vetpressАграрная наукаAgrarian science0869-81552686-701XРедакция журнала "Аграрная наука"10.32634/0869-8155-2023-372-7-31-39vetpress-2696Research ArticleЗООТЕХНИЯ И ВЕТЕРИНАРИЯZOOTECHNICS AND VETERINARY MEDICINEГенетическая архитектура признаков воспроизводства свиней породы ландрас российской репродукцииGenetic architecture of reproductive traits in Russian Landrace pigshttps://orcid.org/0000-0001-7533-4281БелоусА. А.BelousA. A.

Анна Александровна Белоус, кандидат биологических наук, лаборатория генетических технологий в агро- и аквахозяйстве,

Дубровицы, 60, Подольск, Московская обл., 142132

Anna Alexandrovna Belous, Сandidate of biological sciences, Laboratory of genetic technologies in agrarian and aquatic husbandry,

60 Dubrovitsy, Podolsk Municipal District, Moscow Region, 142132

belousa663@gmail.comhttps://orcid.org/0000-0002-2080-0182ВолковаВ. В.VolkovaV. V.

Валерия Владимировна Волкова, кандидат биологических наук, лаборатория функциональной и эволюционной геномики животных,

Дубровицы, 60, Подольск, Московская обл., 142132

Valeria Vladimirovna Volkova, Сandidate of biological sciences, Laboratory of functional and evolutional animal genomics,

60 Dubrovitsy, Podolsk Municipal District, Moscow Region, 142132

moonlit-elf@mail.ruhttps://orcid.org/0000-0002-4874-2615РешетниковаА. А.ReshetnikovaA. A.

Анастасия Александровна Решетникова, младший научный сотрудник, лаборатория генетических технологий в агро- и аквахозяйстве,

Дубровицы, 60, Подольск, Московская обл., 142132

Anastasia Alexandrovna Reshetnikova, junior researcher, Laboratory of genetic technologies in agrarian and aquatic husbandry,

60 Dubrovitsy, Podolsk Municipal District, Moscow Region, 142132

reshetnikova.aa@yandex.ruhttps://orcid.org/0000-0002-1153-5815ОтрадновП. И.OtradnovP. I.

Петр Ильич Отраднов, младший научный сотрудник, лаборатория генетических технологий в агро- и аквахозяйстве, отдел популяционной генетики и генетических основ разведения животных,

Дубровицы, 60, Подольск, Московская обл., 142132

Petr Il’ich Otradnov, junior researcher, Laboratory of genetic technologies in agrarian and aquatic husbandry, department of population genetics and genetic foundations of animalbreeding,

60 Dubrovitsy, Podolsk Municipal District, Moscow Region, 142132

deriteronard@gmail.comhttps://orcid.org/0000-0003-4017-6863ЗиновьеваН. А.ZinovyevaN. A.

Наталия Анатольевна Зиновьева, доктор биологических наук, академик РАН, профессор, директор,

Дубровицы, 60, Подольск, Московская обл., 142132

Nataliya Anatolyevna Zinovyeva, Doctor of Biological Sciences, Academician of the Russian Academy of Sciences, Professor, Director,

60 Dubrovitsy, Podolsk Municipal District, Moscow Region, 142132

priemnaya-vij@mail.ruФедеральный исследовательский центр животноводства — ВИЖ им. академика Л.К. ЭрнстаРоссияFederal Research Center of Animal Husbandry — VIZ academician L.K. ErnstRussian Federation202324072023073139Copyright © Белоус А.А., Волкова В.В., Решетникова А.А., Отраднов П.И., Зиновьева Н.А., 20232023Белоус А.А., Волкова В.В., Решетникова А.А., Отраднов П.И., Зиновьева Н.А.Belous A.A., Volkova V.V., Reshetnikova A.A., Otradnov P.I., Zinovyeva N.A.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.vetpress.ru/jour/article/view/2696Актуальность

Актуальность. В настоящее время развитие молекулярной и популяционной генетики является актуальной задачей. Необходимость выявления достоверных генов-кандидатов связано с увеличением поголовья свиней и увеличением качества выходной продукции — как племенной, так и мясной. В связи с этим метод полногеномного анализа решает вопросы генетической обусловленности количественных и хозяйственно полезных признаков.

