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Marine Biotechnology

, Volume 21, Issue 2, pp 262–275 | Cite as

Constructing a High-Density Genetic Linkage Map for Large Yellow Croaker (Larimichthys crocea) and Mapping Resistance Trait Against Ciliate Parasite Cryptocaryon irritans

  • Shengnan Kong
  • Qiaozhen Ke
  • Lin Chen
  • Zhixiong Zhou
  • Fei Pu
  • Ji Zhao
  • Huaqiang Bai
  • Wenzhu Peng
  • Peng XuEmail author
Original Article

Abstract

The large yellow croaker (Larimichthys crocea) is the most economically important marine cage-farming fish in China in the past decade. However, the sustainable development of large yellow croaker aquaculture has been severely hampered by several diseases, of which, the white spot disease caused by ciliate protozoan parasite Cryptocaryon irritans ranks the most damaging disease in large yellow croaker cage farms. To better understand the genetic basis of parasite infection and disease resistance to C. irritans, it is vital to map the traits and localize the underlying candidate genes in L. crocea genome. Here, we constructed a high-density genetic linkage map using double-digest restriction-site associated DNA (ddRAD)-based high-throughput SNP genotyping data of a F1 mapping family, which had been challenged with C. irritans for resistant trait measure. A total of 5261 SNPs was grouped and oriented into 24 linkage groups (LGs), representing 24 chromosomes of L. crocea. The total genetic map length was 1885.67 cM with an average inter-locus distance of 0.36 cM. Quantitative trait loci (QTL) mapping identified seven significant QTLs in four LGs linked to C. irritans disease resistance. Candidate genes underlying disease resistance were identified from the reference genome, including ifnar1, ifngr2, ikbke, and CD112. Comparative genomic analysis between large yellow croaker and the four closely related species revealed high evolutionary conservation of chromosomes, though inter-chromosomal rearrangements do exist. Especially, the croaker genome structure was closer to the medaka genome than stickleback, indicating that the croaker genome might retain the teleost ancestral genome structure. The high-density genetic linkage map provides an important tool and resource for fine mapping, comparative genome analysis, and molecular selective breeding of large yellow croaker.

Keywords

Large yellow croaker Genetic linkage map Comparative genomic QTL Cryptocaryon irritans 

Notes

Author Contributions

PX conceived of the project. PX contributed to the funding acquisition. SK wrote the manuscript. SK, LC, and WP performed the analysis and designed the charts and tables. QK, JZ, and HB conducted the C. irritans challenge experiment. ZZ and FP conducted the ddRAD libraries. All authors have validated the manuscript and appreciate to improve the quality of it.

Funding Information

We acknowledge the financial support from the State Key Laboratory of Large Yellow Croaker Breeding (Fujian Fuding Seagull Fishing Food Co., Ltd.) (LYC2017RS05 and LYC2017ZY01), the Fundamental Research Funds for the Central Universities of Xiamen University (Nos. 20720180123 and 20720160110), the Science and Technology Platform Construction of Fujian Province (No. 2018 N2005), the Local Science and Technology Development Project Guide by The Central Government (2017L3019), and the Natural Science Foundation of Fujian Province (Grant No. 2017 J06022).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interests.

Supplementary material

10126_2019_9878_MOESM1_ESM.xlsx (178 kb)
ESM 1 (XLSX 177 kb)
10126_2019_9878_MOESM2_ESM.txt (2.3 mb)
ESM 2 (TXT 2364 kb)

