Abstract
Breeding program to improve economically important growth traits in striped catfish (Pangasianodon hypophthalmus) requires effective molecular markers. This study was conducted to identify single nucleotide polymorphisms (SNPs) of Insulin-like Growth Factor-Binding Protein 7 (IGFBP7) gene which plays multiple roles in regulating growth, energy metabolism and development. The association between SNPs in IGFBP7 gene and growth traits in striped catfish was analyzed in order to uncover the SNPs that have potential to be valuable markers for improving growth traits. Firstly, fragments of IGFBP7 gene from ten fast-growing fish and ten slow-growing fish were sequenced in order to discover SNPs. After filtering the detected SNPs, an intronic SNP (2060A > G) and two non-synonymous SNPs (344 T > C and 4559C > A) causing Leu78Pro and Leu189Met in protein, respectively, were subjected to further validated by individual genotyping in 70 fast-growing fish and 70 slow-growing fish using single base extension method. Our results showed that two SNPs (2060A > G and 4559 C > A (p. Leu189Met)) were significantly associated with the growth in P. hypophthalmus (p < 0.001), thus being candidate SNP markers for the growth traits of this fish. Moreover, linkage disequilibrium and association analysis with growth traits of haplotypes generated from the 3 filtered SNPs (344 T > C, 2060 A > G and 4559 C > A) were examined. These revealed that the non-coding SNP locus (2060A > G) had higher genetic diversity at which the G allele was predominant over the A allele in the fast-growing fish. Furthermore, the results of qPCR showed that expression of IGFBP7 gene with genotype GG (at locus 2060) in fast-growing group was significantly higher than that with genotype AA in slow-growing group (p < 0.05). Our study provides insights into the genetic variants of IGFBP7 gene and useful data source for development molecular marker for growth traits in breeding of the striped catfish.
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References
Allard JB, Duan C (2018) IGF-Binding Proteins: Why do they exist and why are there so many? Front Endocrinol 9:117. https://doi.org/10.3389/fendo.2018.00117
Chen B, Xiao W, Zou Z, Zhu J, Li D, Yu J, Yang H (2020) Ghrelin gene single nucleotide polymorphisms and their effects on Nile tilapia (Oreochromis niloticus) growth. Aquac Rep. 18:100469. https://doi.org/10.1016/j.aqrep.2020.100469
Chesnokov Y, Artemyeva AM (2015) Evaluation of the measure of polymorphism information of genetic diversity. Selskokhozyaist Biol. 50:571–578. https://doi.org/10.15389/agrobiology.2015.5.571eng
Chu M, Jia Y, Wu Z, Huan H, Guo X, Yin S, Zhang K (2022) Genome-wide characterization of three IGFs in hybrid yellow catfish (Pseudobagrus fulvidraco ♀× Pseudobagrus vachellii ♂) and the association of IGF2 allelic variants with growth traits. Aquac Rep. 26:101315. https://doi.org/10.1016/j.aqrep.2022.101315
Cuevas-Rodríguez B, Sifuentes-Rincón A, Ambriz-Morales P, García-Ulloa GM, Valdez González F, Rodríguez-González H (2016) Novel single nucleotide polymorphisms in candidate genes for growth in tilapia (Oreochromis niloticus). Rev Bras Zootec 45:345–348. https://doi.org/10.1590/S1806-92902016000600009
Delaserrana DG, Macqueen DJ (2018) Insulin-Like Growth Factor-Binding Proteins of teleost fishes. Front Endocrinol 9:80. https://doi.org/10.3389/fendo.2018.00080
Diopere E, Hellemans B, Volckaert FA, Maes GE (2013) Identification and validation of single nucleotide polymorphisms in growth- and maturation-related candidate genes in sole (Solea solea L). Mar Genom 9:33–38. https://doi.org/10.1016/j.margen.2012.09.001
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
FAO (2022) The state of world fisheries and aquaculture 2022. Towards blue transformation. Rome, FAO. https://doi.org/10.4060/cc0461en. Accessed 22 May 2022
Feng X, Yu X, Tong J (2014) Novel single nucleotide polymorphisms of the insulin-like growth factor-I gene and their associations with growth traits in common carp (Cyprinus carpio L.). Int J Mol Sci 15:22471–22482. https://doi.org/10.3390/ijms151222471
