Advertisement

Science China Life Sciences

, Volume 61, Issue 8, pp 934–946 | Cite as

A genome-wide association study on growth traits in orange-spotted grouper (Epinephelus coioides) with RAD-seq genotyping

  • Hui Yu
  • Xinxin You
  • Jia Li
  • Xinhui Zhang
  • Shuai Zhang
  • Shoujia Jiang
  • Xueqiang Lin
  • Hao-Ran Lin
  • Zining Meng
  • Qiong Shi
Research Paper

Abstract

The orange-spotted grouper, Epinephelus coioides, is one of the most popular fish in China and Southeast Asian countries because of its important economic value. However, molecular mechanism underlying the growth of orange-spotted grouper has never been fully understood. Herein, we performed a genome-wide association study (GWAS) on a natural population of 198 individuals aiming to screen the whole genome of orange-spotted grouper for identification of growth-related loci by restrictionsite associated DNA sequencing. In this research, 261,366 single nucleotide polymorphisms (SNPs) were developed, in which 110 SNPs were identified to be correlated with growth and 20 SNPs were further confirmed to be associated with both body weight and total length. From these identified SNPs, we annotated a total of 34 genes, including adgrb2, csnkza1, cers5, col22a1, creb5, dnd1, dzank1, dnai1, npy2r, fat3, lrrk2, lrp5, map3k9, and so on. Among these candidate genes, npy2r (neuropeptide Y receptor Y2) was reported to play a critical role in growth of the orange-spotted grouper. In addition, population structure, principal component analysis, kinship matrix and linkage disequilibrium were examined to verify the accuracy and reliability of our GWAS results. Our data will also provide a valuable genetic resource for further marker-assisted selection program to improve growth quality in groupers.

Keywords

orange-spotted grouper genome-wide association study (GWAS) restriction-site associated DNA sequencing (RAD-seq) growth traits npy2r 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

We thank Dr. Yong Zhang, a genetic Professor at Sun Yat-Sen University, for sharing the reference genome sequence of orange-spotted grouper. The work was supported by National Natural Science Foundation of China (31370047), Shenzhen Scientific R&D Grant (GJHS20160331150703934) and Shenzhen Dapeng Special Program for Industrial Development (KY20160102, KY20170205).

Supplementary material

11427_2017_9161_MOESM1_ESM.pdf (193 kb)
Supplementary material, approximately 193 KB.
11427_2017_9161_MOESM2_ESM.pdf (34 kb)
Supplementary material, approximately 34.2 KB.
11427_2017_9161_MOESM3_ESM.pdf (109 kb)
Supplementary material, approximately 108 KB.
11427_2017_9161_MOESM4_ESM.xlsx (7.1 mb)
Supplementary material, approximately 7.14 MB.
11427_2017_9161_MOESM5_ESM.xlsx (14 kb)
Supplementary material, approximately 14.2 KB.
11427_2017_9161_MOESM6_ESM.docx (16 kb)
Table S2 Pearson correlation coefficients for body weight and total length

References

  1. Babbucci, M., Ferraresso, S., Pauletto, M., Franch, R., Papetti, C., Patarnello, T., Carnier, P., and Bargelloni, L. (2016). An integrated genomic approach for the study of mandibular prognathism in the European seabass (Dicentrarchus labrax). Sci Rep 6, 38673.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Baird, N.A., Etter, P.D., Atwood, T.S., Currey, M.C., Shiver, A.L., Lewis, Z.A., Selker, E.U., Cresko, W.A., and Johnson, E.A. (2008). Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3, e3376.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Baxter, S.W., Davey, J.W., Johnston, J.S., Shelton, A.M., Heckel, D.G., Jiggins, C.D., and Blaxter, M.L. (2011). Linkage mapping and comparative genomics using next-generation RAD sequencing of a non-model organism. PLoS ONE 6, e19315.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Busov, V., Meilan, R., Pearce, D.W., Rood, S.B., Ma, C., Tschaplinski, T.J., and Strauss, S.H. (2006). Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profiles in Populus. Planta 224, 288–299.CrossRefPubMedGoogle Scholar
