Skip to main content
Log in

Identification of Quantitative Trait Loci for Resistance to RSIVD in Red Sea Bream (Pagrus major)

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

Abstract

Red sea bream iridoviral disease (RSIVD) is a major viral disease in red sea bream farming in Japan. Previously, we identified one candidate male individual of red sea bream that was significantly associated with convalescent individuals after RSIVD. The purpose of this study is to identify the quantitative trait loci (QTL) linked to the RSIVD-resistant trait for future marker-assisted selection (MAS). Two test families were developed using the candidate male in 2014 (Fam-2014) and 2015 (Fam-2015). These test families were challenged with RSIV, and phenotypes were evaluated. Then, de novo genome sequences of red sea bream were obtained through next-generation sequencing, and microsatellite markers were searched and selected for linkage map construction. One immune-related gene, MHC class IIβ, was also used for linkage map construction. Of the microsatellite markers searched, 148 and 197 were mapped on 23 and 27 linkage groups in the female and male linkage maps, respectively, covering approximately 65% of genomes in both sexes. One QTL linked to an RSIVD-resistant trait was found in linkage group 2 of the candidate male in Fam-2014, and the phenotypic variance of the QTL was 31.1%. The QTL was closely linked to MHC class IIβ. Moreover, the QTL observed in Fam-2014 was also significantly linked to an RSIVD-resistant trait in the candidate male of Fam-2015. Our results suggest that the RSIVD-resistant trait in the candidate male was controlled by one major QTL closely linked to the MHC class IIβ gene and could be useful for MAS of red sea bream.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Blanco-Gonzales E, Aritaki M, Taniguchi N (2012) Microsatellite multiplex panels for population genetic analysis of red sea bream Pagrus major. Fish Sci 78:603–611

    Article  Google Scholar 

  • Bouza C, Hermida M, Pardo BG, Fernández C, Fortes GG, Castro J, Sánchez L, Presa P, Pérez M, Sanjuán A, de Carlos A, Alvarez-Dios JA, Ezcurra S, Cal RM, Piferrer F, Martínez P (2007) A microsatellite genetic map of the turbot (Scophthalmus maximus). Genetics 177:2457–2467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broman KW, Wu H, Sen S, Churchill GA (2003) R/QTL: QTL mapping in experimental crosses. Bioinformatics 19:889–890

    Article  CAS  PubMed  Google Scholar 

  • Butler JM (2005) Forensic DNA typing: biology, technology, and genetics of STR markers. Academic Press, Massachusetts

    Google Scholar 

  • Carson EW, Beasley RR, Jones KL, Lance SL, De Ma Lozano-Vilano L, Vela-Valladares L, Banda-Villanueva I, Turner TF, De la Maza-Benignos M (2013) Development of polymorphic microsatellite markers for the microendemic pupfishes Cyprinodon julimes and C. pachycephalus. Conserv Genet Resour 5:853–856

    Article  Google Scholar 

  • Castoe TA, Poole AW, De Koning AP, Jones KL, Tomback DF, Oyler-McCance SJ, Fike JA, Lance SL, Streicher JW, Smith EN, Pollock DD (2012) Rapid microsatellite identification from Illumina paired-end genomic sequencing in two birds and a snake. PLoS One 7:e30953

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • Chavanne H, Janssen K, Hofherr J, Contini F, Haffray P, Komen H, Nielsen EE, Bargelloni L (2016) A comprehensive survey on selective breeding programs and seed market in the European aquaculture fish industry. Aquac Int 24:1287–1307

    Article  Google Scholar 

  • Che R, Sun Y, Sun D, Xu T (2014) Characterization of the miiuy croaker (Miichthys miiuy) transcriptome and development of immune-relevant genes and molecular markers. PLoS One 9:e94046

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen SL, Liu YG, Xu MY, Li J (2005) Isolation and characterization of polymorphic microsatellite loci from and EST-library of red sea bream (Chrysophrys major) and cross-species amplification. Mol Ecol Notes 5:215–217

