Skip to main content
Log in

QTL mapping for glycogen content and shell pigmentation in the Pacific oyster Crassostrea gigas using microsatellites and SNPs

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

Glycogen content and shell pigmentation are two important economic traits of the Pacific oyster Crassostrea gigas. The first set of quantitative trait loci (QTLs) controlling the two traits was determined in an F1 full-sib family based on a sex-averaged linkage map. The linkage map was constructed using 120 SSRs, and 66 expressed sequence tag-derived single nucleotide polymorphisms (EST–SNPs). Two QTLs were found to be associated with glycogen content, explaining 0.27–79.05 % of the phenotypic variation. One QTL on LG9 were found to be related to shell pigmentation, the paternal and maternal alleles explaining 6.75 and 17.44 % of the phenotypic variation. The relationship of glycogen content with left shell depth and QTL linkage group analysis suggests that left shell depth and volume might be used to assist in indirect selection for glycogen content. The constructed linkage map and determined QTLs can provide a tool for further genetic analysis of the traits and be potential for marker-assisted selection in C. gigas breeding.

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

  • Adamkewicz SL, Castagna M (1988) Genetics of shell color and pattern in the bay scallop Argopecten irradians. J Hered 79:14–17

    Google Scholar 

  • Bacca H, Huvet A, Fabioux C, Daniel J-Y, Delaporte M, Pouvreaua S, Van Wormhoudt A, Moal J (2005) Molecular cloning and seasonal expression of oyster glycogen phosphorylase and glycogen synthase genes. Comp Biochem Physiol 140B:635–646

    Article  CAS  Google Scholar 

  • Brake J, Evans F, Langdon C (2004) Evidence for genetic control of pigmentation of shell and mantle edge in selected families of Pacific oysters, Crassostrea gigas. Aquaculture 229:89–98

    Article  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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cotter E, Malham SK, O’Keeffe S, Lynch SA, Latchford JW, King JW, Beaumont AR, Culloty SC (2010) Summer mortality of the Pacific oyster, Crassostrea gigas, in the Irish Sea: the influence of growth, biochemistry and gametogenesis. Aquaculture 303:8–21

    Article  Google Scholar 

  • Cut IG, Lathrop GM (2004) Duplicating SNPs. Nat Genet 36:789–790

    Article  Google Scholar 

  • Darvasi A, Weinreb A, Minke V, Wellert JI, Soller M (1993) Detecting marker-QTL linkage and estimating QTL gene effect and map location using a saturated genetic map. Genetics 134:943–951

    CAS  PubMed Central  PubMed  Google Scholar 

  • de Villena FPM, Sapienza C (2001) Nonrandom segregation during meiosis: the unfairness of females. Mamm Genome 12:331–339

    Article  Google Scholar 

  • Dégremont L, Bédier E, Boudry P (2010) Summer mortality of hatchery-produced Pacific oyster spat (Crassostrea gigas). II. response to selection for survival and its influence on growth and yield. Aquaculture 299:21–29

    Article  Google Scholar 

  • Deng YW, Fu S, Lu YZ, Du XD, Wang QH, Huang HL, Liu D (2013) Fertilization, hatching, survival, and growth of third-generation colored Pearl oyster (Pinctada martensii) Stocks. J Appl Aquacult 25:113–120

    Article  Google Scholar 

  • Doucleff M, Jin Y, Gao F, Riaz S, Krivanek AF, Walker MA (2004) A genetic linkage map of grape, utilizing Vitis rupestris and Vitis arizonica. Theor Appl Genet 109:1178–1187

    Article  CAS  PubMed  Google Scholar 

  • Evans S, Camara MD, Langdon CJ (2009) Heritability of shell pigmentation in the Pacific oyster, Crassostrea gigas. Aquaculture 286:211–216

    Article  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Garcia RM, Winkler FM (2012) Association between shell color of breeds (Lamarck, 1819) and the survival, growth and larval development of their progenies. Lat Am J Aquat Res 40:367–375

    Article  Google Scholar 

  • Gary FN (1980) Genetics of shell color in Mytilus edulis L. and the association of growth rate with shell color. J Exp Mar Biol Ecol 47:89–94

    Article  Google Scholar 

  • Guo X, Li Q, Wang QZ, Kong LF (2012) Genetic mapping and QTL analysis of growth-related traits in the Pacific oyster. Mar Biotechnol 14:218–226

    Article  CAS  PubMed  Google Scholar 

  • Hackett CA, Broadfoot LB (2003) Effects of genotyping errors, missing values and segregation distortion in molecular marker data on the construction of linkage maps. Heredity 90:33–38

    Article  CAS  PubMed  Google Scholar 

  • Hedgecock D, Grupe P, Voigt M (2006) Mapping genes affecting shell color and shape in the Pacific oyster Crassostrea gigas. J Shellfish Res 25:738