  5. Calabrese, G.M., Mesner, L.D., Stains, J.P., Tommasini, S.M., Horowitz, M.C., Rosen, C.J., and Farber, C.R. (2017). Integrating GWAS and coexpression network data identifies bone mineral density Genes SPTBN1 and MARK3 and an osteoblast functional module. Cell Syst 4, 46–59.e4.CrossRefPubMedGoogle Scholar
  6. Cameron, R.S., Liu, C., and Pihkala, J.P.S. (2013). Myosin 16 levels fluctuate during the cell cycle and are downregulated in response to DNA replication stress. Cytoskeleton 70, 328–348.CrossRefPubMedGoogle Scholar
  7. Campbell, N.R., LaPatra, S.E., Overturf, K., Towner, R., and Narum, S.R. (2014). Association mapping of disease resistance traits in rainbow trout using restriction site associated DNA sequencing. G3 4, 2473–2481.CrossRefPubMedGoogle Scholar
  8. Cardon, L.R., and Bell, J.I. (2001). Association study designs for complex diseases.. Nat Rev Genet 2, 91–99.CrossRefPubMedGoogle Scholar
  9. Carpio, Y., Acosta, J., Morales, A., Herrera, F., González, L.J., and Estrada, M.P. (2006). Cloning, expression and growth promoting action of Red tilapia (Oreochromis sp.) neuropeptide Y. Peptides 27, 710–718.CrossRefPubMedGoogle Scholar
  10. Chutimanitsakun, Y., Nipper, R.W., Cuesta-Marcos, A., Cistué, L., Corey, A., Filichkina, T., Johnson, E.A., and Hayes, P.M. (2011). Construction and application for QTL analysis of a restriction site associated DNA (RAD) linkage map in barley. BMC Genomics 12, 4.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Dadds, M.R., Moul, C., Cauchi, A., Hawes, D.J., and Brennan, J. (2013). Replication of a ROBO2 polymorphism associated with conduct problems but not psychopathic tendencies in children. Psychiatr Genet 23, 251–254.CrossRefPubMedGoogle Scholar
  12. Danzmann, R.G., and Gharbi, K. (2007). Linkage mapping in aquaculture species. In: Aquaculture Genome Technologies. (London: Blackwell Publishing Ltd.), pp. 139–167.CrossRefGoogle Scholar
  13. Davey, J.W., Hohenlohe, P.A., Etter, P.D., Boone, J.Q., Catchen, J.M., and Blaxter, M.L. (2011). Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12, 499–510.CrossRefPubMedGoogle Scholar
  14. Denisova, E., Heidenreich, B., Nagore, E., Rachakonda, P.S., Hosen, I., Akrap, I., Traves, V., García-Casado, Z., López-Guerrero, J.A., Requena, C., Sanmartin, O., Serra-Guillén, C., Llombart, B., Guillén, C., Ferrando, J., Gimeno, E., Nordheim, A., Hemminki, K., and Kumar, R. (2015). Frequent DPH3 promoter mutations in skin cancers. Oncotarget in press doi: 10.18632/oncotarget.5771.Google Scholar
  15. Dona, M., Bachmann-Gagescu, R., Texier, Y., Toedt, G., Hetterschijt, L., Tonnaer, E.L., Peters, T.A., van Beersum, S.E.C., Bergboer, J.G.M., Horn, N., de Vrieze, E., Slijkerman, R.W.N., van Reeuwijk, J., Flik, G., Keunen, J.E., Ueffing, M., Gibson, T.J., Roepman, R., Boldt, K., Kremer, H., and van Wijk, E. (2015). NINL and DZANK1 co-function in vesicle transport and are essential for photoreceptor development in zebrafish. PLoS Genet 11, e1005574.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Dong, L., Xiao, S., Wang, Q., and Wang, Z. (2016). Comparative analysis of the GBLUP, emBayesB, and GWAS algorithms to predict genetic values in large yellow croaker (Larimichthys crocea). BMC Genomics 17, 460.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Duan, Z., Sun, C., Shen, M.M., Wang, K., Yang, N., Zheng, J., and Xu, G. (2016). Genetic architecture dissection by genome-wide association analysis reveals avian eggshell ultrastructure traits. Sci Rep 6, 28836.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Dushyanth, K., Bhattacharya, T.K., Shukla, R., Chatterjee, R.N., Sitaramamma, T., Paswan, C., and Guru Vishnu, P. (2016). Gene expression and polymorphism of Myostatin gene and its association with growth traits in chicken. Animal Biotech 27, 269–277.CrossRefGoogle Scholar