    Article  CAS  Google Scholar 

  • Chen SL, Zhang YX, Xu MY, Ji XS, Yu GC, Dong CF (2006) Molecular polymorphism and expression analysis of MHC class II B gene from red sea bream (Chrysophrys major). Dev Comp Immunol 30:407–418

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Danzmann RG (2006) Linkage analysis package for outcrossed families with male or female exchange of the mapping parent, version 2.3. Available: http://www.uoguelph.ca/˜rdanzman/software/LINKMFEX

  • Danzmann RG, Cairney M, Davidson WS, Ferguson MM, Gharbi K, Guyomard R, Holm LE, Leder E, Okamoto N, Ozaki A, Rexroad CE III, Sakamoto T, Taggart JB, Woram RA (2005) A comparative analysis of the rainbow trout genome with 2 other species of fish (Arctic charr and Atlantic salmon) within the tetraploid derivative Salmonidae Family (subfamily: Salmoninae). Genome 48:1037–1051

    Article  CAS  PubMed  Google Scholar 

  • Das S, Sahoo PK (2014) Markers for selection of disease resistance in fish: a review. Aquac Int 22:1793–1812

    Article  CAS  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  PubMed Central  Google Scholar 

  • Franch R, Louro B, Tsalavouta M, Chatzoplis 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 

  • Fuji K, Kobayashi K, Hasegawa O, Coimbra MRM, 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 

  • Fuji K, Hasegawa O, Honda K, Kumasaka K, Sakamoto T, Okamoto N (2007) Marker-assisted breeding of a lymphocystis disease-resistant Japanese flounder (Paralichthys olivaceus). Aquaculture 272:291–295

    Article  Google Scholar 

  • Guo W, 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

    Article  Google Scholar 

  • Hatanaka A, Yamada S, Sakamoto T, Mitsuboshi T (2006) Isolation and application of microsatellite DNA markers for pedigree tracing of seedlings of red sea bream (Pagrus major). J World Aquacult Soc 37:139–143

    Article  Google Scholar 

  • Hauser L, Adcock GJ, Smith PJ, Ramirez JHB, Carvalho GR (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci 99:11742–11747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houston RD, Haley CS, Hamilton A, Guy DR, Mota-Velasco JC, Gheyas AA, Tinch AE, Taggart JB, Bron JE, Starkey WG, McAndrew BJ, Verner-Jeffreys DW, Paley RK, Rimmer GSE, Tew IJ, Bishop SC (2010) The susceptibility of Atlantic salmon fry to freshwater infectious pancreatic necrosis is largely explained by a major QTL. Heredity 105:318–327

    Article  CAS  PubMed  Google Scholar 

  • Imajo M, Ikawa T, Oshima S (2007) Characterization of a new fibroblast cell line from a tail fin of red sea bream, Pagrus major, and phylogenetic relationships of a recent RSIV isolate in Japan. Virus Res 126:45–52

    Article  Google Scholar 

  • Inami M, Hatanaka A, Mitsuboshi T, Yamada S, Tataushi A, Fukuda H, Sakamoto T (2005) A microsatellite linkage map of red sea bream (Pagrus major) and mapping of QTL markers associated with resistance to red sea bream iridovirus (RSIV). Plant Animal Genome XIII Abstracts. Available on http://www.intlpag.org/13/abstracts/PAG13_P607.html

  • Inouye K, Yamano K, Maeno Y, Nakajima K, Matsuoka M, Wada Y, Sorimachi M (1992) Iridovirus infection of cultured red sea bream, Pagrus major. Fish Pathol 27:19–27. (in Japanese with English abstract)

    Article  Google Scholar 

  • Jiang L, Chu G, Zhang Q, Wang Z, Wang X, Zhai J, Yu H (2013) A microsatellite genetic linkage map of half smooth tongue sole (Cynoglossus semilaevis). Mar Genomics 9:17–23

    Article  PubMed  Google Scholar 

  • Kawakami H, Nakajima K (2002) Cultured fish affected by red sea bream iridoviral disease from 1996 to 2000. Fish Pathol 37:45–47. (in Japanese with English abstract)

