Skip to main content
SpringerLink
Log in

Construction of the First High-Density Genetic Linkage Map and Analysis of Quantitative Trait Loci for Growth-Related Traits in Sinonovacula constricta

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

Abstract

The razor clam (Sinonovacula constricta) is an important aquaculture species, for which a high-density genetic linkage map would play an important role in marker-assisted selection (MAS). In this study, we constructed a high-density genetic map and detected quantitative trait loci (QTLs) for Sinonovacula constricta with an F1 cross population by using the specific locus amplified fragment sequencing (SLAF-seq) method. A total of 315,553 SLAF markers out of 467.71 Mreads were developed. The final linkage map was composed of 7516 SLAFs (156.60-fold in the parents and 20.80-fold in each F1 population on average). The total distance of the linkage map was 2383.85 cM, covering 19 linkage groups with an average inter-marker distance of 0.32 cM. The proportion of gaps less than 5.0 cM was on average 96.90%. A total of 16 suggestive QTLs for five growth-related traits (five QTLs for shell height, six QTLs for shell length, three QTLs for shell width, one QTL for total body weight, and one QTL for soft body weight) were identified. These QTLs were distributed on five linkage groups, and the regions showed overlapping on LG9 and LG13. In conclusion, the high-density genetic map and QTLs for S. constricta provide a valuable genetic resource and a basis for MAS.

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

Similar content being viewed by others

References

  • Abdelrahman H, ElHady M, Alcivar-Warren A, Allen S, Al-Tobasei R, Bao L, Beck B, Blackburn H, Bosworth B, Buchanan J, Chappell J, Daniels W, Dong S, Dunham R, Durland E, Elaswad A, Gomez-Chiarri M, Gosh K, Guo X, Hackett P, Hanson T, Hedgecock D, Howard T, Holland L, Jackson M, Jin Y, Kahlil K, Kocher T, Leeds T, Li N, Lindsey L, Liu S, Liu Z, Martin K, Novriadi R, Odin R, Palti Y, Peatman E, Proestou D, Qin G, Reading B, Rexroad C, Roberts S, Salem M, Severin A, Shi H, Shoemaker C, Stiles S, Tan S, Tang KF, Thongda W, Tiersch T, Tomasso J, Prabowo WT, Vallejo R, van der Steen H, Vo K, Waldbieser G, Wang H, Wang X, Xiang J, Yang Y, Yant R, Yuan Z, Zeng Q, Zhou T (2017) Aquaculture genomics, genetics and breeding in the United States: current status, challenges, and priorities for future research. BMC Genomics 18:191

    Article  PubMed  PubMed Central  Google Scholar 

  • Amores A, Catchen J, Nanda I, Warren W, Walter R, Schartl M, Postlethwait JH (2014) A RAD-tag genetic map for the platyfish (Xiphophorus maculatus) reveals mechanisms of karyotype evolution among teleost fish. Genetics 197:625–641

    Article  PubMed  PubMed Central  Google Scholar 

  • Bai ZY, Han X, Luo M, Lin JY, Wang GL, Li JL (2015) Constructing a microsatellite-based linkage map and identifying QTL for pearl quality traits in triangle pearl mussel (Hyriopsis cumingii). Aquaculture 437:102–110

    Article  CAS  Google Scholar 

  • Bai ZY, Han XK, Liu XJ, Li QQ, Li JL (2016) Construction of a high-density genetic map and QTL mapping for pearl quality-related traits in Hyriopsis cumingii. Sci Rep 6:32608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui Y, Wang H, Qiu X, Liu H, Yang R (2015) Bayesian analysis for genetic architectures of body weights and morphological traits using distorted markers in Japanese flounder Paralichthys olivaceus. Mar Biotechnol 17:693–702

    Article  CAS  PubMed  Google Scholar 

  • Faure S, Noyer JL, Horry JP, Bakry F, Lanaud C, Gonzalez de Leon D (1993) A molecular marker-based linkage map of diploid bananas (Musa acuminata). Theor Appl Genet 87:517–526

    Article  CAS  PubMed  Google Scholar 

  • Franch R, Louro B, Tsalavouta M, Chatziplis D, Tsigenopoulos CS, Sarropoulou E, Antonello J, Magoulas A, Mylonas CC, Babbucci M, Patarnello T, Power DM, Kotoulas G, Bargelloni L (2006) A genetic linkage map of the hermaphrodite teleost fish Sparus aurata L. Genetics 174:851–861

    Article  CAS  PubMed  PubMed Central  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 (NY) 14:218–226