  19. Eaton, D.A.R. (2014). PyRAD: assembly of de novo RADseq loci for phylogenetic analyses. Bioinformatics 30, 1844–1849.CrossRefPubMedGoogle Scholar
  20. 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., and 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, 196.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gonzalez-Pena, D., Gao, G., Baranski, M., Moen, T., Cleveland, B.M., Kenney, P.B., Vallejo, R.L., Palti, Y., and Leeds, T.D. (2016). Genomewide association study for identifying loci that affect fillet yield, carcass, and body weight traits in rainbow trout (Oncorhynchus mykiss). Front Genet 7, 203.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gorman, S.W., Haider, N.B., Grieshammer, U., Swiderski, R.E., Kim, E., Welch, J.W., Searby, C., Leng, S., Carmi, R., Sheffield, V.C., and Duhl, D.M. (1999). The cloning and developmental expression of unconventional myosin IXA (MYO9A) a gene in the Bardet-Biedl syndrome (- BBS4) region at chromosome 15q22–q23. Genomics 59, 150–160.CrossRefPubMedGoogle Scholar
  23. Gosejacob, D., Jäger, P.S., Vom Dorp, K., Frejno, M., Carstensen, A.C., Köhnke, M., Degen, J., Dörmann, P., and Hoch, M. (2016). Ceramide synthase 5 is essential to maintain C16:0-ceramide pools and contributes to the development of diet-induced obesity. J Biol Chem 291, 6989–7003.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Guichard, C., Harricane, M.C., Lafitte, J.J., Godard, P., Zaegel, M., Tack, V., Lalau, G., and Bouvagnet, P. (2001). Axonemal dynein intermediatechain gene (DNAI1) mutations result in situs inversus and primary ciliary dyskinesia (Kartagener Syndrome). Am J Hum Genet 68, 1030–1035.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Guo, L., Xia, J., Yang, S., Li, M., You, X., Meng, Z., and Lin, H. (2015). GHRH, PRP-PACAP and GHRHR target sequencing via an ion torrent personal genome machine reveals an association with growth in orangespotted grouper (Epinephelus coioides). Int J Mol Sci 16, 26137–26150.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gutierrez, A.P., Yáñez, J.M., Fukui, S., Swift, B., and Davidson, W.S. (2015). Genome-wide association study (GWAS) for growth rate and age at sexual maturation in atlantic salmon (Salmo salar). PLoS ONE 10, e0119730.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hamann, J., Aust, G., Araç, D., Engel, F.B., Formstone, C., Fredriksson, R., Hall, R.A., Harty, B.L., Kirchhoff, C., Knapp, B., Krishnan, A., Liebscher, I., Lin, H.H., Martinelli, D.C., Monk, K.R., Peeters, M.C., Piao, X., Prömel, S., Schöneberg, T., Schwartz, T.W., Singer, K., Stacey, M., Ushkaryov, Y.A., Vallon, M., Wolfrum, U., Wright, M.W., Xu, L., Langenhan, T., and Schiöth, H.B. (2015). International union of basic and clinical pharmacology. XCIV. Adhesion G protein-coupled receptors. Pharmacol Rev 67, 338–367.PubMedGoogle Scholar
  28. Han, K.M., Dharmawardhana, P., Arias, R.S., Ma, C., Busov, V., and Strauss, S.H. (2011). Gibberellin-associated cisgenes modify growth, stature and wood properties in Populus. Plant Biotech J 9, 162–178.CrossRefGoogle Scholar
  29. Hardy, J., and Singleton, A. (2009). Genomewide association studies and human disease. N Engl J Med 360, 1759–1768.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hecht, B.C., Campbell, N.R., Holecek, D.E., and Narum, S.R. (2013). Genome-wide association reveals genetic basis for the propensity to migrate in wild populations of rainbow and steelhead trout. Mol Ecol 22, 3061–3076.CrossRefPubMedGoogle Scholar