    Google Scholar 

  • Hedgecock D, Li G, Voigt ML (2007) Mapping heterosis QTL in the Pacific oyster Crassostrea gigas. Aquaculture 272:268

    Google Scholar 

  • Horikoshi H (1958) Glycogen. Chem Field 34:36–39

    Google Scholar 

  • Hu ZQ, Xu SZ (2009) PROC QTL—a SAS procedure for mapping quantitative trait loci. Int J Plant Genomics 2009:141234

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Imai T, Sakai S (1961) Study of breeding of Japanese oyster, Crassostrea gigas. Tohoku J Agric Res 12:125–171

    Google Scholar 

  • Jiang CJ, Zeng ZB (1997) Mapping quantitative trait loci with dominant and missing markers in various crosses from two inbred lines. Genetica 101:47–58

    Article  CAS  PubMed  Google Scholar 

  • Jin SB, Zhang XF, Jia ZY, Fu HT, Zheng XH, Sun XW (2012) Genetic linkage mapping and genetic analysis of QTL related to eye cross and eye diameter in common carp (Cyprinus carpio L.) using microsatellites and SNPs. Aquaculture 259:176–182

    Article  Google Scholar 

  • Jin YL, Li Q, Kong LF, Yu H. (2014) Development, inheritance and evaluation of 55 novel single nucleotide polymorphism markers for parentage assignment in the Pacific oyster (Crassostrea gigas). Genes Genom 36:129–141

  • Kobayashi T, Kawahara I, Hasekura O, Kijima A (2004) Genetic control of bluish shell color variation in the Pacific abalone, Haliotis discus hannai. J Shellfish Res 23:1153–1156

    Google Scholar 

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

    Article  Google Scholar 

  • Lallias D, Beaumont AR, Haley CS, Boudry P, Heurtebise S, Lapègue S (2007) A first-generation genetic linkage map of the European flat oyster Ostrea edulis (L) based on AFLP and microsatellite markers. Anim Genet 38:560–568

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li L, Guo XM (2004) AFLP-based genetic linkage maps of the Pacific oyster Crassostrea gigas Thunberg. Mar Biotechnol 6:26–36

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Park C, Kijima A (2002) Isolation and characterization of microsatellite loci in the Pacific abalone, Haliotis discus hannai. J Shellfish Res 21:811–815

    Google Scholar 

  • Li Q, Liu WG, Shirasu K, Chen WM, Jiang SX (2006) Reproductive cycle and biochemical composition of the Zhe oyster Crassostrea plicatula Gmelin in an eastern coastal bay of China. Aquaculture 261:752–759

    Article  CAS  Google Scholar 

  • Li Q, Wang QZ, Liu SK, Kong LF (2011a) Selection response and realized heritability for growth in three stocks of the Pacific oyster Crassostrea gigas. Fish Sci 77:643–648

    Article  CAS  Google Scholar 

  • Li Q, Yang L, Ke QZ, Kong LF (2011b) Gametogenic cycle and biochemical composition of the clam Mactra chinensis (Mollusca: Bivalvia): Implications for aquaculture and wild stock management. Mar Biol Res 7:407–415

    Article  Google Scholar 

  • Li HJ, Liu X, Zhang GF (2012) A Consensus Microsatellite-Based linkage map for the hermaphroditic bay scallop (Argopecten irradians) and its application in size-related QTL analysis. PLoS One 7:e46926

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lyttle TW (1991) Segregation distorters. Annu Rev Genet 25:511–557

    Article  CAS  PubMed  Google Scholar 

  • Mathieu M, Lubet P (1993) Storage tissue metabolism and reproduction in marine bivalves—a brief review. Invertebr Reprod Dev 23:123–129

    Article  CAS  Google Scholar 

  • Mitton JB (1977) Shell color and pattern variation in Mytilus edulis and its adaptive significance. Chesap Sci 18:387–390

    Article  Google Scholar 

  • Nell JA (2001) The history of oyster farming in Australia. Mar Fish Rev 63:14–25

    Google Scholar 

  • Piepho HP (2000) Optimal marker density for interval mapping in a backcross population. Heredity 84:437–440

    Article  PubMed  Google Scholar 

  • Rasaei A, Ghobadi ME, Ghobadi M, Abdi-niya K, Rasaei A, Ghobadi ME, Ghobadi M, Abdi-niya K (2011) The study of traits correlation and path analysis of the grain yield of the peas in semi-dry conditions in Kermanshah. International Conference on Food Engineering and Biotechnology, IACSIT Press, pp 246–249

  • Rice RW (1989) Analyzing tables of statistical test. Evolution 43:223–225

    Article  Google Scholar 

  • Sauvage C, Boudry P, De Koning D-J, Haley CS, Heurtebise S, Lapègue S (2010) QTL for resistance to summer mortality and OsHV-1 load in the Pacific oyster (Crassostrea gigas). Anim Genet 41:390–399

