Association of a Synonymous SNP of INHA Gene with Litter Size Trait in Indonesian Thin-Tailed Sheep
Abstract
The inhibin alpha (INHA) serves as a marker for the number of fully developed ovarian follicles and plays a crucial role in regulating the secretion of pituitary FSH (follicle-stimulating hormone) and the frequency of ovulation. This study aims to examine the effect of INHA gene polymorphisms on the litter size of thin-tailed sheep. Detection of single nucleotide polymorphisms (SNPs) in the INHA gene was performed using PCR and DNA sequencing techniques. A total of 45 ewes were included in the study. Three SNPs were identified: g.236311141G>C, g.236311367G>A, and g.236311368G>A. Further investigation of the g.236311367G > A variant revealed that individuals with the GA genotype had a significantly higher litter size than those with the AA or GG genotype (p<0.05). SNPs at positions g.236311141G/C and g.236311368G/A were non-synonymous mutations resulting in amino acid changes p.A225P and V301I, respectively. Our results suggest that g.236311367G>A loci may serve as a potential molecular marker for improving the litter size trait in thin-tailed sheep.
References
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Nikitkina, E., A. Krutikova, A. Musidray, & K. Plemyashov. 2021. Search for Associations of FSHR, INHA, INHAB, PRL, TNP2 and SPEF2 Genes polymorphisms with semen quality in Russian holstein bulls (pilot study). Animals 11:2882. https://doi.org/10.3390/ani11102882
Pan, X., S. Liu, F. Li, W. Wang, C. Li, Y. Ma, & T. Li. 2014. Molecular characterization, expression profiles of the ovine FSHR gene and its association with litter size. Mol. Biol. Rep. 41:7749–7754. https://doi.org/10.1007/s11033-014-3666-8
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Sambrook, J. & D. Russell. 2001. Molecular Cloning: a Laboratory Manual. 3rd ed. Cold Spring Harbor Laboratory Press, New York.
Su, P., Y. Luo, Y. Huang, Z. Akhatayeva, D. Xin, Z. Guo, C. Pan, Q. Zhang, H. Xu, & X. Lan. 2022. Short variation of the sheep PDGFD gene is correlated with litter size. Gene 844:146797. https://doi.org/10.1016/j.gene.2022.146797
Tao, L., X. He, X. Wang, R. Di, & M. Chu. 2021. Litter size of sheep (Ovis aries): inbreeding depression and homozygous regions. Gene 12:109. https://doi.org/10.3390/genes12010109
Tian, X., H. Sun, & Y. Wang. 2010. Genetic polymorphism of INHA gene and its effect on litter size in three sheep breeds. Journal Northwest A F University Natural 38:23-29.
Vaishnav, S., A. Chauhan, A. Ajay, B. L. Saini, S. Kumar, A. Kumar, B. Bhushan, & G. K. Gaur. 2023. Allelic to Genome Wide Perspectives of Swine Genetic Variation to litter size and its component traits. Mol. Biol. Rep. 50:3705-3721. https://doi.org/10.1007/s11033-022-08168-5
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Wang, W., Y. La, F. Li, S. Liu, X. Pan, C. Li, & X. Zhang. 2020. Molecular characterization and expression profiles of the ovine Lhβ gene and its association with litter size in Chinese indigenous small-tailed han sheep. Animals 10:460. https://doi.org/10.3390/ani10030460
Wasti, S., N. Sah, D. L. Kuehu, Y. S. Kim, R. Jha, & B. Mishra. 2020. Expression of follistatin is associated with egg formation in the oviduct of laying hens. Anim. Sci. J. 91:e13396. https://doi.org/10.1111/asj.13396
