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Identification of Candidate Growth-Related SNPs and Genes Using GWAS in Brown-Marbled Grouper (Epinephelus fuscoguttatus)

  • Yang Yang
  • Lina Wu
  • Xi Wu
  • Bijun Li
  • Wenhua Huang
  • Zhuoying Weng
  • Zixuan Lin
  • Leling Song
  • Yin Guo
  • Zining MengEmail author
  • Xiaochun LiuEmail author
  • Junhong Xia
Review Article

Abstract

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.

Keywords

GWAS Growth Epinephelus fuscoguttatus bmp2k SNP 

Notes

Acknowledgments

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.

Authors’ Contributions

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.

Funding Information

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.

Supplementary material

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References

  1. Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664PubMedPubMedCentralCrossRefGoogle Scholar
  2. 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
  3. 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
  4. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635PubMedCrossRefGoogle Scholar
  5. Buchman AR, Berg P (1988) Comparison of intron-dependent and intron-independent gene expression. Mol Cell Biol 8:4395–4405PubMedPubMedCentralCrossRefGoogle Scholar
  6. Chen Y, Cai S, Jian J (2019) Protection against Vibrio alginolyticus in pearl gentian grouper (♀Epinephelus fuscoguttatus × ♂Epinephelus lanceolatu) immunized with an acfA-deletion live attenuated vaccine. Fish Shellfish Immunol 86:875–881CrossRefGoogle Scholar
  7. Cheng M, Tian Y, Li Z, Wang L, Wu Y, Zhang J, Pang Z, Ma W, Zhai J (2019) The complete mitochondrial genome of the hybrid offspring Epinephelus fuscoguttatus ♀ × Epinephelus tukula ♂. Mitochondr DNA B 4:2717–2718CrossRefGoogle Scholar
  8. Chung S, Perry RP (1989) Importance of introns for expression of mouse ribosomal protein gene rpL32. Mol Cell Biol 9:2075–2082PubMedPubMedCentralCrossRefGoogle Scholar
  9. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, Depristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158PubMedPubMedCentralCrossRefGoogle Scholar
  10. De-Santis C, Jerry DR (2007) Candidate growth genes in finfish - where should we be looking? Aquaculture 272:22–38CrossRefGoogle Scholar
  11. Degl'innocenti D, Marzocchini R, Rosati F, Cellini E, Raugei G, Ramponi G (1999) Acylphosphatase expression during macrophage differentiation and activation of U-937 cell line. Biochimie 81:1031–1035PubMedCrossRefGoogle Scholar
  12. Gasser RB, Hu M, Chilton NB, Campbell BE, Jex AJ, Otranto D, Cafarchia C, Beveridge I, Zhu X (2007) Single-strand conformation polymorphism (SSCP) for the analysis of genetic variation. Nat Protoc 1:3121–3128CrossRefGoogle Scholar
  13. Geng X, Liu S, Yao J, Bao L, Zhang J, Li C, Wang R, Sha J, Zeng P, Zhi D, Liu Z (2016) A genome-wide association study identifies multiple regions associated with head size in catfish. G3 (Bethesda) 6:3389–3398PubMedPubMedCentralCrossRefGoogle Scholar
  14. 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
  15. Guo L, Xia J, Yang S, Li M, You X, Meng Z, Lin H (2015) GHRH, PRP-PACAP and GHRHR target sequencing via an ion torrent personal genome machine reveals an association with growth in orange-spotted grouper (Epinephelus coioides). Int J Mol Sci 16:26137–26150PubMedPubMedCentralCrossRefGoogle Scholar
  16. 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
  17. Gutierrez AP, Yáñ Ez JM, Fukui S, Swift B, Davidson WS (2015) Genome-wide association study (GWAS) for growth rate and age at sexual maturation in Atlantic salmon (Salmo salar). PLoS One 10PubMedPubMedCentralCrossRefGoogle Scholar
  18. Huang H, Wei Y, Meng Z, Zhang Y, Liu X, Guo L, Luo J, Chen G, Lin H (2014) Polymorphisms of leptin-b gene associated with growth traits in orange-spotted grouper (Epinephelus coioides). Int J Mol Sci 15:11996–12006PubMedPubMedCentralCrossRefGoogle Scholar