  31. Hosseinzadeh, Z., Singh, Y., Shimshek, D.R., van der Putten, H., Wagner, C.A., and Lang, F. (2017). Leucine-rich repeat kinase 2 (Lrrk2)-sensitive Na+/K+ ATPase activity in dendritic cells. Sci Rep 7, 41117.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Huang, H., Wei, Y., Meng, Z., Zhang, Y., Liu, X., Guo, L., Luo, J., Chen, G., and Lin, H. (2014). Polymorphisms of leptin-b gene associated with growth traits in orange-spotted grouper (Epinephelus coioides). Int J Mol Sci 15, 11996–12006.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Huang, R., Sun, J., Luo, Q., He, L., Liao, L., Li, Y., Guo, F., Zhu, Z., and Wang, Y. (2015). Genetic variations of body weight and GCRV resistance in a random mating population of grass carp. Oncotarget in press doi: 10.18632/oncotarget.5945.Google Scholar
  34. Jeong, B.C., Kim, M.Y., Lee, J.H., Kee, H.J., Kho, D.H., Han, K.E., Qian, Y.R., Kim, J.K., and Kim, K.K. (2006). Brain-specific angiogenesis inhibitor 2 regulates VEGF through GABP that acts as a transcriptional repressor. FEBS Lett 580, 669–676.CrossRefPubMedGoogle Scholar
  35. Jiang, L., and Li, H. (2017). Single locus maintains large variation of sex reversal in half-smooth tongue sole (Cynoglossus semilaevis ). G3 7, 583–589.CrossRefPubMedGoogle Scholar
  36. Kakioka, R., Kokita, T., Kumada, H., Watanabe, K., and Okuda, N. (2013). A RAD-based linkage map and comparative genomics in the gudgeons (genus Gnathopogon, Cyprinidae). BMC Genomics 14, 32.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kang, H.M., Sul, J.H., Service, S.K., Zaitlen, N.A., Kong, S.Y., Freimer, N. B., Sabatti, C., and Eskin, E. (2010). Variance component model to account for sample structure in genome-wide association studies. Nat Genet 42, 348–354.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kessuwan, K., Kubota, S., Liu, Q., Sano, M., Okamoto, N., Sakamoto, T., Yamashita, H., Nakamura, Y., and 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.CrossRefPubMedGoogle Scholar
  39. Koch, M., Schulze, J., Hansen, U., Ashwodt, T., Keene, D.R., Brunken, W. J., Burgeson, R.E., Bruckner, P., and Bruckner-Tuderman, L. (2004). A novel marker of tissue junctions, collagen XXII. J Biol Chem 279, 22514–22521.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lam, H.M., Xu, X., Liu, X., Chen, W., Yang, G., Wong, F.L., Li, M.W., He, W., Qin, N., Wang, B., Li, J., Jian, M., Wang, J., Shao, G., Wang, J., Sun, S.S.M., and Zhang, G. (2010). Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet 42, 1053–1059.CrossRefPubMedGoogle Scholar
  41. Le Pabic, P., Ng, C., and Schilling, T.F. (2014). Fat-dachsous signaling coordinates cartilage differentiation and polarity during craniofacial development. PLoS Genet 10, e1004726.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Li, H., Peng, Z., Yang, X., Wang, W., Fu, J., Wang, J., Han, Y., Chai, Y., Guo, T., Yang, N., Liu, J., Warburton, M.L., Cheng, Y., Hao, X., Zhang, P., Zhao, J., Liu, Y., Wang, G., Li, J., and Yan, J. (2013). Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nat Genet 45, 43–50.CrossRefPubMedGoogle Scholar
  43. Li, R., Li, Y., Fang, X., Yang, H., Wang, J., Kristiansen, K., and Wang, J. (2009). SNP detection for massively parallel whole-genome resequencing. Genome Res 19, 1124–1132.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Liao, R., Zhang, X., Chen, Q., Wang, Z., Wang, Q., Yang, C., and Pan, Y. (2016). Genome-wide association study reveals novel variants for growth and egg traits in Dongxiang blue-shelled and White Leghorn chickens. Anim Genet 47, 588–596.CrossRefPubMedGoogle Scholar
  45. Lipka, A.E., Tian, F., Wang, Q., Peiffer, J., Li, M., Bradbury, P.J., Gore, M. A., Buckler, E.S., and Zhang, Z. (2012). GAPIT: genome association and prediction integrated tool. Bioinformatics 28, 2397–2399.CrossRefPubMedGoogle Scholar