Fletcher R (2020) Catfish can be key drivers of global aquaculture growth. The Fish site. https://thefishsite.com/articles/catfish-can-be-key-drivers-of-global-aquaculture-growth. Accessed 8 Oct 2020
Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hu Z, Wu J, Qin L, Jin H, Cao Y, Zhao Y (2021) IGFBP7 downregulation or overexpression effect on bovine preadipocyte differentiation. Anim Biotechnol 32:21–30. https://doi.org/10.1080/10495398.2019.1642906
Hwa V, Oh Y, Rosenfeld RG (1999) The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr Rev 20:761–787. https://doi.org/10.1210/edrv.20.6.0382
Jiang L-S, Ruan Z-H, Lu Z-Q, Li Y-F, Luo Y-Y, Zhang X-Q, Liu W-S (2022) Novel SNPs in the 3’UTR region of GHRb gene associated with growth traits in striped catfish (Pangasianodon hypophthalmus), a valuable aquaculture species. Fishes 7:230. https://doi.org/10.3390/fishes7050230
Jo B-S, Choi SS (2015) Introns: The functional benefits of introns in genomes. Genomics Inform 13:112. https://doi.org/10.5808/GI.2015.13.4.112
Kamangar BB, Gabillard JC, Bobe J (2006) Insulin-like growth factor-binding protein (IGFBP)-1, -2, -3, -4, -5, and -6 and IGFBP-related protein 1 during rainbow trout postvitellogenesis and oocyte maturation: molecular characterization, expression profiles, and hormonal regulation. Endocrinology 147:2399–2410. https://doi.org/10.1210/en.2005-1570
Kim OTP, Nguyen PT, Shoguchi E, Hisata K, Vo TTB, Inoue J, Shinzato C, Le BTN, Nishitsuji K, Kanda M, Nguyen VH, Nong HV, Satoh N (2018) A draft genome of the striped catfish, Pangasianodon hypophthalmus, for comparative analysis of genes relevant to development and a resource for aquaculture improvement. BMC Genom 19:733. https://doi.org/10.1186/s12864-018-5079-x
Lau HE, Chalasani SH (2014) Divergent and convergent roles for insulin-like peptides in the worm, fly and mammalian nervous systems. Invert Neurosci 14:71–78. https://doi.org/10.1007/s10158-013-0166-9
Li W-H, Deng XM, Li Barr N, Wang SH, Zhao Y, Du Z, Zhang R, Wu KL, Wu CX (2005) Isolation of differentially expressed genes in double-muscling large white pig by SSH and q-PCR strategy. Prog Biochem Biophys 32:353–358
Li X, Bai J, Hu Y, Ye X, Li S, Yu L (2012) Genotypes, haplotypes and diplotypes of IGF-II SNPs and their association with growth traits in largemouth bass (Micropterus salmoides). Mol Biol Rep 39:4359–4365. https://doi.org/10.1007/s11033-011-1223-2
Li D, Lou Q, Zhai G, Peng X, Cheng X, Dai X, Zhuo Z, Shang G, Jin X, Chen X, Han D, He J, Yin Z (2014) Hyperplasia and cellularity changes in IGF-1-overexpressing skeletal muscle of crucian carp. Endocrinology 155:2199–2212. https://doi.org/10.1210/en.2013-1938
Li J, Liu J, Campanile G, Plastow G, Zhang C, Wang Z, Cassandro M, Gasparrini B, Salzano A, Hua G, Liang A, Yang L (2018) Novel insights into the genetic basis of buffalo reproductive performance. BMC Genom 19:814. https://doi.org/10.1186/s12864-018-5208-6
Liu J, Zhu K-C, Pan J-M, Guo H-Y, Liu B-S, Zhang N, Yang J-W, Zhang D-C (2023) Characterization of the MMP9 gene and its association with cryptocaryon irritans resistance traits in trachinotus ovatus (Linnaeus, 1758). Genes 14:475. https://doi.org/10.3390/genes14020475
Louro B, Martins RST, Pinto PIS, Reinhardt R, de Koning D-J, Canario AVM, Power DM (2019) SuperSAGE digital expression analysis of differential growth rate in a European sea bass population. Aquac Fish 4:17–26. https://doi.org/10.1016/j.aaf.2018.03.001
Mareco EA, Garcia de la Serrana D, Johnston IA, Dal-Pai-Silva M (2015) Characterization of the transcriptome of fast and slow muscle myotomal fibres in the pacu (Piaractus mesopotamicus). BMC Genom 16:182. https://doi.org/10.1186/s12864-015-1423-6
McCauley JL, Kenealy SJ, Margulies EH, Schnetz-Boutaud N, Gregory SG, Hauser SL, Oksenberg JR, Pericak-Vance MA, Haines JL, Mortlock DP (2007) SNPs in Multi-species Conserved Sequences (MCS) as useful markers in association studies: a practical approach. BMC Genom 8:266. https://doi.org/10.1186/1471-2164-8-266
McKinney GJ, Seeb JE, Seeb LW (2017) Managing mixed-stock fisheries: genotyping multi-SNP haplotypes increases power for genetic stock identification. Can J Fish Aquat 74:429–434. https://doi.org/10.1139/cjfas-2016-0443
