Abstract
Golden shell color and mineral content are important economic traits of Pacific oyster (Crassostrea gigas). In this study, we mapped a series of quantitative trait loci (QTLs) that control zinc (Zn) and magnesium (Mg) content, shell color and growth performance to two sex-averaged linkage maps from the FAM-A and FAM-B families. In total, ten QTLs were identified in seven linkage groups (LGs) in the FAM-B family, and seven QTLs were identified in four linkage groups in the FAM-A family. Two QTLs affecting the trait of golden shell color were identified in LG8 of the FAM-A and LG10 of the FAM-B families, which could explain 20.2 and 10.5% of the phenotypic variations, respectively. Two QTLs for Zn content were identified that could contribute to 17.9 and 34.44% of the phenotypic variations in FAM-A. Six QTLs for Zn and Mg contents were identified in four LGs (LG1, LG2, LG5, and LG9) in FAM-B, which explained 13.5–26.7% of the phenotypic variations. In addition, seven QTLs related to oyster growth were recognized in both FAM-A and FAM-B families accounting for 14.6–36.7% of the phenotypic variations. All of the DNA markers in QTL regions were blasted and 14 genes associated with above traits were identified. The mRNA expression of these genes was determined by quantitative RT-PCR. These QTLs and candidate genes could be used as potential targets for marker-assisted selection in C. gigas breeding.
Similar content being viewed by others
References
Bai J, Li Q, Cong RH, Sun WJ, Liu J, Feng YW (2011) Development and characterization of 68 expressed sequence tag derived simple sequence repeat markers in the Pacific oyster, Crassostrea gigas. J World Aquacult Soc 42:444–455
Bai Z, Han X, Luo M, Lin Y, Wang G, Li J (2015) Constructing a microsatellite-based linkage map and identifying QTL for pearl quality traits in triangle pearl mussel (Hyriopsis cumingii). Aquaculture 437:102–110
Baranski M, Moen T, Vage DI (2010) Mapping of quantitative trait loci for flesh colour and growth traits in Atlantic salmon (Salmo salar). Genet Sel Evol 42:1–14
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
Dato-Cajegas CRS, Yakupitiyage A (1996) The need for dietary mineral supplementation for Nile tilapia, Oreochromis niloticus, cultured in a semi-intensive system. Aquaculture 144:227–237
Dégremont L, Ernande B, Bédier E, Boudry P (2007) Summer mortality of hatchery-produced Pacific oyster spat (Crassostrea gigas). I. Estimation of genetic parameters for survival and growth. Aquaculture 262:41–53
Evans S, Camara MD, Langdon CJ (2009) Heritability of shell pigmentation in the Pacific oyster, Crassostrea gigas. Aquaculture 286:211–216
FAO (2017) Yearbook of fishery and aquaculture statistic. Available from http://www.fao.org//fishery/publications/yearbooks/en. Accesssed 21 Dec 2017
Feng D, Li Q, Yu H, Zhao X, Kong LF (2015) Comparative transcriptome analysis of the Pacific oyster Crassostrea gigas characterized by shell colors: identification of genetic bases potentially involved in pigmentation. PLoS One 10:e0145257
Ge J, Li Q, Yu H, Kong L (2014) Identification and mapping of a SCAR marker linked to a locus involved in shell pigmentation of the Pacific oyster (Crassostrea gigas). Aquaculture 434:249–253
Ge J, Li Q, Yu H, Kong L (2015a) Identification of single-locus PCR-based on markers linked to shell background color in the in the Pacific oyster Crassostrea gigas. Mar Biotechnol 17:655–662
Ge J, Li Q, Yu H, Kong L (2015b) Mendelian inheritance of golden shell color in the Pacific oyster Crassostrea gigas. Aquaculture 441:21–24
Goddard ME, Hayes BJ (2009) Mapping genes for complex traits in domestic animals and their use in breeding programmes. Nat Rev Genet 10:381–391
Gong XP, Liang X, Wu CH, Guo Y, Zhao Y, Li SS, Li XH, Kong FM (2016) Selenium effects and quantitative trait locus (QTL) mapping for mineral nutrient efficiency traits in wheat at the seedling stage. J Plant Nutr 39:1087–1102
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
Guo WJ, Tong J, Yu X, Zhu C, Feng X, Fu B, He S, Zeng F, Wang X, Liu H, Liu L (2013) A second generation genetic linkage map for silver carp (Hypophthalmichehys molitrix) using microsatellite markers. Aquaculture 412-413:97–106