  46. Liu, F., Sun, F., Xia, J.H., Li, J., Fu, G.H., Lin, G., Tu, R.J., Wan, Z.Y., Quek, D., and Yue, G.H. (2014). A genome scan revealed significant associations of growth traits with a major QTL and GHR2 in tilapia. Sci Rep 4, 7256.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Liu, J.L., Wang, T.S., and Zhao, M. (2016a). Genome-wide association mapping for female infertility in inbred mice. G3 6, 2929–2935.CrossRefPubMedGoogle Scholar
  48. Liu, L.Y.M., Lin, M.H., Lai, Z.Y., Jiang, J.P., Huang, Y.C., Jao, L.E., and Chuang, Y.J. (2016b). Motor neuron-derived Thsd7a is essential for zebrafish vascular development via the Notch-dll4 signaling pathway. J Biomed Sci 23, 59.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Liu, W., and Collodi, P. (2010). Zebrafish dead end possesses ATPase activity that is required for primordial germ cell development. FASEB J 24, 2641–2650.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Luo, W., Cheng, D., Chen, S., Wang, L., Li, Y., Ma, X., Song, X., Liu, X., Li, W., Liang, J., Yan, H., Zhao, K., Wang, C., Wang, L., and Zhang, L. (2012). Genome-wide association analysis of meat quality traits in a porcine Large White×Minzhu intercross population. Int J Biol Sci 8, 580–595.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Ma, X., Guan, L., Xuan, J., Wang, H., Yuan, Z., Wu, M., Liu, R., Zhu, C., Wei, C., Zhao, F., Du, L., and Zhang, L. (2016). Effect of polymorphisms in the CAMKMT gene on growth traits in Ujumqin sheep. Anim Genet 47, 618–622.CrossRefPubMedGoogle Scholar
  52. Martínez-López, M.J., Alcántara, S., Mascaró, C., Pérez-Brangulí, F., Ruiz- Lozano, P., Maes, T., Soriano, E., and Buesa, C. (2005). Mouse Neuron navigator 1, a novel microtubule-associated protein involved in neuronal migration. Mol Cell Neurosci 28, 599–612.CrossRefPubMedGoogle Scholar
  53. Mgonja, E.M., Balimponya, E.G., Kang, H., Bellizzi, M., Park, C.H., Li, Y., Mabagala, R., Sneller, C., Correll, J., Opiyo, S., Talbot, N.J., Mitchell, T., and Wang, G.L. (2016). Genome-wide association mapping of rice resistance genes against Magnaporthe oryzae isolates from four African countries. Phytopathology 106, 1359–1365.CrossRefPubMedGoogle Scholar
  54. Mierzejewska, K., Heo, J., Kang, J.W., Kang, H., Ratajczak, J., Ratajczak, M.Z., Kucia, M., and Shin, D.M. (2013). Genome-wide analysis of murine bone marrow-derived very small embryonic-like stem cells reveals that mitogenic growth factor signaling pathways play a crucial role in the quiescence and ageing of these cells. Int J Mol Med 32, 281–290.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Millamena, O.M. (2002). Replacement of fish meal by animal by-product meals in a practical diet for grow-out culture of grouper Epinephelus coioides. Aquaculture 204, 75–84.CrossRefGoogle Scholar
  56. Mousavi, M., Tong, C., Liu, F., Tao, S., Wu, J., Li, H., and Shi, J. (2016). De novo SNP discovery and genetic linkage mapping in poplar using restriction site associated DNA and whole-genome sequencing technologies. BMC Genomics 17, 656.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Nakagawa, S. (2004). A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15, 1044–1045.CrossRefGoogle Scholar
  58. Nalls, M.A., Pankratz, N., Lill, C.M., Do, C.B., Hernandez, D.G., Saad, M., DeStefano, A.L., Kara, E., Bras, J., Sharma, M., Schulte, C., Keller, M. F., Arepalli, S., Letson, C., Edsall, C., Stefansson, H., Liu, X., Pliner, H., Lee, J.H., Cheng, R., Ikram, M.A., Ioannidis, J.P.A., Hadjigeorgiou, G.M., Bis, J.C., Martinez, M., Perlmutter, J.S., Goate, A., Marder, K., Fiske, B., Sutherland, M., Xiromerisiou, G., Myers, R.H., Clark, L.N., Stefansson, K., Hardy, J.A., Heutink, P., Chen, H., Wood, N.W., Houlden, H., Payami, H., Brice, A., Scott, W.K., Gasser, T., Bertram, L., Eriksson, N., Foroud, T., and Singleton, A.B. (2014). Large-scale metaanalysis of genome-wide association data identifies six new risk loci for Parkinson’s disease. Nat Genet 46, 989–993.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Nie, F., Liu, T., Zhong, L., Yang, X., Liu, Y., Xia, H., Liu, X., Wang, X., Liu, Z., Zhou, L., Mao, Z., Zhou, Q., and Chen, T. (2016). MicroRNA- 148b enhances proliferation and apoptosis in human renal cancer cells via directly targeting MAP3K9. Mol Med Rep 13, 83–90.CrossRefPubMedGoogle Scholar