References

  1. Abernathy JW, Xu P, Li P, Xu D-H, Kucuktas H, Klesius P, Arias C, Liu Z (2007) Generation and analysis of expressed sequence tags from the ciliate protozoan parasite Ichthyophthirius multifiliis. BMC Genomics 8:176CrossRefGoogle Scholar
  2. Andrey S, Eyal S, Avner C, Howe AE, Raisa D, Noam Z, Kocher TD, Gideon H, Micha R (2006) Amh and Dmrta2 genes map to tilapia (Oreochromis spp.) linkage group 23 within quantitative trait locus regions for sex determination. Genetics 174:1573–1581CrossRefGoogle Scholar
  3. Ao J, Li J, You X, Mu Y, Ding Y, Mao K, Bian C, Mu P, Shi Q, Chen X (2015a) Construction of the high-density genetic linkage map and chromosome map of large yellow croaker (Larimichthys crocea). Int J Mol Sci 16:26237–26248CrossRefGoogle Scholar
  4. Ao J, Mu Y, Xiang L-X, Fan D, Feng M, Zhang S, Shi Q, Zhu L-Y, Li T, Ding Y, Nie L, Li Q, Dong W-R, Jiang L, Sun B, Zhang X, Li M, Zhang H-Q, Xie S, Zhu Y, Jiang X, Wang X, Mu P, Chen W, Yue Z, Wang Z, Wang J, Shao J-Z, Chen X (2015b) Genome sequencing of the perciform fish Larimichthys crocea provides insights into molecular and genetic mechanisms of stress adaptation. PLoS Genet 11:e1005118CrossRefGoogle Scholar
  5. Baury B, Masson D, Mcdermott BM, Jarry A, Blottière HM, Blanchardie P, Laboisse CL, Lustenberger P, Racaniello VR, Denis MG (2003) Identification of secreted CD155 isoforms. Biochem Biophys Res Commun 309:175–182CrossRefGoogle Scholar
  6. Berthier-Schaad Y, Kao WHL, Coresh J, Zhang L, Ingersoll RG, Stephens R, Smith MW (2010) Reliability of high-throughput genotyping of whole genome amplified DNA in SNP genotyping studies. Electrophoresis 28:2812–2817CrossRefGoogle Scholar
  7. Bradley KM, Breyer JP, Melville DB, Broman KW, Knapik EW, Smith JR (2011) An SNP-based linkage map for zebrafish reveals sex determination loci. G3 (Bethesda) 1:3–9CrossRefGoogle Scholar
  8. Cantin E, Tanamachi B, Openshaw H, Mann J, Clarke K (1999) Gamma interferon (IFN-gamma) receptor null-mutant mice are more susceptible to herpes simplex virus type 1 infection than IFN-gamma ligand null-mutant mice. J Virol 73:5196–5200Google Scholar
  9. Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140CrossRefGoogle Scholar
  10. Chen L, Peng W, Kong S, Pu F, Chen B, Zhou Z, Feng J, Li X, Xu P (2018) Genetic mapping of head size related traits in common carp (Cyprinus carpio). Front Genet 9.  https://doi.org/10.3389/fgene.2018.00448
  11. De LPF, Calvopinilla E, Lópezgil E, Marínlópez A, Mateos F, Castilloolivares J, Lorenzo G, Ortego J (2013) Ns1 is a key protein in the vaccine composition to protect Ifnar(-/-) mice against infection with multiple serotypes of African horse sickness virus. PLoS One 8:e70197CrossRefGoogle Scholar
  12. 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 272:291–295CrossRefGoogle Scholar
  13. Geng X, Sha J, Liu S, Bao L, Zhang J, Wang R, Yao J, Li C, Feng J, Sun F, Sun L, Jiang C, Zhang Y, Chen A, Dunham R, Zhi D, Liu Z (2015) A genome-wide association study in catfish reveals the presence of functional hubs of related genes within QTLs for columnaris disease resistance. BMC Genomics 16:196CrossRefGoogle Scholar
  14. Geng X, Liu S, Yuan Z, Jiang Y, Zhi D, Liu Z (2017) A genome-wide association study reveals that genes with functions for bone development are associated with body conformation in catfish. Mar Biotechnol 19:570–578CrossRefGoogle Scholar
  15. Gilfillan S, Chan CJ, Cella M, Haynes NM, Rapaport AS, Boles KS, Andrews DM, Smyth MJ, Colonna M (2008) DNAM-1 promotes activation of cytotoxic lymphocytes by nonprofessional antigen-presenting cells and tumors. J Exp Med 205:2965–2973CrossRefGoogle Scholar
  16. 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 15:166CrossRefGoogle Scholar
