Identification of Candidate Growth-Related SNPs and Genes Using GWAS in Brown-Marbled Grouper (Epinephelus fuscoguttatus)
Brown-marbled grouper, Epinephelus fuscoguttatus, is not only an important commercial fish species, but also an important crossbreeding parent in grouper industry. Improvement of growth traits of this species contributes to the development of grouper breeding. Currently, the development of molecular marker associated with growth of brown-marbled grouper is rare. Thus, we performed the first genome-wide association study (GWAS) for five growth traits in 172 brown-marbled groupers with 43,688 SNPs detected by ddRAD-seq. We identified a total of 5 significant and 18 suggestive QTLs located in multiple chromosomes associated with growth traits. In the 20 kb window of the significant SNPs and suggestive SNPs, 5 and 14 potential candidate genes affecting growth were detected, respectively. Five potential candidate genes near the significantly associated SNPs were selected for expression analysis. Among of which, bmp2k, wasf1, and acyp2 involved in bone development, maintenance of mitochondrion structure, and metabolism were differentially expressed. Interestingly, the SNP 23:29601315 located in the intron of bmp2k was significantly associated with body weight, body length, body height, and body thickness and suggestively associated with total length. We verified the locus using another new group including 123 individuals. The results showed that individuals with CC genotype have better growth traits comparing other individuals. Our findings not only contribute to understanding the molecular mechanism of growth regulation, but also promote the advance of marker-assisted selection in brown-marbled grouper.
KeywordsGWAS Growth Epinephelus fuscoguttatus bmp2k SNP
We thank Mr. Xiaoli Yang (Zhanjiang Hengxing aquatic science and technology co. LTD) and Dr. Haifa Zhang (Marine fisheries Development center of Guangdong Province) for providing fish samples; Jianan He (Sun Yat-sen University) for collecting the samples.
Y.Y., Z.M., and X. L. designed the study. Y.Y., L.W., L.S., and W.H. collected the samples. Y.Y. and Z.M. performed the laboratory work. Y.Y., L.W., B.L., Y.G., and Z.M. performed analyses. J.X. contributed technical assistance. Y.Y., Z.M, and X.L. drafted the paper.
This research was funded by Agriculture Research System of China (ARS-47); Science and Technology Planning Project of Guangzhou (201804020013); National Natural Science Foundation of China (31872572); Yang Fan Innovative & Entrepreneurial Research Team Project (No.201312H10); National Natural Science Foundation of China (u1401213, 31802266); and the Program of the China-ASEAN Maritime Cooperation Fund of the Chinese government.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interests.
- Amenyogbe E, Chen G, Wang Z (2019) Identification, characterization, and expressions profile analysis of growth hormone receptors (GHR1 and GHR2) in hybrid grouper (Epinephelus fuscoguttatus ♀ × Epinephelus polyphekadion ♂). Genomics. https://doi.org/10.1016/j.ygeno.2019.05.012 CrossRefGoogle Scholar
- Bonferroni C (1936) Teoria statistica delle classi e calcolo delle probabilita. Pubblicazioni del R Istituto Superiore di Scienze Economiche e Commericiali di Firenze 8:3–62Google Scholar
- Gonzalez-Pena D, Gao G, Baranski M, Moen T, Cleveland BM, Brett Kenney P, Vallejo RL, Palti Y, Leeds TD (2016) Genome-wide association study for identifying loci that affect fillet yield, carcass, and body weight traits in rainbow trout (Oncorhynchus mykiss). Front Genet 7Google Scholar
- Guo L, Yang S, Li MM, Meng ZN, Lin HR (2016) Divergence and polymorphism analysis of IGF1Ra and IGF1Rb from orange-spotted grouper, Epinephelus coioides (Hamilton). Genet Mol Res 15Google Scholar
- Löhr H, Hess S, Pereira MMA, Reinoß P, Leibold S, Schenkel C, Wunderlich CM, Kloppenburg P, Brüning JC, Hammerschmidt M (2018) Diet-induced growth is regulated via acquired Leptin resistance and engages a Pomc-Somatostatin-growth hormone circuit. Cell Rep 23:1728–1741PubMedPubMedCentralCrossRefGoogle Scholar
- Lv W, Zheng X, Kuang Y, Cao D, Yan Y, Sun X (2016) QTL variations for growth-related traits in eight distinct families of common carp (Cyprinus carpio). BMC Genet 17Google Scholar
- Mamauag REP, Ragaza JA, Nacionales T (2019) Fish performance, nutrient digestibilities, and hepatic and intestinal morphologies in grouper Epinephelus fuscoguttatus fed fermented copra meal. Aquac Res 14Google Scholar
- Peng W, Xu J, Zhang Y, Feng J, Dong C, Jiang L, Feng J, Chen B, Gong Y, Chen L, Xu P (2016) Erratum: an ultra-high density linkage map and QTL mapping for sex and growth-related traits of common carp (Cyprinus carpio. Sci Rep 6Google 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 7Google Scholar
- Rimmer MA, Thampisamraj YC, Jayagopal P, Thineshsanthar D, Damodar PN, Toledo JD (2013) Spawning of tiger grouper Epinephelus fuscoguttatus and squaretail coralgrouper Plectropomus areolatus in sea cages and onshore tanks in Andaman and Nicobar Islands, India. Aquaculture 410-411:197–202CrossRefGoogle Scholar
- Salem M, Al-Tobasei R, Ali A, Lourenco D, Gao G, Palti Y, Kenney B, Leeds TD (2018) Genome-wide association analysis with a 50K transcribed gene SNP- Chip identifies QTL affecting muscle yield in rainbow trout. Front Genet 9Google Scholar
- Sun Y, Guo CY, Wang DD, Li XF, Xiao L, Zhang X, You X, Shi Q, Hu GJ, Fang C, Lin HR, Zhang Y (2016) Transcriptome analysis reveals the molecular mechanisms underlying growth superiority in a novel grouper hybrid (Epinephelus fuscogutatus♀× E. lanceolatus♂). BMC Genetics 17:24PubMedPubMedCentralCrossRefGoogle Scholar
- Xu T, Zhang X, Ruan Z, Yu H, Chen J, Jiang S, Bian C, Wu B, Shi Q, You X (2019) Genome resequencing of the orange-spotted grouper (Epinephelus coioides) for a genome-wide association study on ammonia tolerance. Aquaculture 512Google Scholar
- Yu H, You X, Li J, Liu H, Meng Z, Xiao L, Zhang H, Lin HR, Zhang Y, 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 17PubMedPubMedCentralCrossRefGoogle Scholar
- 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 19:379–390PubMedCrossRefGoogle Scholar