Методы

Методы. В исследовании метод GWAS применялся по воспроизводительным показателям свиноматок породы ландрас.

Результаты

Результаты. Были выявлены и описаны 35 достоверных и имеющих биологический функционал генов-кандидатов, расположенных вблизи или внутри идентифицированных значимых SNP, и отвечающих за различные воспроизводительные показатели организма свиноматок. Гены были отнесены к двум кластерам, из них 20 генов относились к 1-му кластеру, отвечавшему за митохондриальный и сопряженный транспорт электронов, синтез АТФ, а также связывание жирных кислот и триптофана (AFF4, IL13, IL4, IRF1, SHROOM1, IL-5, UQCRQ, MRPL13, TTR, ENPEP, NOL4, PCDH7, DSG3, RASSF6, ALB, AFP, ANKRD17, SOX9), и 15 — ко 2-му, связанному с ответом на бактериальную и вирусную инфекцию (YTHDC2, KIF3A, EYA1, DSG2, DSG4, PPIH, RNF125, TRAPPC8, PITX2, KIAA1462, MTPAP, JMJD6, METTL23, SRSF2 и U2AF1).

Relevance

Relevance. Currently, the development of molecular and population genetics is a relevant task. The need to identify reliable candidate genes is associated with increase in pig population and quality improvement of both breeding and meat products. In this regard, the whole-genome analysis method solves issues of the genetic determination in quantitative and economically important traits.

Methods

Methods. In this study, the GWAS method was applied to reproductive traits of Landrace sows.

Results

Results. 35 reliable candidate genes with biological functionality were identified and described, located near or within the identified significant SNP, responsible for various reproductive traits of sow organisms. Genes were classified into two clusters — 20 genes belonged to Cluster 1, which was responsible for mitochondrial and coupled electron transport, ATP synthesis, as well as binding of fatty acids and tryptophan (AFF4, IL13, IL4, IRF1, SHROOM1, IL-5, UQCRQ, MRPL13, TTR, ENPEP, NOL4, PCDH7, DSG3, RASSF6, ALB, AFP, ANKRD17, SOX9), and 15 genes belonged to Cluster 2, which was associated with response to bacterial and viral infections (YTHDC2, KIF3A, EYA1, DSG2, DSG4, PPIH, RNF125, TRAPPC8, PITX2, KIAA1462, MTPAP, JMJD6, METTL23, SRSF2, and U2AF1).