    Article  CAS  Google Scholar 

  • Haldane JBS (1922) Sex ratio and unisexual sterility in hybrid animals. J Genet 12:101–109

    Article  Google Scholar 

  • Huang XH, Zhao Y, Wei XH, Li CY, Wang A, Zhao Q, Li WJ, Guo YL, Deng LW, Zhu CR, Fan DL, Lu YQ, Weng QJ, Liu KY, Zhou TY, Jing YF, Si LZ, Dong GJ, Huang T, Lu TT, Feng Q, Qian Q, Li JY, Han B (2012) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32–U53

    Article  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  PubMed Central  Google Scholar 

  • Hubert S, Higgins B, Borza T, Bowman S (2010) Development of a SNP resource and a genetic linkage map for Atlantic cod (Gadus morhua). BMC Genomics 11:191

    Article  PubMed  PubMed Central  Google Scholar 

  • Huxley JS (1928) Sexual difference of linkage in Gammarus chevreuxi. J Genet 20:145–156

    Article  Google Scholar 

  • Jansen J, de Jong AG, van Ooijen JW (2001) Constructing dense genetic linkage maps. Theor Appl Genet 102:1113–1122

    Article  CAS  Google Scholar 

  • Ji GS, Zhang QJ, Du RH, Lv P, Ma X, Fan S, Li SY, Hou SL, Han YC, Liu GQ (2017) Construction of a high-density genetic map using specific-locus amplified fragments in sorghum. BMC Genomics 18:51

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiao W, Fu X, Dou J, Li H, Su H, Mao J, Yu Q, Zhang L, Hu X, Huang X (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

    Article  CAS  PubMed  Google Scholar 

  • Jones DB, Jerry DR, Khatkar MS, Raadsma HW, Zenger KR (2013) A high-density SNP genetic linkage map for the silver-lipped pearl oyster, Pinctada maxima: a valuable resource for gene localisation and marker-assisted selection. BMC Genomics 14:810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones DB, Jerry DR, Khatkar MS, Moser G, Raadsma HW, Taylor JJ, Zenger KR (2014) Quantitative trait loci and genetic association analysis reveals insights into complex pearl quality traits in donor silver-lipped pearl oysters. Aquaculture 434:476–485

    Article  Google Scholar 

  • Kessuwan K, 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

    Article  CAS  PubMed  Google Scholar 

  • Kosambi DD (1943) The estimation of map distances from recombination values. Ann Hum Genet 12:172–175

    Google Scholar 

  • Laghari MY, Lashari P, Zhang X, Xu P, Xin B, Zhang Y, Narejo NT, Sun X (2013) Mapping quantitative trait loci (QTL) for body weight, length and condition factor traits in backcross (BC1) family of common carp ( Cyprinus carpio L.) Mol Biol Rep 41:721–731

    Article  PubMed  Google Scholar 

  • Lallias D, Beaumont AR, Haley CS, Boudry P, Heurtebise S, Lapegue 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  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindblad-Toh K, Winchester E, Daly MJ, Wang DG, Hirschhorn JN, Laviolette JP, Ardlie K, Reich DE, Robinson E, Sklar P, Shah N, Thomas D, Fan JB, Gingeras T, Warrington J, Patil N, Hudson TJ, Lander ES (2000) Large-scale discovery and genotyping of single-nucleotide polymorphisms in the mouse. Nat Genet 24:381–386

    Article  CAS  PubMed  Google Scholar 

  • Liu DY, Ma CX, Hong WG, Huang L, Liu M, Liu H, Zeng HP, Deng DJ, Xin HG, Song J, Xu CH, Sun XW, Hou XL, Wang XW, Zheng HK (2014) Construction and analysis of high-density linkage map using high-throughput sequencing data. PLoS One 9:e98855

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu S, Vallejo RL, Gao G, Palti Y, Weber GM, Hernandez A, Rd RC (2015) Identification of single-nucleotide polymorphism markers associated with cortisol response to crowding in rainbow trout. Mar Biotechnol 17:328

    Article  CAS  PubMed  Google Scholar 

  • Liu P, Wang L, Wan ZY, Ye BQ, Huang S, Wong SM, Yue GH (2016) Mapping qtl for resistance against viral nervous necrosis disease in Asian seabass. Mar Biotechnol 18:107–116

    Article  CAS  PubMed  Google Scholar 

  • Luo L, Zhang YM, Xu S (2005) A quantitative genetics model for viability selection. Heredity (Edinb) 94:347–355