  19. Jiang DL, Gu XH, Li BJ, Zhu ZX, Qin H, Meng Z, Lin HR, Xia JH (2019) Identifying a long QTL cluster across chrLG18 associated with salt tolerance in Tilapia using GWAS and QTL-seq. Mar Biotechnol 21:250–261PubMedCrossRefGoogle Scholar
  20. Kearns AE, Donohue MM, Sanyal B, Demay MB (2001) Cloning and characterization of a novel protein kinase that impairs osteoblast differentiation in vitro. J Biol Chem 276:42213–42218PubMedCrossRefGoogle Scholar
  21. Lalitha S (2000) Primer Premier 5. Biotech Software Internet Rep 1:270–272CrossRefGoogle Scholar
  22. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359PubMedPubMedCentralCrossRefGoogle Scholar
  23. Le Hir H, Nott A, Moore MJ (2003) How introns influence and enhance eukaryotic gene expression. Trends Biochem Sci 28:215–220PubMedCrossRefGoogle Scholar
  24. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079PubMedPubMedCentralCrossRefGoogle Scholar
  25. Li N, Zhou T, Geng X, Jin Y, Wang X, Liu S, Xu X, Gao D, Li Q, Liu Z (2018) Identification of novel genes significantly affecting growth in catfish through GWAS analysis. Mol Gen Genomics 293:587–599CrossRefGoogle Scholar
  26. Li S, Liu H, Bai J, Zhu X (2017) Transcriptome assembly and identification of genes and SNPs associated with growth traits in largemouth bass (Micropterus salmoides). Genetica 145:175–187PubMedCrossRefGoogle Scholar
  27. Liu G, Gong Z, Li Q (2019) The complete mitochondrial genome of the breed Ningbo brown-marbled grouper (Epinephelus fuscoguttatus). Mitochondr DNA B 4:2109–2110CrossRefGoogle Scholar
  28. 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
  29. 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
  30. 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
  31. Mohamad N, Mohd Roseli FA, Azmai MNA, Saad MZ, Md Yasin IS, Zulkiply NA, Nasruddin NS (2019) Natural concurrent infection of Vibrio harveyi and V. alginolyticus in cultured hybrid groupers in Malaysia. J Aquat Anim Health 31:88–96PubMedCrossRefGoogle Scholar
  32. Mukai Y, Lim LS (2016) Morphogenesis of free neuromasts in the larvae of brown-marbled grouper Epinephelus fuscoguttatus. Mar Freshw Behav Physiol 49:159–171CrossRefGoogle Scholar
  33. Nazari S, Jafari V, Pourkazemi M, Miandare HK, Abdolhay HA (2016) Association between myostatin gene (MSTN-1) polymorphism and growth traits in domesticated rainbow trout (Oncorhynchus mykiss). Agri Gene 1:109–115CrossRefGoogle Scholar
  34. Nguyen NH, Rastas PMA, Premachandra HKA, Knibb W (2018) First high-density linkage map and single nucleotide polymorphisms significantly associated with traits of economic importance in yellowtail kingfish Seriola lalandi. Frontiers in Genetics 9:127PubMedPubMedCentralCrossRefGoogle Scholar
  35. Noor NM, Defoirdt T, Alipiah N, Karim M, Daud H, Natrah I (2019) Quorum sensing is required for full virulence of Vibrio campbellii towards tiger grouper (Epinephelus fuscoguttatus) larvae. J Fish Dis 42:489–495PubMedCrossRefGoogle Scholar
  36. Nurdalila AA, Mayalvanan Y, Baharum SN (2019) Metabolite profiling of Epinephelus fuscoguttatus infected with vibriosis reveals omega 9 as potential metabolite biomarker. Fish Physiol Biochem 45:1203–1215PubMedCrossRefGoogle Scholar
  37. 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
  38. 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
  39. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MR, Bender D, Maller J, Sklar P, De Bakker PIW, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575PubMedPubMedCentralCrossRefGoogle Scholar
  40. Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842PubMedPubMedCentralCrossRefGoogle Scholar
  41. Reis Neto RV, Yoshida GM, Lhorente JP, Yáñez JM (2019) Genome-wide association analysis for body weight identifies candidate genes related to development and metabolism in rainbow trout (Oncorhynchus mykiss). Mol Gen Genomics 294:563–571CrossRefGoogle Scholar
  42. Ribas L, Robledo D, Gómez-Tato A, Viñas A, Martínez P, Piferrer F (2016) Comprehensive transcriptomic analysis of the process of gonadal sex differentiation in the turbot (Scophthalmus maximus). Mol Cell Endocrinol 422:132–149PubMedCrossRefGoogle Scholar