  17. Gu XH, Jiang DL, Huang Y, Li BJ, Chen CH, Lin HR, Xia JH (2018) Identifying a major QTL associated with salinity tolerance in Nile Tilapia using QTL-Seq. Mar Biotechnol 20:98–107CrossRefGoogle Scholar
  18. Guyon R, Rakotomanga M, Azzouzi N, Coutanceau JP, Bonillo C, D’cotta H, Pepey E, Soler L, Rodier-Goud M, D’hont A (2012) A high-resolution map of the Nile tilapia genome: a resource for studying cichlids and other percomorphs. BMC Genomics 13:222–222CrossRefGoogle Scholar
  19. Iguchimanaka A, Kai H, Yamashita Y, Kai S, Taharahanaoka S, Honda S, Yasui T, Kikutani H, Shibuya K, Shibuya A (2008) Accelerated tumor growth in mice deficient in DNAM-1 receptor. J Exp Med 205:2959–2964CrossRefGoogle Scholar
  20. Ivashkiv LB, Donlin LT (2014) Regulation of type I interferon responses. Nat Rev Immunol 14:36–49CrossRefGoogle Scholar
  21. Jabbar TK, Calvo-Pinilla E, Mateos F, Gubbins S, Bin-Tarif A, Bachanek-Bankowska K, Alpar O, Ortego J, Takamatsu HH, Mertens PP (2013) Protection of IFNAR (-/-) mice against bluetongue virus serotype 8, by heterologous (DNA/rMVA) and homologous (rMVA/rMVA) vaccination, expressing outer-capsid protein VP2. PLoS One 8:e60574CrossRefGoogle Scholar
  22. Jian J, Wu Z (2003) Effects of traditional Chinese medicine on nonspecific immunity and disease resistance of large yellow croaker, Pseudosciaena crocea (Richardson). Aquaculture 218:1–9CrossRefGoogle Scholar
  23. Kasahara M, Naruse K, Sasaki S, Nakatani Y, Qu W, Ahsan B, Yamada T, Nagayasu Y, Doi K, Kasai Y (2007) The medaka draft genome and insights into vertebrate genome evolution. Nature 447:714–719CrossRefGoogle Scholar
  24. Kocher TD, Lee WJ, Sobolewska H, Penman D, Mcandrew B (1998) A genetic linkage map of a cichlid fish, the tilapia (Oreochromis niloticus). Genetics 148:1225–1232Google Scholar
  25. Kosambi DD (1943) The estimation of map distance from recombination values. Ann Eugenics 12:172–175CrossRefGoogle Scholar
  26. Krause CD, Pestka S (2005) Evolution of the class 2 cytokines and receptors, and discovery of new friends and relatives. Pharmacol Ther 106:299–346CrossRefGoogle Scholar
  27. Krzywinski M, Schein JI (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645CrossRefGoogle Scholar
  28. Kucuktas H, Wang S, Li P, He C, Xu P, Sha Z, Liu H, Jiang Y, Baoprasertkul P, Somridhivej B (2009) Construction of genetic linkage maps and comparative genome analysis of catfish using gene-associated markers. Genetics 181:1649–1660CrossRefGoogle Scholar
  29. Kujur A, Upadhyaya HD, Shree T, Bajaj D, Das S, Saxena MS, Badoni S, Kumar V, Tripathi S, Gowda CL (2015) Ultra-high density intra-specific genetic linkage maps accelerate identification of functionally relevant molecular tags governing important agronomic traits in chickpea. Sci Rep 5:9468CrossRefGoogle Scholar
  30. Le W, Zi YW, Bai B, Shu QH, Chua E, Lee M, Hong YP, Yan FW, Peng L, Feng L (2015) Construction of a high-density linkage map and fine mapping of QTL for growth in Asian seabass. Sci Rep 5:16358CrossRefGoogle Scholar
  31. Li Y-W, Luo X-C, Dan X-M, Huang X-Z, Qiao W, Zhong Z-P, Li A-X (2011) Orange-spotted grouper (Epinephelus coioides) TLR2, MyD88 and IL-1β involved in anti-Cryptocaryon irritans response. Fish Shellfish Immunol 30:1230–1240CrossRefGoogle Scholar
  32. Li HL, Gu XH, Li BJ, Chen CH, Lin HR, Xia JH (2017) Genome-wide QTL analysis identified significant associations between hypoxia tolerance and mutations in the GPR132 and ABCG4 genes in Nile Tilapia. Mar Biotechnol 19:441–453CrossRefGoogle Scholar
  33. Lin G, Wang L, Ngoh ST, Ji L, Orbán L, Yue GH (2018) Mapping QTL for omega-3 content in hybrid saline Tilapia. Mar Biotechnol 20:10–19CrossRefGoogle Scholar