    Article  CAS  Google Scholar 

  • Miller MR, Dunham JP, Amores A, Cresko WA, Johnson EA (2007) Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Res 17:240–248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Negrínbáez D, Navarro A, Rodríguezramilo ST, Afonso JM, Zamorano MJ (2016) Identification of quantitative trait loci associated with the skeletal deformity lsk complex in gilthead seabream (Sparus aurata L.) Mar Biotechnol 18:98–106

    Article  Google Scholar 

  • Niu DH, Li JL, Liu DB (2008) Polymorphic microsatellite loci for population studies of the razor clam, Sinonovacula constricta. Conserv Genet 9:1393–1394

    Article  Google Scholar 

  • Niu D, Wang L, Sun F, Liu Z, Li J (2013) Development of molecular resources for an intertidal clam, Sinonovacula constricta, using 454 transcriptome sequencing. PLoS One 8:e67456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu DH, Wang F, Xie SM, Sun FY, Wang Z, Peng MX, Li JL (2016) Developmental transcriptome analysis and identification of genes involved in larval metamorphosis of the razor clam, Sinonovacula constricta. Mar Biotechnol 18:168–175

    Article  CAS  PubMed  Google Scholar 

  • Petersen JL, Baerwald MR, Ibarra AM, May B (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

    Article  Google Scholar 

  • Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7:e37135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poland JA, Brown PJ, Sorrells ME, Jannink JL (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS One 7:e32253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi ZM, Huang L, Zhu RS, Xin DW, Liu CY, Han X, Jiang HW, Hong WG, Hu GH, Zheng HK, Chen QS (2014) A high-density genetic map for soybean based on specific length amplified fragment sequencing. PLoS One 9:e104871

    Article  PubMed  PubMed Central  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 

  • Qiu G-F, Xiong L-W, Liu Z-Q, Yan Y-L, Shen H (2016) A first generation microsatellite-based linkage map of the Chinese mitten crab Eriocheir sinensis and its application in quantitative trait loci (QTL) detection. Aquaculture 451:223–231

    Article  CAS  Google Scholar 

  • Ren P, Peng W, You W, Huang Z, Guo Q, Chen N, He P, Ke J, Gwo J-C, Ke C (2016) Genetic mapping and quantitative trait loci analysis of growth-related traits in the small abalone Haliotis diversicolor using restriction-site-associated DNA sequencing. Aquaculture 454:163–170

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sauvage C, Boudry P, de Koning DJ, Haley CS, Heurtebise S, Lapegue 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 

  • Shi Y, Hong K, Guo X, Gu Z, Wang Y, Wang A (2009) Genetic linkage map of the pearl oyster, Pinctada martensii (Dunker). Aquac Res 41:35–44

    Article  CAS  Google Scholar 

  • Shi Y, Wang S, Gu Z, Lv J, Zhan X, Yu C, Bao Z, Wang A (2014) High-density single nucleotide polymorphisms linkage and quantitative trait locus mapping of the pearl oyster, Pinctada fucata martensii Dunker. Aquaculture 434:376–384

    Article  Google Scholar 

  • Sun L, Yang W, Zhang Q, Cheng T, Pan H, Xu Z, Zhang J, Chen C (2013a) Genome-wide characterization and linkage mapping of simple sequence repeats in mei (Prunus mume Sieb. Et Zucc.) PLoS One 8:e59562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun XW, Liu DY, Zhang XF, Li WB, Liu H, Hong WG, Jiang CB, Guan N, Ma CX, Zeng HP, Xu CH, Song J, Huang L, Wang CM, Shi JJ, Wang R, Zheng XH, Lu CY, Wang XW, Zheng HK (2013b) SLAF-seq: an efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS One 8:e58700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor DR, Ingvarsson PK (2003) Common features of segregation distortion in plants and animals. Genetica 117:27–35

    Article  CAS  PubMed  Google Scholar 

  • Tian L, Guo L, Pan Y, Qi Z, Wang J, Song Z (2016) Construction of the first high-density genetic linkage map of Salvia miltiorrhiza using specific length amplified fragment (SLAF) sequencing. Sci Rep 6:24070

    Article  Google Scholar 

  • Van Ooijen JW (2011) Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet Res 93:343–349

    Article  Google Scholar 

  • van Os H, Stam P, Visser RGF, van Eck HJ (2005) SMOOTH: a statistical method for successful removal of genotyping errors from high-density genetic linkage data. Theor Appl Genet 112:187–194