    CAS  PubMed  Google Scholar 

  • Serapion J, Kucuktas H, Feng JN, Liu ZJ (2004) Bioinformatic mining of type I microsatellites from expressed sequence tags of channel catfish (Ictalurus punctatus). Mar Biotechnol 6:364–377

    Article  CAS  PubMed  Google Scholar 

  • Ulgen A, Han Z, Li W (2003) Correlation between quantitative traits and correlation between corresponding LOD scores: detection of pleiotropic effects. BMC Genet 4:S60

    Article  PubMed Central  PubMed  Google Scholar 

  • Vales MI, Schon CC, Capettini F, Chen XM, Corey AE, Mather DE, Mundt CC, Richardson KL, Sandoval-Islas JS, Utz HF, Hayes PM (2005) Effect of population size on the estimation of QTL: a test using resistance to barley stripe rust. Theor Appl Genet 111:1260–1270

    Article  CAS  PubMed  Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0, software for the calculation of genetic linkage maps. Plant Research International, Wageningen

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

    Article  CAS  PubMed  Google Scholar 

  • Wada KT, Komaru A (1990) Inheritance of white coloration of the prismatic layer of shells in the Japanese pearl oyster Pincada fucata martensii and its importance in the pearl culture industry. Nippon Suisan Gakkaishi 56:1787–1790

    Article  Google Scholar 

  • Wada KT, Komaru A (1996) Color and weight of pearls produced by grafting the mantle tissue from a selected population for white shell color of the Japanese pearl oyster Pinctada fucata martensii (Dunker). Aquaculture 142:25–32

    Article  Google Scholar 

  • Wang CM, Zhu CS, Zhai HQ, Wan JM (2005) Mapping segregation distortion loci and quantitative trait loci for spikelet sterility in rice (Oryza sativa L.). Genet Res 86:97–106

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Wang A, Huang XH, Zhao Q, Dong GJ, Qian Q, Sang T, Han B (2011) Mapping 49 quantitative trait loci at high resolution through sequencing-based genotyping of rice recombinant inbred lines. Theor Appl Genet 122:327–340

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang QZ, Li Q, Kong LF, Yu RH (2012) Response to selection for fast growth in the second generation of Pacific Oyster (Crassostrea gigas). J O U C 11:413–418

    Google Scholar 

  • Ward RD, English LJ, McGoldrick DJ, Maguire GB, Nell JA, Thompson PA (2000) Genetic improvement of the Pacific oyster Crassostrea gigas (Thunberg) in Australia. Aquac Res 31:35–44

    Article  Google Scholar 

  • Winkler FM, Estevez BF, Jollan LB, Garrido JP (2001) Inheritance of the general shell color in the scallop Argopecten purpuratus (Bivalvia: Pectinidae). J Hered 92:521–525

    Article  CAS  PubMed  Google Scholar 

  • Xiong MM, Guo SW (1997) Fine-scale mapping of quantitative trait loci using historical recombinations. Genetics 145:1201–1218

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xu SZ (2008) Quantitative trait locus mapping can benefit from segregation distortion. Genetics 180:2201–2208

    Article  PubMed Central  PubMed  Google Scholar 

  • Yu ZN, Guo XM (2003) Genetic linkage map of the eastern oyster Crassostrea virginica Gmelin. Bioll Bull 204:327–338

    Article  CAS  Google Scholar 

  • Yu HH, Xie WB, Wang J, Xing YZ, Xu CG, Li XH, Xiao JH, Zhang QF (2011) Gains in QTL detection using an ultra-high density SNP map based on population sequencing relative to traditional RFLP/SSR Markers. PLoS One 6:e17595

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zeng Z, Ni JB, Ke CH (2013) Expression of glycogen synthase (GYS) and glycogen synthase kinase 3β (GSK3β) of the Fujian oyster, Crassostrea angulata, in relation to glycogen content in gonad development. Comp Biochem Physiol 166B:203–214

    Article  Google Scholar 

  • Zhang ZC, Xue CH, Gao X, Li ZJ, Wang Q (2006) Monthly changes of glycogen, lipid and free amino acid of oyster. JOUC 5:257–262

    CAS  Google Scholar 

  • Zhong XX, Li Q, Yu H, Kong LF (2013) Development and validation of single-nucleotide polymorphism markers in the Pacific oyster, Crassostrea gigas, using high-resolution melting analysis. J World Aquacult Soc 44:455–465

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the grants from 973 Program (2010CB126406), 863 Program (2012AA10A405-6), and National Natural Science Foundation of China (31372524).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Qi Li.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 429 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhong, X., Li, Q., Guo, X. et al. QTL mapping for glycogen content and shell pigmentation in the Pacific oyster Crassostrea gigas using microsatellites and SNPs. Aquacult Int 22, 1877–1889 (2014). https://doi.org/10.1007/s10499-014-9789-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-014-9789-z

Keywords

Navigation