    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 

  • Kim WS, Oh MJ, Jung SJ, Kim YJ, Kitamura SI (2005) Characterization of an iridovirus detected from cultured turbot Scophthalmus maximus in Korea. Dis Aquat Org 64:175–180

    Article  PubMed  Google Scholar 

  • Kjøglum S, Larsen S, Bakke HG, Grimholt U (2006) How specific MHC class I class II combinations affect disease resistance against infectious salmon anaemia in Atlantic salmon (Salmo salar). Fish Shellfish Immunol 21:431–441

    Article  PubMed  Google Scholar 

  • Li R, Yu C, Li Y, Lam T, Yiu S, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1965

    Article  CAS  PubMed  Google Scholar 

  • Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li H, Shan G, Kristiansen K, Li S, Yang H, Wang J, Wang J (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Sakamoto T, Kubota S, Okamoto N, Yamashita H, Takagi M, Shigenobu Y, Sugaya T, Nakamura Y, Sano M, Wuthisuthimethavee S, Ozaki A (2013) A genetic linkage map of kelp grouper (Epinephelus bruneus) based on microsatellite markers. Aquaculture 414–415:63–81

    Article  Google Scholar 

  • Lukacs MF, Harstad H, Grimholt U, Beetz-Sargent M, Cooper GA, Reid L, Bakke HG, Phillips RB, Miller KM, Davidson WS, Koop BF (2007) Genomic organization of duplicated major histocompatibility complex class I regions in Atlantic salmon (Salmo salar). BMC Genomics 8:251

    Article  PubMed  PubMed Central  Google Scholar 

  • Manly KF, Cudmore RH Jr, Meer JM (2001) Map manager QTX, crossplatform software for genetic mapping. Mamm Genome 12:930–932

    Article  CAS  PubMed  Google Scholar 

  • Massault C, Bovenhuis H, Haley C, de Koning DJ (2008) QTL mapping designs for aquaculture. Aquaculture 285:23–29

    Article  CAS  Google Scholar 

  • Miyashita S, Seoka M (2005) Red sea bream. In: Kumai H (ed) Aquaculture System 1 Koseisha Koseikaku, Tokyo, pp. 45–82 (in Japanese)

  • Moen T, Baranski M, Sonesson AK, Kjøglum S (2009) Confirmation and fine-mapping of a major QTL for resistance to infectious pancreatic necrosis in Atlantic salmon (Salmo salar): population-level associations between markers and trait. BMC Genomics 10:368

  • Moen T, Torgersen J, Santi N, Davidson WS, Baranski M, Ødegård J, Kjøglum S, Velle B, Kent M, Lubieniecki KP, Isdal E, Lien S (2015) Epithelial cadherin determines resistance to infectious pancreatic necrosis virus in Atlantic Salmon. Genetics 200(4):1313–1326

  • Moldal T, Bornø G (2015) Infectious pancreatic necrosis (IPN). In: Hjeltnes B, Walde C, Jensen BB, Haukaas A (ed) Fish health report 2015, The Norwegian Veterinary Institute, pp. 26–27

  • Nagaoka Y, Kabeya H, Onuma M, Kasai N, Okada K, Aida Y (1999) Ovine MHC class II DRB1 alleles associated with resistance or susceptibility to development of bovine leukemia virus-induced ovine lymphoma. Cancer Res 59:975–981

    CAS  PubMed  Google Scholar 

  • Nakajima K, Kurita J (2005) Red sea bream iridoviral disease. Virus 55:115–126. (in Japanese with English abstract)

    CAS  PubMed  Google Scholar 

  • Nakajima K, Maeno Y, Kuruta J, Inui Y (1999) Vaccination against red sea bream iridoviral disease in red sea bream. Fish Pathol 32:205–209

    Article  Google Scholar 

  • Nomura K, Ozaki A, Morishima K, Yoshikawa Y, Tanaka H, Unuma T, Ohta H, Araki K (2011) A genetic linkage map of the Japanese eel (Anguilla japonica) based on AFLP and microsatellite markers. Aquaculture 310:329–342