  34. 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 14:1–14CrossRefGoogle Scholar
  35. Meyer A, Van De Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 27:937–945CrossRefGoogle Scholar
  36. Mori M, Rikitake Y, Mandai K, Takai Y (2014) Roles of nectins and nectin-like molecules in the nervous system. Adv Neurobiol 8:91CrossRefGoogle Scholar
  37. Naruse K, Fukamachi S, Mitani H, Kondo M, Matsuoka T, Shu K, Hanamura N, Morita Y, Hasegawa K, Nishigaki R (2000) A detailed linkage map of medaka, Oryzias latipes: comparative genomics and genome evolution. Genetics 154:1773–1784Google Scholar
  38. Nichols KM, Jerri B, Thorgaard GH (2003) Mapping multiple genetic loci associated with Ceratomyxa shasta resistance in Oncorhynchus mykiss. Dis Aquat Org 56:145–154CrossRefGoogle Scholar
  39. Ning Y, Liu X, Wang ZY, Guo W, Li Y, Xie F (2007) A genetic map of large yellow croaker Pseudosciaena crocea. Aquaculture 264:16–26CrossRefGoogle Scholar
  40. Niu S-F, Jin Y, Xu X, Qiao Y, Wu Y, Mao Y, Su Y-Q, Wang J (2013) Characterization of a novel piscidin-like antimicrobial peptide from Pseudosciaena crocea and its immune response to Cryptocaryon irritans. Fish Shellfish Immunol 35:513–524CrossRefGoogle Scholar
  41. Niu D, Du Y, Wang Z, Xie S, Nguyen H, Dong Z, Shen H, Li J (2017) Construction of the first high-density genetic linkage map and analysis of quantitative trait loci for growth-related traits in Sinonovacula constricta. Mar Biotechnol 19:488–496CrossRefGoogle Scholar
  42. Palaiokostas C, Bekaert M, Davie A, Cowan ME, Oral M, Taggart JB, Gharbi K, Mcandrew BJ, Penman DJ, Migaud H (2013) Mapping the sex determination locus in the Atlantic halibut (Hippoglossus hippoglossus) using RAD sequencing. BMC Genomics 14:566CrossRefGoogle Scholar
  43. Peichel CL, Nereng KS, Ohgi KA, Cole BLE, Colosimo PF, Buerkle CA, Schluter D, Kingsley DM (2001) The genetic architecture of divergence between three spine stickleback species. Nature 414:901–905CrossRefGoogle Scholar
  44. Pende D, Bottino C, Castriconi R, Cantoni C, Marcenaro S, Rivera P, Spaggiari GM, Dondero A, Carnemolla B, Reymond N (2005) PVR (CD155) and Nectin-2 (CD112) as ligands of the human DNAM-1 (CD226) activating receptor: involvement in tumor cell lysis. Mol Immunol 42:463–469CrossRefGoogle Scholar
  45. Peng W, Xu J, Zhang Y, Feng J, Dong C, Jiang L, Feng J, Chen B, Gong Y, Chen L (2016) An ultra-high density linkage map and QTL mapping for sex and growth-related traits of common carp (Cyprinus carpio). Sci Rep 6:26693CrossRefGoogle Scholar
  46. 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:e37135CrossRefGoogle Scholar
  47. Rastas P, Paulin L, Hanski I, Lehtonen R, Auvinen P (2013) Lep-MAP: fast and accurate linkage map construction for large SNP datasets. Bioinformatics 29:3128–3134CrossRefGoogle Scholar
  48. Sambrook J, Fritsch EF, Maniatis T (eds) (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York. (in 3 volumes)Google Scholar
  49. Sawayama E, Tanizawa S, Kitamura S-I, Nakayama K, Ohta K, Ozaki A, Takagi M (2017) Identification of quantitative trait loci for resistance to RSIVD in Red Sea bream (Pagrus major). Mar Biotechnol 19:601–613CrossRefGoogle Scholar
  50. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM (2010) A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472:481–485CrossRefGoogle Scholar
  51. Shao C, Niu Y, Rastas P, Liu Y, Xie Z, Li H, Wang L, Jiang Y, Tai S, Tian Y (2015) Genome-wide SNP identification for the construction of a high-resolution genetic map of Japanese flounder (Paralichthys olivaceus): applications to QTL mapping of Vibrio anguillarum disease resistance and comparative genomic analysis. DNA Res 22(2):161–170CrossRefGoogle Scholar