    Article  CAS  PubMed  Google Scholar 

  • Wang WX, Huang SM, Liu YM, Fang ZY, Yang LM, Hua W, Yuan SX, Liu SY, Sun JF, Zhuang M, Zhang YY, Zeng AS (2012) Construction and analysis of a high-density genetic linkage map in cabbage (Brassica oleracea L. var. capitata). BMC Genomics 13:523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Niu D, Li J (2013) Charaterization of novel EST-derived SNP markers by using 454 pyrosequencing in Sinonovacula constricta. Conserv Genet Resour 5:191–193

    Article  Google Scholar 

  • Wang J, Li L, Zhang G (2016) A high-density snp genetic linkage map and qtl analysis of growth-related traits in a hybrid family of oysters (Crassostrea gigas × Crassostrea angulata) using genotyping-by-sequencing. G3-Genes Genomes Genetics 6: 1417-1426

  • 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 

  • Xia JH, Lin G, He X, Yunping B, Liu P, Liu F, Sun F, Tu R, Yue GH (2014) Mapping quantitative trait loci for omega-3 fatty acids in Asian seabass. Mar Biotechnol (NY) 16:1–9

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu XW, Xu RX, Zhu BY, Yu T, Qu WQ, Lu L, Xu Q, Qi XH, Chen XH (2015) A high-density genetic map of cucumber derived from specific length amplified fragment sequencing (SLAF-seq). Front Plant Sci 5:768

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu Y, Zhang X, Yuan J, Li F, Chen X, Zhao Y, Huang L, Zheng H, Xiang J (2015) Genome survey and high-density genetic map construction provide genomic and genetic resources for the Pacific White Shrimp Litopenaeus vannamei. Sci Rep 5:15612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yue GH (2014) Recent advances of genome mapping and marker-assisted selection in aquaculture. Fish Fish 15:376–396

    Article  Google Scholar 

  • Zhan A, Hu J, Hu X, Hui M, Wang M, Peng W, Huang X, Wang S, Lu W, Sun C, Bao Z (2009) Construction of microsatellite-based linkage maps and identification of size-related quantitative trait loci for Zhikong scallop (Chlamys farreri). Anim Genet 40:821–831

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Wang S, Li H, Deng Q, Zheng A, Li S, Li P, Li Z, Wang J (2010) Effects of missing marker and segregation distortion on QTL mapping in F2 populations. Theor Appl Genet 121:1071–1082

    Article  PubMed  Google Scholar 

  • Zhao Z, Gu H, Sheng X, Yu H, Wang J, Huang L, Wang D (2016) Genome-wide single-nucleotide polymorphisms discovery and high-density genetic map construction in cauliflower using specific-locus amplified fragment sequencing. Front Plant Sci 7:334

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31472278), National High Technology Research and Development Program of China (863 Program) (2012AA10A400), and the Shanghai Universities Knowledge Service Platform (ZF1206). We would like to thank the native English-speaking scientists of Elixigen Company.

Author information

Authors and Affiliations

  1. Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, 201306, China

    Donghong Niu, Yunchao Du, Ze Wang, Shumei Xie, Haideng Nguyen, Heding Shen & Jiale Li

  2. National Demonstration Center for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai, 201306, China

    Donghong Niu

  3. Shanghai Engineering Research Center of Aquaculture, Shanghai, 201306, China

    Donghong Niu & Heding Shen

  4. Co-Innovation Center of Jiangsu Marine Bio-industry Technology, Huaihai Institute of Technology, Lianyungang, 222005, China

    Zhiguo Dong & Jiale Li

  5. College of Aquaculture and Life Science, Shanghai Ocean University, Shanghai, 201306, China

    Jiale Li

Authors
  1. Donghong Niu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yunchao Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ze Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shumei Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Haideng Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhiguo Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Heding Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jiale Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jiale Li.

Electronic supplementary material

ESM 1

(DOC 70 kb)

ESM 2

(DOC 77 kb)

ESM 3

(XLSX 292 kb)

ESM 4

(XLSX 292 kb)

ESM 5

(XLSX 292 kb)

ESM 6

(DOC 152 kb)

ESM 7

(DOC 70 kb)

Supplementary Fig. S1

Distribution of the various types of markers. The Y axis is the number of SLAFs, the X axis is the type of SLAFs. (JPEG 84 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Niu, D., Du, Y., Wang, Z. et al. Construction of the First High-Density Genetic Linkage Map and Analysis of Quantitative Trait Loci for Growth-Related Traits in Sinonovacula constricta . Mar Biotechnol 19, 488–496 (2017). https://doi.org/10.1007/s10126-017-9768-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-017-9768-2

Keywords

Search

Navigation