    Article  CAS  Google Scholar 

  • Ojima Y, Yamamoto K (1990) Cellular DNA contents of fishes determined by flow cytometry. La Kromosomo 57:1871–1888

    Google Scholar 

  • Ozaki A, Khoo S, Yoshiura Y, Ototake M, Sakamoto T, Dijkstra JM, Okamoto N (2007) Identification of additional quantitative trait loci (QTL) responsible for susceptibility to infectious pancreatic necrosis virus in rainbow trout. Fish Pathol 42:131–140

    Article  Google Scholar 

  • Ozaki A, Okamoto H, Yamada T, Matsuyama T, Sakai T, Fuji K, Sakamoto T, Okamoto N, Yoshida K, Hatori K, Araki K, Okauchi M (2010) Linkage analysis of resistance to Streptococcus iniae infection in Japanese flounder (Paralichthys olivaceus). Aquaculture 308:S62–S67

    Article  CAS  Google Scholar 

  • Ozaki A, Yoshida K, Fuji K, Kubota S, Kai W, Aoki JY, Kawabata Y, Suzuki J, Akita K, Koyama T, Nakagawa M, Hotta T, Tsuzaki T, Okamoto N, Araki K, Sakamoto T (2013) Quantitative trait loci (QTL) associated with resistance to a monogenean parasite (Benedenia seriolae) in yellowtail (Seriola quinqueradiata) through genome wide analysis. PLoS One 8:e64987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rexroad CE III, Palti Y, Gahr SA, Vallejo RL (2008) A second generation genetic map for rainbow trout (Oncorhynchus mykiss). BMC Genet 9:74

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodrigues MDN, Moreira CGA, Gutierrez HJP, Almeida DB, Junoir DS, Moreira HLM (2015) Development of microsatellite markers for use in breeding catfish, Rhamdia sp. Afr J Biotechnol 14:400–411

    Article  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–396

    Google Scholar 

  • Ruan X, Wang W, Kong J, Yu F, Huang X (2010) Genetic linkage mapping of turbot (Scophthalmus maximus L.) using microsatellite markers and its application in QTL analysis. Aquaculture 308:89–100

    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 

  • Sambrook JG, Figueroa F, Beck S (2005) A genome-wide survey of major histocompatibility complex (MHC) genes and their paralogues in zebrafish. BMC Genomics 6:152

    Article  PubMed  PubMed Central  Google Scholar 

  • Sawayama E, Takagi M (2011) Genetic factors associated with transparency of juvenile red sea bream, Pagrus major. Nippon Suisan Gakkaishi 77:630–638. (in Japanese with English abstract)

    Article  Google Scholar 

  • Sawayama E, Takagi M (2015) Parental contribution and growth hormone gene polymorphism associated with growth phenotypes of red sea bream Pagrus major in mass production: a case study. Aquac Rep 2:144–151

    Article  Google Scholar 

  • Sawayama E, Takagi M (2016) Genetic diversity and structure of domesticated strains of red sea bream, Pagrus major, inferred from microsatellite DNA markers. Aquac Res 47:379–389

    Article  CAS  Google Scholar 

  • Sawayama E, Takagi M (2017) Evaluation of an RSIVD-resistant trait of red sea bream Pagrus major broodstock using DNA-based pedigree tracings: a field study. Fish Pathol 52:23–30

    Article  Google Scholar 

  • Sharif S, Mallard BA, Sargeant JM (2000) Presence of glutamine at position 74 of pocket 4 in the BoLA-DR antigen binding groove is associated with occurrence of clinical mastitis caused by Staphylococcus species. Vet Immunol Immunopathol 76:231–238

    Article  CAS  PubMed  Google Scholar 

  • Smith R, Sheppard K, DiPetrillo K, Churchill G (2009) Quantitative trait locus analysis using J/qtl. Methods Mol Biol 573:175–188