  60. Omelchenko, T., and Hall, A. (2012). Myosin-IXA regulates collective epithelial cell migration by targeting RhoGAP activity to cell-cell junctions. Curr Biol 22, 278–288.CrossRefPubMedPubMedCentralGoogle Scholar
  61. Ouna, B.A., Stewart, M., Helbig, C., and Clayton, C. (2012). The Trypanosoma brucei CCCH zinc finger proteins ZC3H12 and ZC3H13. Mol Biochem Parasitol 183, 184–188.CrossRefPubMedGoogle Scholar
  62. Palaiokostas, C., Bekaert, M., Taggart, J.B., Gharbi, K., McAndrew, B.J., Chatain, B., Penman, D.J., and Vandeputte, M. (2015). A new SNPbased vision of the genetics of sex determination in European sea bass (Dicentrarchus labrax). Genet Sel Evol 47, 68.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Palaiokostas, C., Ferraresso, S., Franch, R., Houston, R.D., and Bargelloni, L. (2016). Genomic prediction of resistance to pasteurellosis in gilthead sea bream (Sparus aurata) using 2b-RAD sequencing. G3 in press doi: 10.1534/g3.116.035220.Google Scholar
  64. Peterson, D.R., Mok, H.O.L., and Au, D.W.T. (2015). Modulation of telomerase activity in fish muscle by biological and environmental factors. Compar Biochem Physiol C Toxicol Pharmacol 178, 51–59.CrossRefGoogle Scholar
  65. Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A.R., Bender, D., Maller, J., Sklar, P., de Bakker, P.I.W., Daly, M.J., and Sham, P.C. (2007). PLINK: a tool set for whole-genome association and population- based linkage analyses. Am J Hum Genet 81, 559–575.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Riggio, V., Matika, O., Pong-Wong, R., Stear, M.J., and Bishop, S.C. (2013). Genome-wide association and regional heritability mapping to identify loci underlying variation in nematode resistance and body weight in Scottish Blackface lambs. Heredity 110, 420–429.CrossRefPubMedPubMedCentralGoogle Scholar
  67. Rowe, H.C., Renaut, S., and Guggisberg, A. (2011). RAD in the realm of next-generation sequencing technologies. Mol Ecol 20, 3499–3502.PubMedGoogle Scholar
  68. Sánchez-Molano, E., Cerna, A., Toro, M.A., Bouza, C., Hermida, M., Pardo, B.G., Cabaleiro, S., Fernández, J., and Martínez, P. (2011). Detection of growth-related QTL in turbot (Scophthalmus maximus). BMC Genomics 12, 473.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Slavov, G.T., Nipper, R., Robson, P., Farrar, K., Allison, G.G., Bosch, M., Clifton-Brown, J.C., Donnison, I.S., and Jensen, E. (2014). Genomewide association studies and prediction of 17 traits related to phenology, biomass and cell wall composition in the energy grass Miscanthus sinensis. New Phytol 201, 1227–1239.CrossRefPubMedGoogle Scholar
  70. Smith, J.D., Hing, A.V., Clarke, C.M., Johnson, N.M., Perez, F.A., Park, S. S., Horst, J.A., Mecham, B., Maves, L., Nickerson, D.A., Nickerson, D. A., and Cunningham, M.L. (2014). Exome sequencing identifies a recurrent de novo ZSWIM6 mutation associated with acromelic frontonasal dysostosis. Am J Hum Genet 95, 235–240.CrossRefPubMedPubMedCentralGoogle Scholar
  71. Song, W., Pang, R., Niu, Y., Gao, F., Zhao, Y., Zhang, J., Sun, J., Shao, C., Liao, X., Wang, L., Tian, Y., and Chen, S. (2012). Construction of highdensity genetic linkage maps and mapping of growth-related quantitative trail loci in the Japanese flounder (Paralichthys olivaceus). PLoS ONE 7, e50404.CrossRefPubMedPubMedCentralGoogle Scholar