  52. Shih VF-S, Tsui R, Caldwell A, Hoffmann A (2011) A single NFκB system for both canonical and non-canonical signaling. Cell Res 21:86–102CrossRefGoogle Scholar
  53. Smith PL, Lombardi G, Foster GR (2005) Type I interferons and the innate immune response—more than just antiviral cytokines. Mol Immunol 42:869–877CrossRefGoogle Scholar
  54. Song J, Li Q, Yu Y, Wan S, Han L, Du S (2018) Mapping genetic loci for quantitative traits of golden shell color, mineral element contents, and growth-related traits in Pacific oyster (Crassostrea gigas). Mar Biotechnol 20:666–675CrossRefGoogle Scholar
  55. Sun B, Greiner-Tollersrud L, Koop BF, Robertsen B (2014) Atlantic salmon possesses two clusters of type I interferon receptor genes on different chromosomes, which allows for a larger repertoire of interferon receptors than in zebrafish and mammals. Dev Comp Immunol 47:275–286CrossRefGoogle Scholar
  56. Taharahanaoka S, Miyamoto A, Hara A, Honda S, Shibuya K, Shibuya A (2005) Identification and characterization of murine DNAM-1 (CD226) and its poliovirus receptor family ligands. Biochem Biophys Res Commun 329:996–1000CrossRefGoogle Scholar
  57. Taharahanaoka S, Shibuya K, Kai H, Miyamoto A, Morikawa Y, Ohkochi N, Honda S, Shibuya A (2006) Tumor rejection by the poliovirus receptor family ligands of the DNAM-1 (CD226) receptor. Blood 107:1491–1496CrossRefGoogle Scholar
  58. Takai Y, Miyoshi J, Ikeda W, Ogita H (2008) Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nat Rev Mol Cell Biol 9:603CrossRefGoogle Scholar
  59. Takeda H (2008) Draft genome of the medaka fish: a comprehensive resource for medaka developmental genetics and vertebrate evolutionary biology. Develop Growth Differ 50:S157–S166CrossRefGoogle Scholar
  60. Tenoever BR, Ng S-L, Chua MA, Mcwhirter SM, García-Sastre A, Maniatis T (2007) Multiple functions of the IKK-related kinase IKKε in interferon-mediated antiviral immunity. Science 315:1274–1278CrossRefGoogle Scholar
  61. Tsai HY, Hamilton A, Tinch AE, Guy DR, Bron JE, Taggart JB, Gharbi K, Stear M, Matika O, Pong-Wong R (2016) Genomic prediction of host resistance to sea lice in farmed Atlantic salmon populations. Genet Sel Evol 48:47CrossRefGoogle Scholar
  62. Van Ooijen JW (2011) Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet Res 93:343–349CrossRefGoogle Scholar
  63. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78CrossRefGoogle Scholar
  64. Wang L, Wan ZY, Bai B, Huang SQ, Chua E, Lee M, Pang HY, Wen YF, Liu P, Liu F, Sun F, Lin G, Ye BQ, Yue GH (2015) Construction of a high-density linkage map and fine mapping of QTL for growth in Asian seabass. Sci Rep 5:16358 https://www.nature.com/articles/srep16358#supplementary-information. Accessed 18 Jan 2019
  65. Wang L, Bai B, Huang S, Liu P, Wan ZY, Ye B, Wu J, Yue GH (2017) QTL mapping for resistance to Iridovirus in Asian seabass using genotyping-by-sequencing. Mar Biotechnol 19:517–527CrossRefGoogle Scholar
  66. Wu C, Zhang D, Kan M, Lv Z, Zhu A, Su Y, Zhou D, Zhang J, Zhang Z, Xu M (2014) The draft genome of the large yellow croaker reveals well-developed innate immunity. Nat Commun 5:5227CrossRefGoogle Scholar
  67. Xiao S, Wang P, Yan Z, Fang L, Yang L, Li JT, Wang ZY (2015) Gene map of large yellow croaker (Larimichthys crocea) provides insights into teleost genome evolution and conserved regions associated with growth. Sci Rep 5:18661CrossRefGoogle Scholar
  68. Xu J, Zhao Z, Zhang X, Zheng X, Li J, Jiang Y, Kuang Y, Zhang Y, Feng J, Li C, Yu J, Li Q, Zhu Y, Liu Y, Xu P, Sun X (2014a) Development and evaluation of the first high-throughput SNP array for common carp (Cyprinus carpio). BMC Genomics 15:307CrossRefGoogle Scholar