генетическая архитектураполногеномное ассоциативное исследованиепоказатели воспроизводствагены-кандидатысвиноматки породы ландрасgenetic architectureGWASreproduction traitscandidate geneslandrace sowsИсследование выполнено при финансовой поддержке Российского научного фонда (проект № 21-76-10038).The research was carried out with the financial support of the Russian Science Foundation (project No. 21-76-10038).ReferencesTeng G., Yu Q. Pig behavior research and its application in breeding-landrace pigs as an example. Biomedical Research. 2017; 28 (Spec. Iss.): 111–117.Teng G., Yu Q. Pig behavior research and its application in breeding-landrace pigs as an example. Biomedical Research. 2017; 28 (Spec. Iss.): 111–117.Alam M., Chang H.-K., Lee S.-S., Choi T.-J. Genetic analysis of major production and reproduction traits of Korean Duroc, Landrace and Yorkshire pigs. Animals. 2021; 11(5): 1321. https://doi.org/10.3390/ani11051321Alam M., Chang H.-K., Lee S.-S., Choi T.-J. Genetic analysis of major production and reproduction traits of Korean Duroc, Landrace and Yorkshire pigs. Animals. 2021; 11(5): 1321. https://doi.org/10.3390/ani11051321Sato S. et al. SNP- and haplotype-based genome-wide association studies for growth, carcass, and meat quality traits in a Duroc multigenerational population. BMC Genetics. 2016; 17: 60. https://doi.org/10.1186/s12863-016-0368-3Sato S. et al. SNP- and haplotype-based genome-wide association studies for growth, carcass, and meat quality traits in a Duroc multigenerational population. BMC Genetics. 2016; 17: 60. https://doi.org/10.1186/s12863-016-0368-3Sevón-Aimonen M.-L., Uimari P. Heritability of sow longevity and lifetime prolificacy in Finnish Yorkshire and Landrace pigs. Agricultural and Food Science. 2013; 22(3): 325–330. https://doi.org/10.23986/afsci.7991Sevón-Aimonen M.-L., Uimari P. Heritability of sow longevity and lifetime prolificacy in Finnish Yorkshire and Landrace pigs. Agricultural and Food Science. 2013; 22(3): 325–330. https://doi.org/10.23986/afsci.7991Ogawa S., Kimata M., Ishii K., Uemoto Y., Satoh M. Genetic analysis for sow stayability at different parities in purebred Landrace and Large White pigs. Animal Science Journal. 2021; 92(1): e13599. https://doi.org/10.1111/asj.13599Ogawa S., Kimata M., Ishii K., Uemoto Y., Satoh M. Genetic analysis for sow stayability at different parities in purebred Landrace and Large White pigs. Animal Science Journal. 2021; 92(1): e13599. https://doi.org/10.1111/asj.13599Wu P. et al. Single step genome-wide association studies based on genotyping by sequence data reveals novel loci for the litter traits of domestic pigs. Genomics. 2018; 110(3): 171–179. https://doi.org/10.1016/j.ygeno.2017.09.009Wu P. et al. Single step genome-wide association studies based on genotyping by sequence data reveals novel loci for the litter traits of domestic pigs. Genomics. 2018; 110(3): 171–179. https://doi.org/10.1016/j.ygeno.2017.09.009Sell-Kubiak E., Dobrzanski J., Derks M.F.L., Lopes M.S., Szwaczkowski T. Meta-analysis of SNPs determining litter traits in pigs. Genes. 2022; 13(10): 1730. https://doi.org/10.3390/genes13101730Sell-Kubiak E., Dobrzanski J., Derks M.F.L., Lopes M.S., Szwaczkowski T. Meta-analysis of SNPs determining litter traits in pigs. Genes. 2022; 13(10): 1730. https://doi.org/10.3390/genes13101730Guo X., Su G., Christensen O.F., Janss L., Lund M.S. Genome-wide association analyses using a Bayesian approach for litter size and piglet mortality in Danish Landrace and Yorkshire pigs. BMC Genomics. 2016; 17: 468.https://doi.org/10.1186/s12864-016-2806-zGuo X., Su G., Christensen O.F., Janss L., Lund M.S. Genome-wide association analyses using a Bayesian approach for litter size and piglet mortality in Danish Landrace and Yorkshire pigs. BMC Genomics. 