  72. Sun, L.F., Li, J., Liang, X.F., Yi, T.L., Fang, L., Sun, J., He, Y.H., Luo, X. N., Dou, Y.Q., and Yang, M. (2015). Microsatellite DNA markers and their correlation with growth traits in mandarin fish (Siniperca chuatsi). Genet Mol Res 14, 19128–19135.CrossRefPubMedGoogle Scholar
  73. Tang, H., Peng, J., Wang, P., and Risch, N.J. (2005). Estimation of individual admixture: analytical and study design considerations. Genet Epidemiol 28, 289–301.CrossRefPubMedGoogle Scholar
  74. Tosh, J.J., Ventura, R.V., An, K.P., Elliot, J.A.K., Ken, M.P., Lie, S., Boulding, E.G., and Schaeffer, L.R. (2014). Genome-wide Association Analysis of Harvest Weight in a North American Atlantic Salmon Population. In Proceedings of the 10th World Congress of Genetics Applied to Livestock Production, pp. 10–12.Google Scholar
  75. Wainwright, E.N., Wilhelm, D., Combes, A.N., Little, M.H., and Koopman, P. (2015). ROBO2 restricts the nephrogenic field and regulates Wolffian duct-nephrogenic cord separation. Dev Biol 404, 88–102.CrossRefPubMedGoogle Scholar
  76. Wang, C.M., Lo, L.C., Feng, F., Zhu, Z.Y., and Yue, G.H. (2008). Identification and verification of QTL associated with growth traits in two genetic backgrounds of Barramundi (Lates calcarifer). Animal Genets 39, 34–39.CrossRefGoogle Scholar
  77. Wang, F., Chen, W., Lin, H., and Li, W. (2014). Cloning, expression, and ligand-binding characterization of two neuropeptide Y receptor subtypes in orange-spotted grouper, Epinephelus coioides. Fish Physiol Biochem 40, 1693–1707.CrossRefPubMedGoogle Scholar
  78. Wang, L., Huang, J., and Jiang, M. (2011). CREB5 computational regulation network construction and analysis between frontal cortex of HIV encephalitis (HIVE) and HIVE-control patients. Cell Biochem Biophys 60, 199–207.CrossRefPubMedGoogle Scholar
  79. Wang, W., Hu, Y., Ma, Y., Xu, L., Guan, J., and Kong, J. (2015a). Highdensity genetic linkage mapping in turbot (Scophthalmus maximus L.) based on SNP markers and major sex- and growth-related regions detection. PLoS ONE 10, e0120410.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Wang, X., Hang, S., Prazak, L., and Gergen, J.P. (2010). NELF potentiates gene transcription in the Drosophila embryo. PLoS ONE 5, e11498.CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wang, Y., Ning, Z., Hu, Y., Chen, J., Zhao, R., Chen, H., Ai, N., Guo, W., and Zhang, T. (2015b). Molecular mapping of restriction-site associated DNA markers in allotetraploid upland cotton. PLoS ONE 10, e0124781.CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wei, Y., Huang, H., Meng, Z., Zhang, Y., Luo, J., Chen, G., and Lin, H. (2013). Single nucleotide polymorphisms in the leptin-a gene and associations with growth traits in the orange-spotted grouper (Epinephelus coioides). Int J Mol Sci 14, 8625–8637.CrossRefPubMedPubMedCentralGoogle Scholar
  83. Wu, K., Liu, H., Yang, M., Tao, Y., Ma, H., Wu, W., Zuo, Y., and Zhao, Y. (2014). High-density genetic map construction and QTLs analysis of grain yield-related traits in Sesame (Sesamum indicum L.) based on RAD-Seq techonology. BMC Plant Biol 14, 274.CrossRefPubMedPubMedCentralGoogle Scholar
  84. Wu, S., Li, B., Lin, H., and Li, W. (2012). Stimulatory effects of neuropeptide Y on the growth of orange-spotted grouper (Epinephelus coioides). Gene Compar Endocrinol 179, 159–166.CrossRefGoogle Scholar
  85. Xia, J.H., Wan, Z.Y., Ng, Z.L., Wang, L., Fu, G.H., Lin, G., Liu, F., and Yue, G.H. (2014). Genome-wide discovery and in silico mapping of gene-associated SNPs in Nile tilapia. Aquaculture 432, 67–73.CrossRefGoogle Scholar
  86. Xu, R., Fang, X.H., and Zhong, P. (2016). Myosin VI contributes to malignant proliferation of human glioma cells. Korean J Physiol Pharmacol 20, 139.CrossRefPubMedPubMedCentralGoogle Scholar