Wijayanti, D., S. Zhang, Y. Yang, Y. Bai, Z. Akhatayeva, C. Pan, H. Zhu, L. Qu, & X. Lan. 2022. Goat SMAD family member 1 (SMAD1): MRNA expression, genetic variants, and their associations with litter size. Theriogenology 193:11–19. https://doi.org/10.1016/j.theriogenology.2022.09.001
Yu, D. Y., R. Z. Wu, Y. Zhao, Z. H. Nie, L. Wei, T. Y. Wang, & Z. P. Liu. 2019. Polymorphisms of four candidate genes and their correlations with growth traits in blue fox (Alopex lagopus). Genes 717:143987. https://doi.org/10.1016/j.gene.2019.143987
Yuan, Z., Li, W., Li, & Yue. 2019. Association of polymorphisms in candidate genes with the litter size in two sheep breeds. Animals 9:958. https://doi.org/10.3390/ani9110958
Yue, L., W. Li, Y. Pan, X. Lan, Q. Zhang, & C. Pan. 2023. Polymorphism of GTF2A1 gene is associated with litter size in sheep. Theriogenology 208:194–200. https://doi.org/10.1016/j.theriogenology.2023.06.004
Zhang, Z., X. He, Q. Liu, J. Tang, R. Di, & M. Chu. 2020. TGIF1 and SF1 polymorphisms are associated with litter size in small tail han sheep. Reprod. Domest. Anim. 55:1145–53. https://doi.org/10.1111/rda.13753
Zhang, Z., Q. Liu, R. Di, W. Hu, X. Wang, X. He, L. Ma, & M. Chu. 2019. Single nucleotide polymorphisms in BMP2 and BMP7 and the association with litter size in small tail han sheep. Anim. Reprod. Sci. 204:183–92. https://doi.org/10.1016/j.anireprosci.2019.04.001
Bian, Z., K. Li, S. Chen, C. Man, F. Wang, & L. Li. 2023. Association between INHA gene polymorphisms and litter size in hainan black goats. PeerJ 11:e15381. https://doi.org/10.7717/peerj.15381
Badan Pusat Statistik. 2023. Produksi Daging Domba menurut Provinsi, 2021-2023. https://www.bps.go.id/id/statistics-table/2/NDgzIzI=/produksi-daging-domba-menurut-provinsi.html
Calvo, J. H., L. Chantepie, M. Serrano, M. P. Sarto, L. P. Iguacel, M. Á. Jiménez, J. L. Alabart, J. Folch, S. Fabre, & B. Lahoz. 2020. A new allele in the BMP15 Gene (FecXRA) that affects prolificacy co-segregates with FecXR and FecXGR in rasa aragonesa sheep. Theriogenology 144:107–111. https://doi.org/10.1016/j.theriogenology.2020.01.010
Chen, S., L. Tao, X. He, R. Di, X. Wang, & M. Chu. 2021. Single-nucleotide polymorphisms in FLT3, NLRP5, and TGIF1 are associated with litter size in small-tailed han sheep. Arch. Anim. Breed. 64:475–486. https://doi.org/10.5194/aab-64-475-2021
Chu, M. X., Z. H. Liu, C. L. Jiao, Y. Q. He, L. Fang, S. C. Ye, G. H. Chen, & J. Y. Wang. 2007. Mutations in BMPR-IB and BMP-15 genes are associated with litter size in small tailed han sheep (Ovis aries), J. Anim. Sci. 85:598–603. https://doi.org/10.2527/jas.2006-324
Cui, Z., X. Shen, X. Zhang, F. Li, F. K. Amevor, Q. Zhu, Y. Wang, D. Li, G. Shu, Y. Tian, & X. Zhao. 2021. A functional polymorphism of inhibin alpha subunit at MiR-181b-1-3p-binding site regulates proliferation and apoptosis of chicken ovarian granular cells. Cell Tissue Res. 384:545–560. https://doi.org/10.1007/s00441-020-03356-w
Dolatabady, M. M., S. Safari, P. Aslanlo, H. Soleimani, & J. H. Zad. 2022. Polymorphism of the ovine BMP15, INHBA and INHA candidate genes for litter size in four Iranian indigenous sheep using PCR-sequencing. JLST 10:1–8.