2016; 17: 468. https://doi.org/10.1186/s12864-016-2806-zAn S.M. et al. Effect of single nucleotide polymorphisms in IGFBP2 and IGFBP3 genes on litter size traits in Berkshire pigs. Animal Biotechnology. 2018; 29(4): 301–308. https://doi.org/10.1080/10495398.2017.1395345An S.M. et al. Effect of single nucleotide polymorphisms in IGFBP2 and IGFBP3 genes on litter size traits in Berkshire pigs. Animal Biotechnology. 2018; 29(4): 301–308. https://doi.org/10.1080/10495398.2017.1395345Fabbri M.C. et al. Identification of candidate genes associated with bacterial and viral infections in wild boars hunted in Tuscany (Italy). Scientific Reports. 2022; 12: 8145. https://doi.org/10.1038/s41598-022-12353-8Fabbri M.C. et al. Identification of candidate genes associated with bacterial and viral infections in wild boars hunted in Tuscany (Italy). Scientific Reports. 2022; 12: 8145. https://doi.org/10.1038/s41598-022-12353-8Lin C. et al. AFF4, a component of the ELL/P-TEFb elongation complex and a shared subunit of MLL chimeras, can link transcription elongation to leukemia. Molecular Cell. 2010; 37(3): 429–437. https://doi.org/10.1016/j.molcel.2010.01.026Lin C. et al. AFF4, a component of the ELL/P-TEFb elongation complex and a shared subunit of MLL chimeras, can link transcription elongation to leukemia. Molecular Cell. 2010; 37(3): 429–437. https://doi.org/10.1016/j.molcel.2010. 01.026Wang M. et al. Associations of IL-4, IL-4R, and IL-13 gene polymorphisms in coal workersʼ pneumoconiosis in China: a case-control study. PLoS ONE. 2011; 6(8): e22624. https://doi.org/10.1371/journal.pone.0022624Wang M. et al. Associations of IL-4, IL-4R, and IL-13 gene polymorphisms in coal workersʼ pneumoconiosis in China: a case-control study. PLoS ONE. 2011; 6(8): e22624. https://doi.org/10.1371/journal.pone.0022624Dawson H.D. et al. Molecular and metabolomic changes in the proximal colon of pigs infected with Trichuris suis. Scientific Reports. 2020; 10: 12853. https://doi.org/10.1038/s41598-020-69462-5Dawson H.D. et al. Molecular and metabolomic changes in the proximal colon of pigs infected with Trichuris suis. Scientific Reports. 2020; 10: 12853. https://doi.org/10.1038/s41598-020-69462-5.Liu Y. et al. Effect of single nucleotide polymorphism of IRF1 gene on cytokine traits in three pig breeds. Journal of Animal and Veterinary Advances. 2010; 9(18): 2346–2350. https://doi.org/10.3923/javaa.2010.2346.2350Liu Y. et al. Effect of single nucleotide polymorphism of IRF1 gene on cytokine traits in three pig breeds. Journal of Animal and Veterinary Advances. 2010; 9(18): 2346–2350. https://doi.org/10.3923/javaa.2010.2346.2350Zhao Z. et al. Suppression of SHROOM1 improves in vitro and in vivo gene integration by promoting homology-directed repair. International Journal of Molecular Sciences. 2020; 21(16): 5821. https://doi.org/10.3390/ijms21165821Zhao Z. et al. Suppression of SHROOM1 improves in vitro and in vivo gene integration by promoting homology-directed repair. International Journal of Molecular Sciences. 2020; 21(16): 5821. https://doi.org/10.3390/ijms21165821Xing K. et al. Identification of genes for controlling swine adipose deposition by integrating transcriptome, whole-genome resequencing, and quantitative trait loci data. Scientific Reports. 2016; 6: 23219. https://doi.org/10.1038/srep23219Xing K. et al. Identification of genes for controlling swine adipose deposition by integrating transcriptome, whole-genome resequencing, and quantitative trait loci data. Scientific Reports. 