DOI QR코드

DOI QR Code

Genome-wide scan for runs of homozygosity identifies candidate genes in Wannan Black pigs

  • Wu, Xudong (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Zhou, Ren (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Zhang, Wei (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Cao, Bangji (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Xia, Jing (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Wang, Caiyun (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Zhang, Xiaodong (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Chu, Mingxing (Key Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences) ;
  • Yin, Zongjun (College of Animal Science and Technology, Anhui Agricultural University) ;
  • Ding, Yueyun (College of Animal Science and Technology, Anhui Agricultural University)
  • Received : 2020.09.28
  • Accepted : 2021.02.07
  • Published : 2021.12.01

Abstract

Objective: Runs of homozygosity (ROH) are contiguous lengths of homozygous genotypes that can reveal inbreeding levels, selection pressure, and mating schemes. In this study, ROHs were evaluated in Wannan Black pigs to assess the inbreeding levels and the genome regions with high ROH frequency. Methods: In a previous study, we obtained 501.52 GB of raw data from resequencing (10×) of the genome and identified 21,316,754 single-nucleotide variants in 20 Wannan Black pig samples. We investigated the number, length, and frequency of ROH using resequencing data to characterize the homozygosity in Wannan Black pigs and identified genomic regions with high ROH frequencies. Results: In this work, 1,813 ROHs (837 ROHs in 100 to 500 kb, 449 ROHs in 500 to 1,000 kb, 527 ROHs in >1,000 kb) were identified in all samples, and the average genomic inbreeding coefficient (FROH) in Wannan Black pigs was 0.5234. Sixty-one regions on chromosomes 2, 3, 7, 8, 13, 15, and 16 harbored ROH islands. In total, 105 genes were identified in 42 ROH islands, among which some genes were related to production traits. Conclusion: This is the first study to identify ROH across the genome of Wannan Black pigs, the Chinese native breed of the Anhui province. Overall, Wannan Black pigs have high levels of inbreeding due to the influence of ancient and recent inbreeding due to the genome. These findings are a reliable resource for future studies and contribute to save and use the germplasm resources of Wannan Black pigs.

Keywords

Acknowledgement

This work was supported by the National Natural Science Foundation of China (31972531), Special Projects of the Central Government Guiding Local Science and Technology Development of Anhui Provincial (202007d06020016), Anhui Provincial Science and Technology Major Project (17030 701008, 17030701061) and the Anhui Provincial Modern Industrial Technology System of Swine.