  69. Xu P, Zhang X, Wang X, Li J, Liu G, Kuang Y, Xu J, Zheng X, Ren L, Wang G, Zhang Y, Huo L, Zhao Z, Cao D, Lu C, Li C, Zhou Y, Liu Z, Fan Z, Shan G, Li X, Wu S, Song L, Hou G, Jiang Y, Jeney Z, Yu D, Wang L, Shao C, Song L, Sun J, Ji P, Wang J, Li Q, Xu L, Sun F, Feng J, Wang C, Wang S, Wang B, Li Y, Zhu Y, Xue W, Zhao L, Wang J, Gu Y, Lv W, Wu K, Xiao J, Wu J, Zhang Z, Yu J, Sun X (2014b) Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nat Genet 46:1212 https://www.nature.com/articles/ng.3098#supplementary-information. Accessed 18 Jan 2019CrossRefGoogle Scholar
  70. 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 16:729–738CrossRefGoogle Scholar
  71. Ying Q, Yong M, Wang J, Chen R, Su YQ, Jia C, Zheng WQ (2016) Analysis of liver and gill miRNAs of Larimichthys crocea against Cryptocryon irritans challenge. Fish Shellfish Immunol 59:484–491CrossRefGoogle Scholar
  72. Yu Y, Zhang X, Yuan J, Wang Q, Li S, Huang H, Li F, Xiang J (2017) Identification of sex-determining loci in Pacific white shrimp Litopeneaus vannamei using linkage and association analysis. Mar Biotechnol 19:277–286CrossRefGoogle Scholar
  73. Yue GH (2014) Recent advances of genome mapping and marker-assisted selection in aquaculture. Fish Fish 15:376–396CrossRefGoogle Scholar
  74. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214CrossRefGoogle Scholar
  75. Zhang X, Zhang Y, Zheng X, Kuang Y, Zhao Z, Zhao L, Li C, Jiang L, Cao D, Lu C (2013) A consensus linkage map provides insights on genome character and evolution in common carp (Cyprinus carpio L.). Mar Biotechnol 15:275–312CrossRefGoogle Scholar
  76. Zhao L, Zhang Y, Ji P, Zhang X, Zhao Z, Hou G, Huo L, Liu G, Li C, Xu P (2013) A dense genetic linkage map for common carp and its integration with a BAC-based physical map. PLoS One 8:e63928CrossRefGoogle Scholar
  77. Zhong X, Wang X, Zhou T, Jin Y, Tan S, Jiang C, Geng X, Li N, Shi H, Zeng Q, Yang Y, Yuan Z, Bao L, Liu S, Tian C, Peatman E, Li Q, Liu Z (2017) Genome-wide association study reveals multiple novel QTL associated with low oxygen tolerance in hybrid catfish. Mar Biotechnol 19:379–390CrossRefGoogle Scholar
  78. Zhou X, Stephens M (2012) Genome-wide efficient mixed model analysis for association studies. Nat Genet 44:821–824CrossRefGoogle Scholar
  79. Zhou H, Chen S, Wang M, Cheng A (2014a) Interferons and their receptors in birds: a comparison of gene structure, phylogenetic analysis, and cross modulation. Int J Mol Sci 15:21045CrossRefGoogle Scholar
  80. Zhou Q-J, Su Y-Q, Niu S-F, Liu M, Qiao Y, Wang J (2014b) Discovery and molecular cloning of piscidin-5-like gene from the large yellow croaker (Larimichthys crocea). Fish Shellfish Immunol 41:417–420CrossRefGoogle Scholar
  81. Zhou T, Liu S, Geng X, Jin Y, Jiang C, Bao L, Yao J, Zhang Y, Zhang J, Sun L (2017) GWAS analysis of QTL for enteric septicemia of catfish and their involved genes suggest evolutionary conservation of a molecular mechanism of disease resistance. Mol Genet Genomics 292:231–242CrossRefGoogle Scholar
  82. Zhou Z, Chen L, Dong C, Peng W, Kong S, Sun J, Pu F, Chen B, Feng J, Xu P (2018) Genome-scale association study of abnormal scale pattern in Yellow River carp identified previously known causative gene in European Mirror carp. Mar Biotechnol 20:1–11CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.State Key Laboratory of Large Yellow Croaker BreedingNingde Fufa Fisheries Company LimitedNingdeChina
  2. 2.State Key Laboratory of Marine Environmental Science, College of Ocean and Earth SciencesXiamen UniversityXiamenChina
  3. 3.College of FisheriesHenan Normal UniversityXinxiangChina
  4. 4.Laboratory for Marine Biology and BiotechnologyQingdao National Laboratory for Marine Science and TechnologyQingdaoChina

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