Mehrabi F, Khalesi M, Farhadi A (2015) Polymorphism of insulin-like growth factor binding protein-3 (IGFBP-3) gene associated with growth traits in Cyprinus carpio L. Iran J Ichthyol. 2:172–176. https://doi.org/10.22034/iji.v2i3.43
Morgan JT, Fink GR, Bartel DP (2019) Excised linear introns regulate growth in yeast. Nature 565:606–611. https://doi.org/10.1038/s41586-018-0828-1
Mu XJ, Lu ZJ, Kong Y, Lam HYK, Gerstein MB (2011) Analysis of genomic variation in non-coding elements using population-scale sequencing data from the 1000 Genomes Project. Nucleic Acids Res 39:7058–7076. https://doi.org/10.1093/nar/gkr342
Nguyen SV, Klemetsdal G, Ødegård J, Gjøen HM (2012) Genetic parameters of economically important traits recorded at a given age in striped catfish (Pangasianodon hypophthalmus). Aquaculture 344–349:82–89. https://doi.org/10.1016/j.aquaculture.2012.03.013
Oh Y, Nagalla SR, Yamanaka Y, Kim H-S, Wilson E, Rosenfeld RG (1996) Synthesis and characterization of Insulin-like Growth Factor-binding Protein (IGFBP)-7: Recombinant human mac25 protein specifically binds IGF-I and -II*. J Biol Chem 271:30322–30325. https://doi.org/10.1074/jbc.271.48.30322
Ozcan-Gokcek E, Isik R, Karahan B, Gamsiz K (2020) Genetic variation of Insulin-like Growth Factor II (IGF-II) gene and its associations with growth traits in European sea bass (Dicentrarchus labrax). Turkish J Fish Aquat Sci 20:541–548. https://doi.org/10.4194/1303-2712-v20_7_04
Park JH, Gail MH, Weinberg CR, Carroll RJ, Chung CC, Wang Z, Chanock SJ, Fraumeni JF Jr, Chatterjee N (2011) Distribution of allele frequencies and effect sizes and their interrelationships for common genetic susceptibility variants. Proc Natl Acad Sci U S A 108:18026–18031. https://doi.org/10.1073/pnas.1114759108
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73
Sharker MR, Hossen S, Nou IS (2020) Characterization of Insulin-Like Growth Factor Binding Protein 7 (Igfbp7) and its potential involvement in shell formation and metamorphosis of Pacific abalone, Haliotis discus hannai. Int J Mol Sci 21:6529. https://doi.org/10.3390/ijms21186529
Shi YY, He L (2005) SHEsis, a powerful software platform for analyses of linkage disequilibrium, haplotype construction, and genetic association at polymorphism loci. Cell Res 15:97–98. https://doi.org/10.1038/sj.cr.7290272
Su J, Su J, Shang X, Wan Q, Chen X, Rao Y (2015) SNP detection of TLR8 gene, association study with susceptibility/resistance to GCRV and regulation on mRNA expression in grass carp, Ctenopharyngodon idella. Fish Shellfish Immunol 43:1–12. https://doi.org/10.1016/j.fsi.2014.12.005
Su JJ, Shang XY, Wan QY, Su JG (2018) SNP-based susceptibility-resistance association and mRNA expression regulation analyses of tlr7 to grass carp Ctenopharyngodon idella reovirus. J Fish Biol 92:1505–1525. https://doi.org/10.1111/jfb.13607
Suárez-Salgado D, Parra-Bracamonte M, Benavides-González F, Alfaro I, Rincón A, Moreno-Medina V, Rosa-Reyna X (2020) Non-synonymous polymorphisms in candidate gene associated with growth traits in channel catfish (Ictalurus punctatus, Rafinesque, 1818). Mol Biol Rep 47:87–95. https://doi.org/10.1007/s11033-019-05110-0
Sun Y, Li Q, Wang G, Zhu D, Chen J, Li P, Tong J (2017) Polymorphisms in the Myostatin-1 gene and their association with growth traits in Ancherythroculter nigrocauda. Chin J Oceanol Limnol 35:597–602. https://doi.org/10.1007/s00343-017-5317-0
Syvanen AC (1999) From gels to chips: “minisequencing” primer extension for analysis of point mutations and single nucleotide polymorphisms. Hum Mutat 13:1–10. https://doi.org/10.1002/(sici)1098-1004(1999)13:1%3c1::aid-humu1%3e3.0.co;2-i
Tian C, Yang M, Lv L, Yuan Y, Liang X, Guo W, Song Y, Zhao C (2014) Single nucleotide polymorphisms in growth hormone gene and their association with growth traits in Siniperca chuatsi (Basilewsky). Int J Mol Sci 15:7029–7036. https://doi.org/10.3390/ijms15047029
Tran TTH, Nguyen HT, Le BTN, Tran PH, Nguyen SV, Kim OTP (2021) Characterization of single nucleotide polymorphism in IGF1 and IGF1R genes associated with growth traits in striped catfish (Pangasianodon hypophthalmus Sauvage, 1878). Aquaculture 538:736542. https://doi.org/10.1016/j.aquaculture.2021.736542