    Article  CAS  PubMed  Google Scholar 

  • Takagi M, Taniguchi N, Cook D, Doyle RW (1997) Isolation and characterization of microsatellite loci from red sea bream Pagrus major and detection in closely related species. Fish Sci 63:199–204

    Article  CAS  Google Scholar 

  • Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11:1441–1452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thevasagayam NM, Sridatta PSR, Jiang J, Tong A, Saju JM, Kathiresan P, Kwan HY, Ngoh SY, Liew WC, Kuznetsova IS, Shen X, Lok S, Vij S, Orbán L (2015) Transcriptome survey of a marine food fish: Asian seabass (Lates calcarifer). J Mar Sci Eng 3:382–400

    Article  Google Scholar 

  • Uchino T, Nakamura Y, Sekino M, Kai W, Fujiwara A, Yasuike M, Sugaya T, Fukuda H, Sano M, Sakamoto T (2016) Constructing genetic linkage maps using the whole genome sequence of Pacific bluefin tuna and a comparison of chromosome structure among teleost species. Adv Biosci Biotechnol 7:85–122

    Article  CAS  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wynne JW, Cook MT, Nowak BF, Eliot NG (2007) Major histocompatibility polymorphism associated with resistance towards amoebic gill disease in Atlantic salmon (Salmo salar L.) Fish Shellfish Immunol 22:707–717

    Article  CAS  PubMed  Google Scholar 

  • Xia JH, Liu F, Zhu ZY, Fu J, Feng J, Li J, Yue GH (2010) A consensus linkage map of the grass carp (Ctenopharyngodon idella) based on microsatellites and SNPs. BMC Genomics 11:135

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu T, Chen S, Ji X, Tian Y (2008) MHC polymorphism and disease resistance to Vibrio anguillarum in 12 selective Japanese flounder (Paralichthys olivaceus) families. Fish Shellfish Immunol 25:213–221

    Article  CAS  PubMed  Google Scholar 

  • Ye H, Liu Y, Liu X, Wang X, Wang Z (2014) Genetic mapping and QTL analysis of growth traits in the large yellow croaker Larimichthys crocea. Mar Biotechnol 16:729–738

    Article  CAS  PubMed  Google Scholar 

  • Yue GH (2013) Recent advances of genome mapping and marker-assisted selection in aquaculture. Fish Fish 15:376–396

    Article  Google Scholar 

  • Zerva L, Cizman B, Mehra NK, Alahari SK, Murali R, Zmijewski CM, Kamoun M, Monos DS (1996) Arginine at positions 13 or 70-71 in pocket 4 of HLA-DRB1 alleles is associated with susceptibility to tuberculoid leprosy. J Exp Med 183:829–836

    Article  CAS  PubMed  Google Scholar 

  • Zou M, Zhang X, Shi Z, Lin L, Ouyang G, Zhang G, Zheng H, Wei K, Ji W (2015) A comparative transcriptome analysis between wild and albino yellow catfish (Pelteobagrus fulvidraco). PLoS One 10:e0131504

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all the staff of Marua Suisan Co., Ltd. for collecting fish samples. We also thank Dr. Sonoko Shimizu for her kind help during the challenge tests, Mr. Shintaro Urasaki for collecting the spleens of RSIVD-infected fish, and Dr. Satoshi Kubota for useful advice on estimating genome coverage of the linkage maps. We also thank Dennis Murphy for editing this manuscript. This work was partly supported by grants from the Ehime Industrial Promotion Foundation and Ehime University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eitaro Sawayama.

Ethics declarations

Ethical Statement

All experiments described in this study were carried out in accordance with the Guide for the Care and Use of Laboratory Animals from Ehime University.

Electronic supplementary material

ESM 1

(XLSX 81 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sawayama, E., Tanizawa, S., Kitamura, SI. et al. Identification of Quantitative Trait Loci for Resistance to RSIVD in Red Sea Bream (Pagrus major). Mar Biotechnol 19, 601–613 (2017). https://doi.org/10.1007/s10126-017-9779-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-017-9779-z

Keywords

Navigation