2016; 6: 23219. https://doi.org/10.1038/srep23219Keel B.N. et al. RNA-Seq Meta-analysis identifies genes in skeletal muscle associated with gain and intake across a multi-season study of crossbred beef steers. BMC Genomics. 2018; 19: 430. https://doi.org/10.1186/s12864-018-4769-8Keel B.N. et al. RNA-Seq Meta-analysis identifies genes in skeletal muscle associated with gain and intake across a multi-season study of crossbred beef steers. BMC Genomics. 2018; 19: 430. https://doi.org/10.1186/s12864-018- 4769-8Kong R.S.G., Liang G., Chen Y., Stothard P., Guan L.L. Transcriptome profiling of the rumen epithelium of beef cattle differing in residual feed intake. BMC Genomics. 2016; 17: 592. https://doi.org/10.1186/s12864-016-2935-4Kong R.S.G., Liang G., Chen Y., Stothard P., Guan L.L. Transcriptome profiling of the rumen epithelium of beef cattle differing in residual feed intake. BMC Genomics. 2016; 17: 592. https://doi.org/10.1186/s12864-016-2935-4Cai M., Li H., Chen R., Zhou X. MRPL13 promotes tumor cell proliferation, migration and EMT process in breast cancer through the PI3K-AKT-mTOR pathway. Cancer Management and Research. 2021; 13: 2009–2024. https://doi.org/10.2147/CMAR.S296038Cai M., Li H., Chen R., Zhou X. MRPL13 promotes tumor cell proliferation, migration and EMT process in breast cancer through the PI3K-AKT-mTOR pathway. Cancer Management and Research. 2021; 13: 2009–2024. https://doi.org/10.2147/CMAR.S296038Drag M.H., Kogelman L.J.A., Maribo H., Meinert L., Thomsen P.D., Kadarmideen H.N. Characterization of eQTLs associated with androstenone by RNA sequencing in porcine testis. Physiological Genomics. 2019; 51(10): 488–499. https://doi.org/10.1152/physiolgenomics.00125.2018Drag M.H., Kogelman L.J.A., Maribo H., Meinert L., Thomsen P.D., Kadarmideen H.N. Characterization of eQTLs associated with androstenone by RNA sequencing in porcine testis. Physiological Genomics. 2019; 51(10): 488–499. https://doi.org/10.1152/physiolgenomics.00125.2018Gaudet P., Livstone M.S., Lewis S.E., Thomas P.D. Phylogenetic-based propagation of functional annotations within the Gene Ontology consortium. Briefings in Bioinformatics. 2011; 12(5): 449–462. https://doi.org/10.1093/bib/bbr042Gaudet P., Livstone M.S., Lewis S.E., Thomas P.D. Phylogenetic-based propagation of functional annotations within the Gene Ontology consortium. Briefings in Bioinformatics. 2011; 12(5): 449–462. https://doi.org/10.1093/bib/ bbr042Tang Z. et al. Genome-wide association study reveals candidate genes for growth relevant traits in pigs. Frontiers in Genetics 2019; 10: 302. https://doi.org/10.3389/fgene.2019.00302Tang Z. et al. Genome-wide association study reveals candidate genes for growth relevant traits in pigs. Frontiers in Genetics 2019; 10: 302. https://doi.org/10.3389/fgene.2019.00302Holmes R.S., Spradling-Reeves K.D., Cox L.A. Mammalian glutamyl aminopeptidase genes (ENPEP) and proteins: Comparative studies of a major contributor to arterial hypertension. Journal of data mining in genomics & proteomics. 2017; 8(2): 2. https://doi.org/10.4172/2153-0602.1000211Holmes R.S., Spradling-Reeves K.D., Cox L.A. Mammalian glutamyl aminopeptidase genes (ENPEP) and proteins: Comparative studies of a major contributor to arterial hypertension. Journal of data mining in genomics & proteomics. 2017; 8(2): 2. https://doi.org/10.4172/2153-0602.1000211Li X. et al. Analyses of porcine public SNPs in coding-gene regions by resequencing and phenotypic association studies. Molecular Biology Reports. 2011; 38(7): 3805–3820. https://doi.org/10.1007/s11033-010-0496-1Li X. et al. Analyses of porcine public SNPs in coding-gene regions by resequencing and phenotypic association studies. Molecular Biology Reports. 