow croaker (Pseudosciaena crocea) using gynogenetic diploid families. Mar Biotechnol 10:83–90

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu Z (2007) Aquaculture genome technologies. Blackwell Publishing, Iowa

    Book  Google Scholar 

  • Liu Z, Cordes JF (2004) DNA marker technologies and their applications in aquaculture genetics. Aquaculture 238:1–37

    Article  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 Central  CAS  PubMed  Google Scholar 

  • Liu X, Sui B, Wang Z, Cai M, Yao C, Chen Q (2011) Estimated reproductive success of brooders and heritability of growth traits for large yellow croaker (Larimichthys crocea) using microsatellites. Chin J Oceanol Limnol 29:990–995

    Article  Google Scholar 

  • Liu X, Zhao G, Wang Z, Cai M, Ye H, Wang Q (2012) Parentage assignment and parental contribution analysis in large yellow croaker Larimichthys crocea using microsatellite markers. Curr Zool 58:244–249

    CAS  Google Scholar 

  • Liu F, Sun F, Li J, Xia JH, Lin G, Tu RJ, Yue GH (2013) A microsatellite-based linkage map of salt tolerant tilapia (Oreochromis mossambicus x Oreochromis spp.) and mapping of sex-determining loci. BMC Genomics 14:58

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ma P (2005) Mariculture in Fujian. Fujian Science and Technology Press, Fuzhou

    Google Scholar 

  • Massault C, Hellemans B, Louro B, Batargias C, Van Houdt JK, Canario A, Volckaert FA, Bovenhuis H, Haley C, de Koning DJ (2010) QTL for body weight, morphometric traits and stress response in European sea bass Dicentrarchus labrax. Anim Genet 41:337–345

    CAS  PubMed  Google Scholar 

  • Moen T, Hoyheim B, Munck H, Gomez-Raya (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  CAS  PubMed  Google Scholar 

  • Moen T, Hayes B, Baranski M, Berg PR, Kjoglum S (2008) A linkage map of the Atlantic salmon (Salmo salar) based on EST-derived SNP markers. BMC Genomics 9:223–236

    Article  PubMed Central  PubMed  Google Scholar 

  • Ning Y, Liu X, Wang Z, Guo W, Li Y, Xie F (2007) A genetic map of large yellow croaker Pseudosciaena crocea. Aquaculture 264:16–26

    Article  CAS  Google Scholar 

  • Oetting WS, Lee HK, Flanders DJ, Wiesner GL, Sellers TA, King RA (1995) Linkage analysis with multiplexed short tandem repeat polymorphisms using infrared fluorescence and M13 tailed primers. Genomics 30:450–458

    Article  CAS  PubMed  Google Scholar 

  • Ozaki A, Sakamoto T, Khoo S, Nakamura K, Coimbra M, Akutsu T, Okamoto N (2001) Quantitative trait loci (QTLs) associated with resistance/susceptibility to infectious pancreatic necrosis virus (IPNV) in rainbow trout (Oncorhynchus mykiss). Mol Genet Genomics 265:23–31

    Article  CAS  PubMed  Google Scholar 

  • Qin Y, Liu X, Zhang H, Zhang G, Guo X (2007) Genetic mapping of size-related quantitative trait loci (QTL) in the bay scallop (Argopecten irradians) using AFLP and microsatellite markers. Aquaculture 272:281–290

    Article  CAS  Google Scholar 

  • Quan C, Wang J, Ding S, Su Y, Yao J (2000) The Êaryotypes of Pseudosciaena crocea (Richardson). J Xiamen Univ (Nat Sci Ed) 29:107–110 (in Chinese with English abstract)

    Google Scholar 

  • Reid DP, Szanto A, Glebe B, Danzmann R, Ferguson M (2004) QTL for body weight and condition factor in Atlantic salmon (Salmo salar): comparative analysis with rainbow trout (Oncorhynchus mykiss) and Arctic charr (Salvelinus alpinus). Heredity 94:166–172

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Rodríguez-Ramilo ST, Herrán RDL, Ruiz-Rejón C, Hermida M, Fernández C, Pereiro P, Figueras A, Bouza C, Toro MA, Martínez P, Fernández J (2014) Identification of quantitative trait loci associated with resistance to viral haemorrhagic septicaemia (VHS) in Turbot (Scophthalmus maximus): a comparison between bacterium, parasite and virus diseases. Mar Biotechnol 16:265–276

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Sánchez-Molano E, Cerna A, Toro MA, Bouza C, Hermida M, Pardo BG, Cabaleiro S, Fernández J, Martínez P (2011) Detection of growth-related QTL in turbot (Scophthalmus maximus). BMC Genomics 12:473–482

    Article  PubMed Central  PubMed  Google Scholar 

  • Seaton G, Hernandez J, Grunchec JA, White I, Allen J, Koning D J, Wei W, Berry D, Haley C, Knott S (2006) GridQTL: a Grid portal for QTL mapping of compute intensive datasets. Proceedings of the 8th World Congress on Genetics Applied to Livestock Production. Belo Horizonte, Minas Gerais, Brazil