Tsai HY, Hamilton A, Guy DR, Houston RD (2014) Single nucleotide polymorphisms in the insulin-like growth factor 1 (IGF1) gene are associated with growth-related traits in farmed Atlantic salmon. Anim Genet 45:709–715. https://doi.org/10.1111/age.12202
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3-new capabilities and interfaces. Nucleic Acids Res 40:115. https://doi.org/10.1093/nar/gks596
Vaiman D, Mercier D, Moazami-Goudarzi K, Eggen A, Ciampolini R, Lépingle A, Velmala R, Kaukinen J, Varvio SL, Martin P (1994) A set of 99 cattle microsatellites: characterization, synteny mapping, and polymorphism. Mamm Genome 5:288–297. https://doi.org/10.1007/bf00389543
Wang G, Li N, Zhang L, Zhang L, Zhang Z, Wang Y (2015) IGFBP7 promotes hemocyte proliferation in small abalone Haliotis diversicolor, proved by dsRNA and cap mRNA exposure. Gene 571:65–70. https://doi.org/10.1016/j.gene.2015.06.051
Wang H, Li B, Yang L, Jiang C, Zhang T, Liu S (2022) Expression profiles and transcript properties of fast-twitch and slow-twitch muscles in a deep-sea highly migratory fish. Pseudocaranx Dentex. Peer J 10:12720. https://doi.org/10.7717/peerj.12720
Wei KY, Xie SM, Wang ST, Chen YK, Niu DH, Li JL (2019) Polymorphism of SNPs in EGFR intron 1 and its association with growth traits in Sinonovacula constricta. J Fish China 43:483–491
Wood AW, Duan C, Bern HA (2005) Insulin-like growth factor signaling in fish. Int Rev Cytol 243:215–285. https://doi.org/10.1016/s0074-7696(05)43004-1
Yamanaka Y, Wilson EM, Rosenfeld RG, Oh Y (1997) Inhibition of insulin receptor activation by insulin-like growth factor binding proteins. J Biol Chem 272:30729–30734. https://doi.org/10.1074/jbc.272.49.30729
Yang Q, Li X, Shi R, Cheng P, Wang N, Chen S (2022) The female-biased expression, transcriptional regulation and knock-down effect of insulin-like growth factor binding protein 7 in Chinese tongue sole Cynoglossus semilaevis. Aquaculture 551:737956. https://doi.org/10.1016/j.aquaculture.2022.737956
Zhang H, Zhao C, Yin S, Li Z, Cao Q, Li X, Xie W, Zhang J, Zhu W, Wang D (2018) Characterization and identification of single nucleotide polymorphism within the IGF-1R gene associated with growth traits of Odontobutis potamophila. J World Aquac Soc 49:366–379. https://doi.org/10.1111/jwas.12504
Zhang S, Li X, Chen X, Pan J, Wang M, Zhong L, Qin Q, Bian W (2019) Significant associations between prolactin gene polymorphisms and growth traits in the channel catfish (Ictalurus punctatus Rafinesque, 1818) core breeding population. Meta Gene 19:32–36. https://doi.org/10.1016/j.mgene.2018.10.006
Zhang M, Yang Q, Shi R, Wang J, Zhang Z, Yang Y, Li W, Chen S, Wang N (2022) Effects of long-term sex steroid hormones (estradiol and testosterone)–supplemented feeds on the growth performance of Chinese tongue sole (Cynoglossus semilaevis). Fish Physiol Biochem 48:1365–1375. https://doi.org/10.1007/s10695-022-01125-w
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This work is funded by Vietnam National Foundation for Science and Technology Development (NAFOSTED) under grant number 106.05-2017.29 to Oanh Thi Phuong Kim.
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Oanh TP Kim designed the project. Sang VN prepared for sampling. Trang THT, Hoang ST, BTNL and H–AV extracted DNA, RNA, PCR, qPCR and Sequencing. Trang THT and HST performed multiplex SNaPshot assay. Oanh TK and Trang TH Tran analyzed SNP data and transcriptional expression data. Oanh TP Kim and Trang TH Tran prepared the manuscript. All authors edited and commented on the manuscript.
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Tran, T.T.H., Tran, H.S., Le, B.T.N. et al. Novel single nucleotide polymorphisms of insulin-like growth factor-binding protein 7 (IGFBP7) gene significantly associated with growth traits in striped catfish (Pangasianodon hypophthalmus Sauvage, 1878). Mol Genet Genomics 298, 883–893 (2023). https://doi.org/10.1007/s00438-023-02016-2
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DOI: https://doi.org/10.1007/s00438-023-02016-2