Hao ZL, Yang LM, Zhan YY, Tian Y, Ding J, Pang YL, Chang YQ (2015) Biochemical components of different colored strains of cultured Japanese scallop (Mizuhopecten yessoensis) under different cultivation systems. Isr J Aquacult Bamidgeh 67:1189–1197
Hedgecock D, Grupe P, Voigt M (2006) Mapping genes affecting shell color and shape in the Pacific Oyster Crassostrea gigas. J Shellfish Res 25:783
Hedgecock D, Shin G, Gracey AY, Den Berg DV, Samanta MP (2015) Second-generation linkage maps for the Pacific oyster Crassostrea gigas reveal errors in assembly of genome scaffolds. G3 (Bethesda) 5:2007–2019
Hubert S, Hedgecock D (2004) Linkage maps of microsatellite DNA markers for the Pacific oyster Crassostrea gigas. Genetics 168:351–362
Hubert S, Cognard E, Hedgecock D (2009) Centromere-mapping in triploid families of the Pacific oyster Crassostrea gigas (Thunberg). Aquaculture 288:172–183
Huvet A, Boudry P, Ohresser M, Delsert C, Bonhomme F (2000) Variable microsatellites in the Pacific oyster Crassostrea gigas and other cupped oyster species. Anim Genet 31:71–72
Jiao WQ, Fu XT, Dou JZ, Li HD, Su HL, Mao JX, Yu Q, Zhang LL, Hu XL, Huang XT, Wang YF, Wang S, Bao ZM (2014) High-resolution linkage and quantitative trait locus mapping aided by genome survey sequencing: building up an integrative genomic framework for a bivalve mollusc. DNA Res 21:85–101
Jin S, Zhang X, Jia Z, Fu H, Zheng X, Sun X (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 358-359:176–182
Jin TT, Chen J, Zhu L, Zhao Y, Guo J, Huang Y (2015) Comparative mapping combined with homologybased cloning of the rice genome reveals candidate genes for grain zinc and iron concentration in maize. BMC Genet 16:17–32
Kessuwan K, Kubota S, Kubota S, Liu Q, Sano M, Okamoto N, Sakamoto T, Yamashita H, Nakamura Y, Ozaki A (2016) Detection of growth-related quantitative trait loci and high-resolution genetic linkage maps using simple sequence repeat markers in the kelp grouper (Epinephelus bruneus). Mar Biotechnol 18:57–84
Li L, Guo XM (2004) AFLP-based genetic linkage maps of the Pacific oyster Crassostrea gigas. Thunberg. Mar Biotechnol 6:26–36
Li G, Hubert S, Bucklin K, Ribes V, Hedgecock D (2003) Characterization of 79 microsatellite DNA markers in the Pacific oyster Crassostrea gigas. Mol Ecol Notes 3:228–232
Li Q, Chen LM, Kong LF (2009a) A genetic linkage map of the sea cucumber, Apostichopus japonicus (Selenka), based on AFLP and microsatellite markers. Anim Genet 40:678–685
Li Q, Liu SK, Kong LF (2009b) Microsatellites within genes and ESTs of the Pacific oyster Crassostrea gigas and their transferability in five other Crassostrea species. Electron J Biotechnol 12:1–9
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
Li Q, Wang QZ, Qi MJ, Ge JL, Cong RH (2011b) Development, characterization, and inheritance of 113 novel EST-SSR markers in the Pacific oyster (Crassostrea gigas). Genes Genomics 33:313–316
Li H, Liu X, Zhang G (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
Lu X, Wang HX, Liu BZ, Xiang JH (2013) Three EST-SSR markers associated with QTL for the growth of the clam Meretrix meretrix revealed by selective genotyping. Mar Biotechnol 15:16–25
Mackay TF, Stone EA, Ayroles JF (2009) The genetics of quantitative traits: challenges and prospects. Nat Rev Genet 10:565–577
Massault C, Bovenhuis H, Haley C, Koning D (2008) QTL mapping designs for aquaculture. Aquaculture 285:23–29
Melchinger AE, Utz HF, Schon CC (1998) Quantitative trait locus (QTL) mapping using different testers and independent population samples in maize reveals low power of QTL detection and large bias in estimates of QTL effects. Genetics 149:383–403
Petersen JL, Baerwald MR, Ibarra AM (2012) A first-generation linkage map of the Pacific lion-paw scallop (Nodipecten subnodosus): initial evidence of QTL for size traits and markers linked to orange shell color. Aquaculture 350:200–209
Plough LV, Hedgecock D (2011) Quantitative trait locus analysis of stage-specific inbreeding depression in the Pacific oyster Crassostrea gigas. Genetics 189:1473–1486