2011; 38(7): 3805–3820. https://doi.org/10.1007/s11033-010-0496-1Reverter A. et al. A gene co-association network regulating gut microbial communities in a Duroc pig population. Microbiome. 2021; 9: 52. https://doi.org/10.1186/s40168-020-00994-8Reverter A. et al. A gene co-association network regulating gut microbial communities in a Duroc pig population. Microbiome. 2021; 9: 52. https://doi.org/10.1186/s40168-020-00994-8Fang Z.-H., Pausch H. Multi-trait meta-analyses reveal 25 quantitative trait loci for economically important traits in Brown Swiss cattle. BMC Genomics. 2019; 20: 695. https://doi.org/10.1186/s12864-019-6066-6Fang Z.-H., Pausch H. Multi-trait meta-analyses reveal 25 quantitative trait loci for economically important traits in Brown Swiss cattle. BMC Genomics. 2019; 20: 695. https://doi.org/10.1186/s12864-019-6066-6Johansson M. et al. The gene for dominant white color in the pig is closely linked to ALB and PDGFRA on chromosome 8. Genomics. 1992; 14(4): 965–969. https://doi.org/10.1016/s0888-7543(05)80118-1Johansson M. et al. The gene for dominant white color in the pig is closely linked to ALB and PDGFRA on chromosome 8. Genomics. 1992; 14(4): 965–969. https://doi.org/10.1016/S0888-7543(05)80118-1Whyte J.J., Prather R.S. Genetic modifications of pigs for medicine and agriculture. Molecular Reproduction and Development. 2011; 78(10–11): 879–891. https://doi.org/10.1002/mrd.21333Whyte J.J., Prather R.S. Genetic modifications of pigs for medicine and agriculture. Molecular Reproduction and Development. 2011; 78(10–11): 879–891. https://doi.org/10.1002/mrd.21333Sidor C., Borreguero-Munoz N., Fletcher G.C., Elbediwy A., Guillermin O., Thompson B.J. Mask family proteins ANKHD1 and ANKRD17 regulate YAP nuclear import and stability. Elife. 2019; 8: e48601. https://doi.org/10.7554/eLife.48601Sidor C., Borreguero-Munoz N., Fletcher G.C., Elbediwy A., Guillermin O., Thompson B.J. Mask family proteins ANKHD1 and ANKRD17 regulate YAP nuclear import and stability. Elife. 2019; 8: e48601. https://doi.org/10.7554/eLife.48601Brenig B., Duan Y., Xing Y., Ding N., Huang L., Schütz E. Porcine SOX9 gene expression is influenced by an 18bp indel in the 5’-untranslated region. PLoS ONE. 2015; 10(10): e0139583. https://doi.org/10.1371/journal.pone.0139583Brenig B., Duan Y., Xing Y., Ding N., Huang L., Schütz E. Porcine SOX9 gene expression is influenced by an 18bp indel in the 5’-untranslated region. PLoS ONE. 2015; 10(10): e0139583. https://doi.org/10.1371/journal.pone.0139583Stachowiak M. et al. Polymorphisms in the SOX9 region and testicular disorder of sex development (38, XX; SRY-negative) in pigs. Livestock Science. 2017; 203: 48–53. https://doi.org/10.1016/j.livsci.2017.07.002Stachowiak M. et al. Polymorphisms in the SOX9 region and testicular disorder of sex development (38, XX; SRY-negative) in pigs. Livestock Science. 2017; 203: 48–53. https://doi.org/10.1016/j.livsci.2017.07.002Hsu P.J. et al. Ythdc2 is an N6-methyladenosine binding protein that regulates mammalian spermatogenesis. Cell Research. 2017; 27(9): 1115–1127. https://doi.org/10.1038/cr.2017.99Hsu P.J. et al. Ythdc2 is an N6-methyladenosine binding protein that regulates mammalian spermatogenesis. Cell Research. 2017; 27(9): 1115–1127. https://doi.org/10.1038/cr.2017.99Stevens M.L. et al. Disease-associated KIF3A variants alter gene methylation and expression impacting skin barrier and atopic dermatitis risk. Nature Communications. 2020; 11: 4092. https://doi.org/10.1038/s41467-020-17895-xStevens M.L. et al. Disease-associated KIF3A variants alter gene methylation and expression impacting skin barrier and atopic dermatitis risk. Nature Communications. 