  • Somridhivej B, Wang S, Sha Z, Liu H, Quilang J, Xu P, Li P, Hue ZL, Liu ZJ (2008) Characterization, polymorphism assessment, and database construction for microsatellites from BAC end sequences of catfish: a resource for integration of linkage and physical maps. Aquaculture 275:76–80

    Article  CAS  Google Scholar 

  • Song W, Li Y, Zhao Y, Liu Y, Niu Y, Pang R, Miao G, Liao X, Shao C, Gao F, Chen S (2012a) Construction of a high-density microsatellite genetic linkage map and mapping of sexual and growth-related traits in half-smooth tongue sole (Cynoglossus semilaevis). PLoS One 7(12):e52097

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Song W, Peng R, Niu Y, Gao F, Zhao Y, Zhang J, Sun J, Shao C, Liao X, Wang L, Tian Y, Chen S (2012b) Construction of high-density genetic linkage maps and mapping of growth-related quantitative trait loci in the Japanese flounder (Paralichthys olivaceus). PLoS One 7(11):e50404

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Tan YD, Wan C, Zhu Y, Lu C, Xiang Z, Deng HW (2001) An amplified fragment length polymorphism map of the silkworm. Genetics 157:1277–1284

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tripathi N, Hoffmann M, Willing E, Lanz C, Weigel D, Dreyer C (2009) Genetic linkage map of the guppy, Poecilia reticulata, and quantitative trait loci analysis of male size and colour variation. Proc Biol Sci 276:2195–2208

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vallejo RL, Palti Y, Liu S, Evenhuis JP, Gao G, Rexroad CE III, Wiens GD (2014) Detection of QTL in rainbow trout affecting survival when challenged with Flavobacterium psychrophilum. Mar Biotechnol 16:349–360

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Visscher PM, Thompson R, Haley CS (1996) Confidence intervals in QTL mapping by bootstrapping. Genetics 143:1013–1020

    PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Waldbieser GC, Bosworth BG, Nonneman DJ, Wolters WR (2001) A microsatellite-based genetic linkage map for channel catfish, Ictalurus punctatus. Genetics 158:727–734

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wang Z, Wang Y, Lin L, Khoo SK, Okamoto N (2002) Genetic polymorphisms in wild and cultured large yellow croaker Pseudosciaena crocea using AFLP finger printing. J Fishery Sci China 9:198–202

    CAS  Google Scholar 

  • Wang CM, Lo LC, Zhu ZY, Yue GH (2006a) A genome scan for quantitative trait loci affecting growth-related traits in an F1 family of Asian seabass (Lates calcarifer). BMC Genomics 7:274–286

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang DX, Su YQ, Wang SF, Wang J (2006b) The karyotypes and their polymorphisms of the Pseudosciaena crocea from different populations. Acta Oceanol Sin 28(6):176–178

    CAS  Google Scholar 

  • Wang CM, Zhu ZY, Lo LC, Feng F, Lin G, Yang WT, Li J, Yue GH (2007) A microsatellite linkage map of Barramundi, Lates calcarifer. Genetics 175:907–915

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang CM, Lo LC, Feng F, Zhu ZY, Yue GH (2008) Identification and verification of QTL associated with growth traits in two genetic backgrounds of Barramundi (Lates calcarifer). Anim Genet 39(1):34–39

    Article  PubMed  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 12:174–192

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Woram RA, McGowan C, Stout JA, Gharbi K, Ferguson MM, Hoyheim B, Davidson EA, Davidson WS, Rexroad C, Danzmann RG (2004) A genetic linkage map for Arctic char (Salvelinus alpinus): evidence for higher recombination rates and segregation distortion in hybrid versus pure strain mapping parents. Genome 47:304–315

    Article  CAS  PubMed  Google Scholar 

  • Ye H, Wang X, Gao T, Wang Z (2010) EST-derived microsatellites in Pseudosciaena crocea and their applicability to related species. Acta Oceanol Sin 29:83–91

    Article  CAS  Google Scholar 

  • Young WP, Wheeler PA, Coryell VH, Keim P, Thorgaard GH (1998) A detailed linkage map of rainbow trout produced using doubled haploids. Genetics 148:839–850

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zamir D, Tadmor Y (1986) Unequal segregation of nuclear genes in plants. Bot Gaz 147:355–358

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank ZY Zhang for his support in data analysis. This study was supported by the National Natural Science Foundation of China (U1205122, 31172397), the National High Technology Research and Development Program of China (2012AA10A403), and the Foundation for Innovation Research Team of Jimei University, China (no. 2010A02).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhiyong Wang.

Additional information

Hua Ye and Yang Liu contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental Table 1

(DOCX 51 kb)

Supplemental Table 2

(DOC 28 kb)

Supplemental Table 3

(DOC 29 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ye, H., Liu, Y., Liu, X. et al. Genetic Mapping and QTL Analysis of Growth Traits in the Large Yellow Croaker Larimichthys crocea . Mar Biotechnol 16, 729–738 (2014). https://doi.org/10.1007/s10126-014-9590-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-014-9590-z

Keywords

Navigation