Qi HG, Wu Q, Li L, Zhang GF (2009) Development and characterization of microsatellite markers for the Pacific oyster Crassostrea gigas. Conserv Genet Resour 1:451–453
Qin Y, Liu X, Zhang H, Zhang G, Guo X (2007) Identification and mapping of amplified fragment length polymorphism markers linked to shell color in bay scallop, Argopecten irradians irradians (Lamarck, 1819). Mar Biotechnol 9:66–73
Qiu X, Xu L, Liu SZ, Wang XL, Meng XY (2008a) Eleven polymorphic simple sequence repeat markers from expressed sequence tags of Pacific oyster Crassostrea gigas EST database. Conserv Genet 10:1773–1775
Qiu XM, Liu SZ, Wang XL, Meng XY (2008b) Eight SSR loci from oyster Crassostrea gigas EST database and cross-species amplification in C. plicatula. Conserv Genet 10:1013–1015
Sauvage C, Boudry P, Koning D, 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
Sekino M, Hamaguchi M, Aranishi F, Okoshi K (2003) Development of novel microsatellite DNA markers from the Pacific oyster Crassostrea gigas. Mar Biotechnol 5:227–233
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
Van Ooijen JW (2006) JoinMap4.0: software for the caculation of genetic linkage maps in experimental populations. Plant Research International, Wageningen
Van Ooijen JW (2009) MapQTL 6.0. software for the mapping of quantitative trait loci in experimental populations. Plant Research International, Wageningen
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wan S, Li Q, Liu T, Hong Y, Kong LF (2017) Heritability estimates for shell color-related traits in the golden shell strain of Pacific oyster (Crassostrea gigas) using a molecular pedigree. Aquaculture 476:65–71
Wang Y, Ren R, Yu ZN (2008) Bioinformatic mining of EST-SSR loci in the Pacific oyster, Crassostrea gigas. Anim Genet 39:287–289
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 Ocean Univ China 11:413–418
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
Xia JH, Lin G, He XP, Liu P, Liu F, Sun F, Tu RJ, Yue GH (2013) Whole genome scanning and association mapping identified a significant association between growth and a SNP in the IFABP-a gene of the Asian seabass. BMC Genomics 14:295–306
Yam KL, Papadakis SE (2004) A simple digital imaging method for measuring and analyzing color of food surfaces. J Food Eng 61:137–142
Yamtich J, Voigt ML, Li G, Hedgecock D (2005) Eight microsatellite loci for the Pacific oyster Crassostrea gigas. Anim Genet 36:524–526
Yu H, Li Q (2007) EST-SSR markers from the Pacific oyster Crassostrea gigas. Mol Ecol Notes 7:860–862
Yu H, Li Q (2008) Exploiting EST databases for the development, characterization of EST-SSRs in the Pacific oyster (Crassostrea gigas). J Hered 99:208–214
Yu ZN, Wang YH, Fu DK (2009) Development of 51 novel EST-SSR loci in the Pacific oyster, Crassostrea gigas by data mining from the public EST database. Conserv Genet Resour 2:13–18
Yu YH, Shao YF, Liu J, Fan YY, Sun CX, Cao ZY (2015) Mapping of quantitative trait loci for contents of macro- and microelements in milled rice (Oryza sativa L.). J Agric Food Chem 63:7813–7818
Zheng H, Zhang T, Sun Z, Liu W, Liu H (2013) Inheritance of shell colours in the noble scallop Chlamys nobilis (Bivalve: Pectinidae). Aquac Res 44:1229–1235
Zhong XX, Li Q, Guo X, Yu H, Kong LF (2014) QTL mapping for glycogen content and shell pigmentation in the Pacific oyster Crassostrea gigas using microsatellites and SNPs. Aquac Int 22:1877–1899
Funding
This work was supported by the grants from the National Natural Science Foundation of China (31772843), the Fundamental Research Funds for the Central Universities (201762014), Taishan Scholars Seed Project of Shandong, and the Industrial Development Project of Qingdao City (17-3-3-64-nsh).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Song, J., Li, Q., Yu, Y. et al. Mapping Genetic Loci for Quantitative Traits of Golden Shell Color, Mineral Element Contents, and Growth-Related Traits in Pacific Oyster (Crassostrea gigas). Mar Biotechnol 20, 666–675 (2018). https://doi.org/10.1007/s10126-018-9837-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-018-9837-1