2020; 11: 4092. https://doi.org/10.1038/s41467-020-17895-xQin M., Li C., Li Z., Chen W., Zeng Y. Genetic diversities and differentially selected regions between Shandong indigenous pig breeds and western pig breeds. Frontiers in Genetics. 2020; 10: 1351. https://doi.org/10.3389/fgene.2019.01351Qin M., Li C., Li Z., Chen W., Zeng Y. Genetic diversities and differentially selected regions between Shandong indigenous pig breeds and western pig breeds. Frontiers in Genetics. 2020; 10: 1351. https://doi.org/10.3389/fgene.2019.01351Almasoudi S.H., Schlosser G. Eya1 protein distribution during embryonic development of Xenopus laevis. Gene Expression Patterns. 2021; 42: 119213. https://doi.org/10.1016/j.gep.2021.119213Almasoudi S.H., Schlosser G. Eya1 protein distribution during embryonic development of Xenopus laevis. Gene Expression Patterns. 2021; 42: 119213. https://doi.org/10.1016/j.gep.2021.119213Berghöfer J., Khaveh N., Mundlos S., Metzger J. Simultaneous testing of ruleand model-based approaches for runs of homozygosity detection opens up a window into genomic footprints of selection in pigs. BMC Genomics. 2022; 23: 564. https://doi.org/10.1186/s12864-022-08801-4Berghöfer J., Khaveh N., Mundlos S., Metzger J. Simultaneous testing of ruleand model-based approaches for runs of homozygosity detection opens up a window into genomic footprints of selection in pigs. BMC Genomics. 2022; 23: 564. https://doi.org/10.1186/s12864-022-08801-4Souza M.R. et al. Transcriptome analysis identifies genes involved with the development of umbilical hernias in pigs. PLoS ONE. 2020; 15(5): e0232542. https://doi.org/10.1371/journal.pone.0232542Souza M.R. et al. Transcriptome analysis identifies genes involved with the development of umbilical hernias in pigs. PLoS ONE. 2020; 15(5): e0232542. https://doi.org/10.1371/journal.pone.0232542Tian M. et al. Transcriptome analysis reveals genes contributed to Min pig villi hair follicle in different seasons. Veterinary Sciences. 2022; 9(11): 639. https://doi.org/10.3390/vetsci9110639Tian M. et al. Transcriptome analysis reveals genes contributed to Min pig villi hair follicle in different seasons. Veterinary Sciences. 2022; 9(11): 639. https://doi.org/10.3390/vetsci9110639Diao S.-q. et al. Exploring the genetic features and signatures of selection in South China indigenous pigs. Journal of Integrative Agriculture. 2021; 20(5): 1359–1371. https://doi.org/10.1016/S2095-3119(20)63260-9Diao S.-q. et al. Exploring the genetic features and signatures of selection in South China indigenous pigs. Journal of Integrative Agriculture. 2021; 20(5): 1359–1371. https://doi.org/10.1016/S2095-3119(20)63260-9Dunkelberger J.R. et al. Genomic regions associated with host response to porcine reproductive and respiratory syndrome vaccination and co-infection in nursery pigs. BMC Genomics. 2017; 18: 865. https://doi.org/10.1186/s12864-017-4182-8Dunkelberger J.R. et al. Genomic regions associated with host response to porcine reproductive and respiratory syndrome vaccination and co-infection in nursery pigs. BMC Genomics. 2017; 18: 865. https://doi.org/10.1186/s12864-017-4182-8Cruz C.D., Torre A., Troncos G., Lambrechts L., Leguia M. Targeted full-genome amplification and sequencing of dengue virus types 1–4 from South America. Journal of Virological Methods. 2016; 235: 158–167. https://doi.org/10.1016/j.jviromet.2016.06.001Cruz C.D., Torre A., Troncos G., Lambrechts L., Leguia M. Targeted full-genome amplification and sequencing of dengue virus types 1–4 from South America. Journal of Virological Methods. 