  87. Xu, X., Dong, G.X., Hu, X.S., Miao, L., Zhang, X.L., Zhang, D.L., Yang, H.D., Zhang, T.Y., Zou, Z.T., Zhang, T.T., Zhuang, Y., Bhak, J., Cho, Y. S., Dai, W.T., Jiang, T.J., Xie, C., Li, R., and Luo, S.J. (2013). The genetic basis of white tigers. Curr Biol 23, 1031–1035.CrossRefPubMedGoogle Scholar
  88. You, W., Tan, G., Sheng, N., Gong, J., Yan, J., Chen, D., Zhang, H., and Wang, Z. (2016). Downregulation of myosin VI reduced cell growth and increased apoptosis in human colorectal cancer. Acta Biochim Biophys Sin 48, 430–436.CrossRefPubMedGoogle Scholar
  89. You, X., Shu, L., Li, S., Chen, J., Luo, J., Lu, J., Mu, Q., Bai, J., Xia, Q., Chen, Q., Cai, Y., Zhang, H., Chen, G., Lin, H., Zhang, Y., and Shi, Q. (2013). Construction of high-density genetic linkage maps for orangespotted grouper Epinephelus coioides using multiplexed shotgun genotyping. BMC Genet 14, 113.CrossRefPubMedPubMedCentralGoogle Scholar
  90. Yu, H., You, X., Li, J., Liu, H., Meng, Z., Xiao, L., Zhang, H., Lin, H.R., Zhang, Y., and Shi, Q. (2016). Genome-wide mapping of growth-related quantitative trait loci in orange-spotted grouper (Epinephelus coioides) using double digest restriction-site associated DNA sequencing (ddRADseq). Int J Mol Sci 17, 501.CrossRefPubMedPubMedCentralGoogle Scholar
  91. Zencir, S., Ovee, M., Dobson, M.J., Banerjee, M., Topcu, Z., and Mohanty, S. (2011). Identification of brain-specific angiogenesis inhibitor 2 as an interaction partner of glutaminase interacting protein. Biochem Biophys Res Commun 411, 792–797.CrossRefPubMedPubMedCentralGoogle Scholar
  92. Zhang, L., Ma, X., Xuan, J., Wang, H., Yuan, Z., Wu, M., Liu, R., Zhu, C., Wei, C., Zhao, F., and Du, L. (2016). Identification of MEF2B and TRHDE gene polymorphisms related to growth traits in a new Ujumqin sheep population. PLoS ONE 11, e0159504.CrossRefPubMedPubMedCentralGoogle Scholar
  93. Zhang, L., Wang, J., Zhang, M., Wang, G., Shen, Y., Wu, D., Wang, C., Li, L., Ren, Y., Wang, B., Zhang, H., Yang, X., Zhao, Y., Han, C., Zhou, J., Pang, C., Yin, L., Zhao, J., Luo, X., and Hu, D. (2017). Association of type 2 diabetes mellitus with the interaction between low-density lipoprotein receptor-related protein 5 (LRP5) polymorphisms and overweight and obesity in rural Chinese adults. J Diabetes 9, 994–1002.CrossRefPubMedGoogle Scholar
  94. Zhang, W., Zhang, Y., Zhang, L., Zhao, H., Li, X., Huang, H., and Lin, H. (2007). The mRNA expression of P450 aromatase, gonadotropin β-subunits and FTZ-F1 in the orange-spotted grouper (Epinephelus coioides) during 17a-methyltestosterone-induced precocious sex change. Mol Reprod Dev 74, 665–673.CrossRefPubMedGoogle Scholar
  95. Zheng, X., Kuang, Y., Lv, W., Cao, D., Sun, Z., and Sun, X. (2016). Genome-wide association study for muscle fat content and abdominal fat traits in common carp (Cyprinus carpio). PLoS ONE 11, e0169127.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Hui Yu
    • 1
    • 2
  • Xinxin You
    • 2
  • Jia Li
    • 2
  • Xinhui Zhang
    • 2
  • Shuai Zhang
    • 2
  • Shoujia Jiang
    • 2
  • Xueqiang Lin
    • 2
  • Hao-Ran Lin
    • 3
  • Zining Meng
    • 3
  • Qiong Shi
    • 1
    • 2
    • 4
  1. 1.BGI Education CenterUniversity of Chinese Academy of SciencesShenzhenChina
  2. 2.Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic AnimalsBGI Academy of Marine Sciences, BGI Marine, BGIShenzhenChina
  3. 3.State Key Laboratory of Biocontrol, Institute of Aquatic Economic Animals, and the Guangdong Province Key Laboratory for Aquatic Economic AnimalsSun Yat-Sen UniversityGuangzhouChina
  4. 4.Laboratory of Aquatic Genomics, College of Life Sciences and OceanographyShenzhen UniversityShenzhenChina

Personalised recommendations