Grieco, V., B. Banco, A. Ferrari, A. Rota, M. Faustini, & M. C. Veronesi. 2011. Inhibin-α immunohistochemical expression in mature and immature canine sertoli and leydig cells. Reprod. Domest. Anim. 46:920–923. https://doi.org/10.1111/j.1439-0531.2011.01784.x
Haile, A., T. Getachew, T. Mirkena, G. Duguma, S. Gizaw, M. Wurzinger, J. Soelkner, O. Mwai, T. Dessie, A. Abebe, Z. Abate, T. Jembere, M. Rekik, R. N. B. Lobo, J. M. Mwacharo, Z. G. Terfa, G. T. Kassie, J. P. Mueller, & B. Rischkowsky. 2020. Community-based sheep breeding programs generated substantial genetic gains and socioeconomic benefits. Animal 14:1362–1370. https://doi.org/10.1017/S1751731120000269
He, X., Z. Zhang, Q. Liu, & M. Chu. 2019. Polymorphisms of the melatonin receptor 1A gene that affects the reproductive seasonality and litter size in small tail han sheep. Reprod. Domest. Anim. 54:1400–1410. https://doi.org/10.1111/rda.13538
Heath, D. A., J. L. Pitman, & K. P. McNatty. 2017. Molecular forms of ruminant BMP15 and GDF9 and putative interactions with receptors. Reproduction 154:521-534. https://doi.org/10.1530/REP-17-0188
Ibrahim, A., I. G. S. Budisatria, R. Widayanti, & W. T. Artama. 2020. The genetic profiles and maternal origin of local sheep breeds on Java Island (Indonesia) based on complete mitochondrial DNA D-loop sequences. Vet. World 13:2625-2634. https://doi.org/10.14202/vetworld.2020.2625-2634
Isa, A. M., M. N. Bemji, M. Wheto, T. J. Williams, & E. M. Ibeagha-Awemu. 2017. Mutations in inhibin alpha gene and their association with litter size in Kalahari Red and Nigerian goats. Livest. Sci. 203:106-109. https://doi.org/10.1016/j.livsci.2017.07.012
Li, M., N. He, R. Sun, Y. Deng, X. Wen, & J. Zhang. 2022. Expression and polymorphisms of SMAD1, SMAD2 and SMAD3 genes and their association with litter size in tibetan sheep (Ovis aries). Genes 13:2307. https://doi.org/10.3390/genes13122307
Li, W., S. Chen, H. Li, Z. Liu, Y. Zhao, L. Chen, X. Zhou, & C. Li. 2016. A New insertion/deletion fragment polymorphism of inhibin-α gene associated with follicular cysts in large white sows. J. Vet. Med. Sci. 78:473–476. https://doi.org/10.1292/jvms.14-0489
Liu, C., Q. Wei, P. Li, Y. Wu, W. Wu, Q. Li, R. Huang, & F. Shi. 2017a. Association of polymorphism of 5′ UTR region at the INHA gene and the litter size in the Suhuai pig. Journal Nanjing Agricultural University 40:1119-1124.
Liu, Q. Y., Y. Q. He, Y. Ge, M. X. Chu, M. Jin, Y. J. Zhang, J. Y. Wang, X. K. Ma, R. Di, D. W. Huang, & N. Li. 2017b. Polymorphism of inhibin a gene and its relationship with litter size in Chinese indigenous goat. JAPS 27:1488-1495. https://www.thejaps.org.pk/docs/v-27-05/12.pdf
Martínez-Royo, A., B. Lahoz, J. L. Alabart, J. Folch, & J. H. Calvo. 2012. Characterisation of the Melatonin Receptor 1A (MTNR1A) Gene in the Rasa Aragonesa Sheep Breed: Association with Reproductive Seasonality. Anim. Reprod. Sci. 133:169–175. https://doi.org/10.1016/j.anireprosci.2012.06.018
Mazinani, M. & B. Rude. 2020. Population, world production and quality of sheep and goat products. Am. J. Anim. Vet. Sci. 4:291–299. https://doi.org/10.3844/ajavsp.2020.291.299
Ma, X., S. Liu, & S. Tian. 2023. A metaanalysis of mRNA expression profiling studies in sheep with different FecB genotypes. Anim. Genet. 54:225-238. https://doi.org/10.1111/age.13304
Nikitkina, E., A. Krutikova, A. Musidray, & K. Plemyashov. 2021. Search for Associations of FSHR, INHA, INHAB, PRL, TNP2 and SPEF2 Genes polymorphisms with semen quality in Russian holstein bulls (pilot study). Animals 11:2882. https://doi.org/10.3390/ani11102882
Pan, X., S. Liu, F. Li, W. Wang, C. Li, Y. Ma, & T. Li. 2014. Molecular characterization, expression profiles of the ovine FSHR gene and its association with litter size. Mol. Biol. Rep. 41:7749–7754. https://doi.org/10.1007/s11033-014-3666-8
Pillai, H. B. & R. T. Venkatachalapathy. 2020. Association of inhibin alpha gene polymorphism with litter size and growth in Malabari goats of India. Small Rumin. Res. 192:106188. https://doi.org/10.1016/j.smallrumres.2020.106188
Putra, W. P. B., Y. Alwi, & H. Suryani. 2021. Morphometrics characterization of Thin-Tail sheep in lowland and highland areas. Trop. Anim. Sci. J. 44:386-398. https://doi.org/10.5398/tasj.2021.44.4.386
Sambrook, J. & D. Russell. 2001. Molecular Cloning: a Laboratory Manual. 3rd ed. Cold Spring Harbor Laboratory Press, New York.