2016; 235: 158–167. https://doi.org/10.1016 /j.jviromet.2016.06.001Wu W.J. et al. Identification of four SNPs and association analysis with meat quality traits in the porcine Pitx2c gene. Science China Life Sciences. 2011; 54(5): 426–433. https://doi.org/10.1007/s11427-011-4167-9Wu W.J. et al. Identification of four SNPs and association analysis with meat quality traits in the porcine Pitx2c gene. Science China Life Sciences. 2011; 54(5): 426–433. https://doi.org/10.1007/s11427-011-4167-9Wu W., Ren Z., Wang Y., Chao Z., Xu D., Xiong Y. Molecular characterization, expression patterns and polymorphism analysis of porcine Six1 gene. Molecular Biology Reports. 2011; 38(4): 2619–2632. https://doi.org/10.1007/s11033-010-0403-9Wu W., Ren Z., Wang Y., Chao Z., Xu D., Xiong Y. Molecular characterization, expression patterns and polymorphism analysis of porcine Six1 gene. Molecular Biology Reports. 2011; 38(4): 2619–2632. https://doi.org/10.1007/s11033-010-0403-9Pérez-Montarelo D. et al. Identification of genes regulating growth and fatness traits in pig through hypothalamic transcriptome analysis. Physiological Genomics. 2014; 46(6): 195–206. https://doi.org/10.1152/physiolgenomics.00151.2013Pérez-Montarelo D. et al. Identification of genes regulating growth and fatness traits in pig through hypothalamic transcriptome analysis. Physiological Genomics. 2014; 46(6): 195–206. https://doi.org/10.1152/physiolgenomics.00151.2013Han X., Jiang T., Yu L., Zeng C., Fan B., Liu B. Molecular characterization of the porcine MTPAP gene associated with meat quality traits: chromosome localization, expression distribution, and transcriptional regulation. Molecular and Cellular Biochemistry. 2012; 364(1–2): 173–180. https://doi.org/10.1007/s11010-011-1216-4Han X., Jiang T., Yu L., Zeng C., Fan B., Liu B. Molecular characterization of the porcine MTPAP gene associated with meat quality traits: chromosome localization, expression distribution, and transcriptional regulation. Molecular and Cellular Biochemistry. 2012; 364(1–2): 173–180. https://doi.org/10.1007/s11010-011- 1216-4Vangimalla S.S., Ganesan M., Kharbanda K.K., Osna N.A. Bifunctional enzyme JMJD6 contributes to multiple disease pathogenesis: new twist on the old story. Biomolecules. 2017; 7(2): 41. https://doi.org/10.3390/biom7020041Vangimalla S.S., Ganesan M., Kharbanda K.K., Osna N.A. Bifunctional enzyme JMJD6 contributes to multiple disease pathogenesis: new twist on the old story. Biomolecules. 2017; 7(2): 41. https://doi.org/10.3390/biom7020041Pan Y. et al. METTL23 mutation alters histone H3R17 methylation in normaltension glaucoma. The Journal of Clinical Investigation. 2022; 132(21): e153589. https://doi.org/10.1172/JCI153589Pan Y. et al. METTL23 mutation alters histone H3R17 methylation in normaltension glaucoma. The Journal of Clinical Investigation. 2022; 132(21): e153589. https://doi.org/10.1172/JCI153589Zhang Y. et al. Effective quality breeding directions: comparison and conservative analysis of hepatic super-enhancers between Chinese and Western pig breeds. Biology. 2022; 11(11): 1631. https://doi.org/10.3390/biology11111631Zhang Y. et al. Effective quality breeding directions: comparison and conservative analysis of hepatic super-enhancers between Chinese and Western pig breeds. Biology. 2022; 11(11): 1631. https://doi.org/10.3390/biology11111631Okeyo-Owuor T. et al. U2AF1 mutations alter sequence specificity of pre-mRNA binding and splicing. Leukemia. 2015; 29(4): 909–917. https://doi.org/10.1038/leu.2014.303Okeyo-Owuor T. et al. U2AF1 mutations alter sequence specificity of pre-mRNA binding and splicing. Leukemia. 2015; 29(4): 909–917. https://doi.org/10.1038/leu.2014.303

The authors declare that there are no conflicts of interest present.