  43. 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
  44. 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
  45. 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
  46. Sung JY, Engmann O, Teylan MA, Nairn AC, Greengard P, Kim Y (2008) WAVE1 controls neuronal activity-induced mitochondrial distribution in dendritic spines. Proceedings of the National Academy of Sciences of the United States of America 105:3112–3116PubMedPubMedCentralCrossRefGoogle Scholar
  47. Tsai HY, Hamilton A, Tinch AE, Guy DR, Gharbi K, Stear MJ, Matika O, Bishop SC, Houston RD (2015) Genome wide association and genomic prediction for growth traits in juvenile farmed Atlantic salmon using a high density SNP array. BMC Genomics 16:969PubMedPubMedCentralCrossRefGoogle Scholar
  48. Wang L, Liu P, Huang S, Ye B, Chua E, Wan ZY, Yue GH (2017) Genome-wide association study identifies loci associated with resistance to viral nervous necrosis disease in Asian Seabass. Mar Biotechnol 19:255–265PubMedCrossRefGoogle Scholar
  49. Wang M, Xu F, Chen K, Li X, Li K, Zhou Y, Xiao J (2019a) A multiplex SNP genotyping by allele-specificspecific PCR based on stem-loop and universal fluorescent primers of Chr1daxin mice. Electrophoresis 40:1600–1605PubMedCrossRefGoogle Scholar
  50. Wang W, Tan S, Luo J, Shi H, Zhou T, Yang Y, Jin Y, Wang X, Niu D, Yuan Z, Gao D, Dunham R, Liu Z (2019b) GWAS analysis indicated importance of NF-κB signaling pathway in host resistance against motile Aeromonas septicemia disease in catfish. Mar Biotechnol 21:335–347PubMedCrossRefGoogle Scholar
  51. Wang Y, Wang X, Meng X, Wang H, Jiang Z, Qiu X (2014) Identification of two SNPs in myostatin (MSTN) gene of Takifugu rubripes and their association with growth traits. Mol Cell Probes 28:200–203PubMedCrossRefGoogle Scholar
  52. Wu L, Yang Y, Li B, Huang W, Wang X, Liu X, Meng Z, Xia J (2019) First genome-wide association analysis for growth traits in the largest coral reef-dwelling bony fishes, the Giant grouper (Epinephelus lanceolatus). Mar Biotechnol 21:707–717PubMedCrossRefGoogle Scholar
  53. 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
  54. Yang Y, Li Q, Shu H, Zhou H, Li X, Hou L (2017) Characterization of the melanocortin-4 receptor gene from Spinibarbus hollandi and the association between its polymorphisms and S. hollandi growth traits. Fish Sci 83:967–976CrossRefGoogle Scholar
  55. 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
  56. Yu H, You X, Li J, Zhang X, Zhang S, Jiang S, Lin X, Lin HR, Meng Z, Shi Q (2018) A genome-wide association study on growth traits in orange-spotted grouper (Epinephelus coioides) with RAD-seq genotyping. Sci China Life Sci 61:934–946PubMedCrossRefGoogle Scholar
  57. 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
  58. 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 20:573–583PubMedCrossRefGoogle Scholar
  59. Zhou Z, Han K, Wu Y, Bai H, Ke Q, Pu F, Wang Y, Xu P (2019) Genome-wide association study of growth and body-shape-related traits in large yellow croaker (Larimichthys crocea) using ddRAD sequencing. Mar Biotechnol 21:655–670PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2020

Authors and Affiliations

  • Yang Yang
    • 1
    • 2
  • Lina Wu
    • 1
    • 2
  • Xi Wu
    • 1
    • 2
  • Bijun Li
    • 1
    • 2
  • Wenhua Huang
    • 1
    • 2
  • Zhuoying Weng
    • 1
    • 2
  • Zixuan Lin
    • 1
  • Leling Song
    • 1
    • 2
  • Yin Guo
    • 1
    • 2
  • Zining Meng
    • 1
    • 2
    • 3
    Email author
  • Xiaochun Liu
    • 1
    • 2
    • 3
    Email author
  • Junhong Xia
    • 1
    • 2
  1. 1.State Key Laboratory of Biocontrol, Institute of Aquatic Economic Animals and Guangdong Provincial Key Laboratory for Aquatic Economic Animals, Life Science SchoolSun Yat-sen UniversityGuangzhouPeople’s Republic of China
  2. 2.Southern Laboratory of Ocean Science and EngineeringZhuhaiPeople’s Republic of China
  3. 3.Guangdong Provincial Key Laboratory for Aquatic Economic AnimalsGuangzhouPeople’s Republic of China

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