Su, P., Y. Luo, Y. Huang, Z. Akhatayeva, D. Xin, Z. Guo, C. Pan, Q. Zhang, H. Xu, & X. Lan. 2022. Short variation of the sheep PDGFD gene is correlated with litter size. Gene 844:146797. https://doi.org/10.1016/j.gene.2022.146797
Tao, L., X. He, X. Wang, R. Di, & M. Chu. 2021. Litter size of sheep (Ovis aries): inbreeding depression and homozygous regions. Gene 12:109. https://doi.org/10.3390/genes12010109
Tian, X., H. Sun, & Y. Wang. 2010. Genetic polymorphism of INHA gene and its effect on litter size in three sheep breeds. Journal Northwest A F University Natural 38:23-29.
Vaishnav, S., A. Chauhan, A. Ajay, B. L. Saini, S. Kumar, A. Kumar, B. Bhushan, & G. K. Gaur. 2023. Allelic to Genome Wide Perspectives of Swine Genetic Variation to litter size and its component traits. Mol. Biol. Rep. 50:3705-3721. https://doi.org/10.1007/s11033-022-08168-5
Wang, S. Z., E. Guang-Xin, Y. Zeng, Y. G. Han, Y. F. Huang, & R. S. Na. 2021. Three SNPs within exons of INHA and ACVR2B genes are significantly associated with litter size in dazu black goats. Reprod. Domest. Anim. 6:936–941. https://doi.org/10.1111/rda.13927
Wang, W., Y. La, F. Li, S. Liu, X. Pan, C. Li, & X. Zhang. 2020. Molecular characterization and expression profiles of the ovine Lhβ gene and its association with litter size in Chinese indigenous small-tailed han sheep. Animals 10:460. https://doi.org/10.3390/ani10030460
Wasti, S., N. Sah, D. L. Kuehu, Y. S. Kim, R. Jha, & B. Mishra. 2020. Expression of follistatin is associated with egg formation in the oviduct of laying hens. Anim. Sci. J. 91:e13396. https://doi.org/10.1111/asj.13396
Wijayanti, D., S. Zhang, Y. Yang, Y. Bai, Z. Akhatayeva, C. Pan, H. Zhu, L. Qu, & X. Lan. 2022. Goat SMAD family member 1 (SMAD1): MRNA expression, genetic variants, and their associations with litter size. Theriogenology 193:11–19. https://doi.org/10.1016/j.theriogenology.2022.09.001
Yu, D. Y., R. Z. Wu, Y. Zhao, Z. H. Nie, L. Wei, T. Y. Wang, & Z. P. Liu. 2019. Polymorphisms of four candidate genes and their correlations with growth traits in blue fox (Alopex lagopus). Genes 717:143987. https://doi.org/10.1016/j.gene.2019.143987
Yuan, Z., Li, W., Li, & Yue. 2019. Association of polymorphisms in candidate genes with the litter size in two sheep breeds. Animals 9:958. https://doi.org/10.3390/ani9110958
Yue, L., W. Li, Y. Pan, X. Lan, Q. Zhang, & C. Pan. 2023. Polymorphism of GTF2A1 gene is associated with litter size in sheep. Theriogenology 208:194–200. https://doi.org/10.1016/j.theriogenology.2023.06.004
Zhang, Z., X. He, Q. Liu, J. Tang, R. Di, & M. Chu. 2020. TGIF1 and SF1 polymorphisms are associated with litter size in small tail han sheep. Reprod. Domest. Anim. 55:1145–53. https://doi.org/10.1111/rda.13753
Zhang, Z., Q. Liu, R. Di, W. Hu, X. Wang, X. He, L. Ma, & M. Chu. 2019. Single nucleotide polymorphisms in BMP2 and BMP7 and the association with litter size in small tail han sheep. Anim. Reprod. Sci. 204:183–92. https://doi.org/10.1016/j.anireprosci.2019.04.001
Authors
AbuzahraM., WijayantiD., EffendiM. H., MustofaI., MunyanezaJ. P., EidL. A., & UgboE. N. (2024). Association of a Synonymous SNP of INHA Gene with Litter Size Trait in Indonesian Thin-Tailed Sheep. Tropical Animal Science Journal, 47(3), 273-279. https://doi.org/10.5398/tasj.2024.47.3.273
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