References

  1. Chen H, Huang T, Zhang Z, et al. Genome-wide association studies and meta-analysis reveal novel quantitative trait loci and pleiotropic loci for swine head-related traits. J Anim Sci 2017;95:2354-66. https://doi.org/10.2527/jas.2016.1137
  2. Maselli V, Polese G, Larson G, et al. A dysfunctional sense of smell: the irreversibility of olfactory evolution in freeliving pigs. Evol Biol 2014;41:229-39. https://doi.org/10.1007/s11692-013-9262-3
  3. Novoselova TA, Meuwissen MPM, Jongbloed AW, Huirne RBM. Expected economic performance of genetic modification in pork production. NJAS-Wageningen J Life Sci 2013; 64-65:9-15. https://doi.org/10.1016/j.njas.2012.03.002
  4. Muhammad H, Iqbal Z, Bashir Q. Genetic polymorphism among five species of Indus River carps on the basis of random amplified polymorphic DNA (RAPD) analysis. Rend Lincei Sci Fis Nat 2017;28:73-80. https://doi.org/10.1007/s12210-016-0576-9
  5. Gorlov IF, Kolosov YA, Shirokova NV, et al. GDF9 gene polymorphism and its association with litter size in two Russian sheep breeds. Rend Lincei Sci Fis Nat 2018;29:61-6. https://doi.org/10.1007/s12210-017-0659-2
  6. Forutan M, Mahyari SA, Baes C, et al. Inbreeding and runs of homozygosity before and after genomic selection in North American Holstein cattle. BMC Genomics 2018;19:98. https://doi.org/10.1186/s12864-018-4453-z
  7. Christensen OF, Nielsen B, Su G, et al. A bivariate genomic model with additive, dominance and inbreeding depression effects for sire line and three-way crossbred pigs. Genet Sel Evol 2019;51:45. https://doi.org/10.1186/s12711-019-0486-2
  8. Do C, Yang C, Choi J, et al. The outcomes of selection in a closed herd on a farm in operation. Asian-Australas J Anim Sci 2015;28:1244-51. https://doi.org/10.5713/ajas.14.0962
  9. Ouborg NJ, Pertoldi C, Loeschcke V, Bijlsma R, Hedrick PW. Conservation genetics in transition to conservation genomics. Trends Genet 2010;26:177-87. https://doi.org/10.1016/j.tig.2010.01.001
  10. Sell-Kubiak E, Czarniecki A, Strabel T. Challenges in inbreeding estimation of large populations based on Polish HolsteinFriesian cattle pedigree. J Appl Genet 2018;59:313-23. https://doi.org/10.1007/s13353-018-0441-x
  11. Simino J, Shi G, Arnett D, Broeckel U, Hunt SC, Rao DC. Variants on chromosome 6p22.3 associated with blood pressure in the HyperGEN study: follow-up of FBPP quantitative trait loci. Am J Hypertens 2011;24:1227-33. https://doi.org/10.1038/ajh.2011.140
  12. Purfield DC, Berry DP, McParland S, Bradley DG. Runs of homozygosity and population history in cattle. BMC Genet 2012;13:70. https://doi.org/10.1186/1471-2156-13-70
  13. Zavarez LB, Utsunomiya YT, Carmo AS, et al. Assessment of autozygosity in Nellore cows (Bos indicus) through high-density SNP genotypes. Front Genet 2015;6:5. https://doi.org/10.3389/fgene.2015.00005
  14. Kim ES, Cole JB, Huson H, et al. Effect of artificial selection on runs of homozygosity in US Holstein cattle. PLoS One 2013;8:e80813. https://doi.org/10.1371/journal.pone.0080813
  15. Ceballos FC, Joshi PK, Clark DW, Ramsay M, Wilson JF. Runs of homozygosity: windows into population history and trait architecture. Nat Rev Genet 2018;19:220-34. https://doi.org/10.1038/nrg.2017.109
  16. Purfield DC, McParland S, Wall E, Berry DP. The distribution of runs of homozygosity and selection signatures in six commercial meat sheep breeds. PLoS One 2017;12:e0176780. https://doi.org/10.1371/journal.pone.0176780
  17. Metzger J, Karwath M, Tonda R, et al. Runs of homozygosity reveal signatures of positive selection for reproduction traits in breed and non-breed horses. BMC Genomics 2015;16:764. https://doi.org/10.1186/s12864-015-1977-3
  18. Shi L, Wang L, Liu J, et al. Estimation of inbreeding and identification of regions under heavy selection based on runs of homozygosity in a Large White pig population. J Anim Sci Biotechnol 2020;11:46. https://doi.org/10.1186/s40104-020-00447-0
  19. China National Commission of Animal Genetic Resources. Animal genetic resources in China pigs. Beijing, China: China Agricultural Press; 2011.
  20. Ding YY, Zhang W, Zhang MQ, et al. Functional and association studies of the cholesteryl ester transfer protein (CETP) gene in a Wannan Black pig model. Anim Genet 2015;46: 702-6. https://doi.org/10.1111/age.12370
  21. Ding X, Ding Y, Zhang C, Huang L, He X, Yin Z et al. Polymorphisms and sequencing analysis in 5' upstream and intron 2 region of H-FABP gene in Anhui Wannan Black pig population. J Anim Vet Adv 2011;10:1568-72. https://doi.org/10.3923/javaa.2011.1568.1572
  22. Zhang XD, Zhu HY, Zhou J, et al. Relationship between polymorphisms in exon 10 of FSHR gene and litter size in swine. Genet Mol Res 2015;14:8252-61. https://doi.org/10.4238/2015.July.27.13
  23. Ding X, Zhang X, Yang Y, et al. Polymorphism, expression of natural resistance-associated macrophage protein 1 encoding gene (NRAMP1) and Its association with immune traits in pigs. Asian-Australas J Anim Sci 2014;27:1189-95. https://doi.org/10.5713/ajas.2014.14017
  24. Tang GQ, Xuea J, Lian MJ, et al. Inbreeding and genetic diversity in three imported swine breeds in china using pedigree data. Asian-Australas J Anim Sci 2013;26:755-65. https://doi.org/10.5713/ajas.2012.12645
  25. Zhang W, Yang M, Wang YL, et al. Genomic analysis reveals selection signatures of the Wannan Black pig during domestication and breeding. Asian-Australas J Anim Sci 2020;33:712-21. https://doi.org/10.5713/ajas.19.0289
  26. Purcell S, Neale B, Todd-Brown K, et al. PLINK: A tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007;81:559-75. https://doi.org/10.1086/519795
  27. Peripolli E, Metzger J, de Lemos MVA, et al. Autozygosity islands and ROH patterns in Nellore lineages: evidence of selection for functionally important traits. BMC Genomics 2018;19:680. https://doi.org/10.1186/s12864-018-5060-8
  28. Xu Z, Sun H, Zhang Z, et al. Assessment of autozygosity derived from runs of homozygosity in Jinhua pigs disclosed by sequencing data. Front Genet 2019;10:274. https://doi.org/10.3389/fgene.2019.00274
  29. Zhao G, Zhang T, Liu Y, et al. Genome-wide assessment of runs of homozygosity in Chinese Wagyu beef cattle. Animals 2020;10:1425. https://doi.org/10.3390/ani10081425
  30. Mastrangelo S, Ciani E, Sardina MT, et al. Runs of homozygosity reveal genome-wide autozygosity in Italian sheep breeds. Anim Genet 2018;49:71-81. https://doi.org/10.1111/age.12634
  31. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009;4:44-57. https://doi.org/10.1038/nprot.2008.211
  32. Gibson J, Morton NE, Collins A. Extended tracts of homozygosity in outbred human populations. Hum Mol Genet 2006;15:789-95. https://doi.org/10.1093/hmg/ddi493
  33. Peripolli E, Munari DP, Silva MVGB, Lima ALF, Irgang R, Baldi F. Runs of homozygosity: current knowledge and applications in livestock. Anim Genet 2017;48:255-71. https://doi.org/10.1111/age.12526
  34. He SG, Di J, Han B, et al. Genome-wide scan for runs of homozygosity identifies candidate genes related to economically important traits in Chinese merino. Animals 2020;10:524. https://doi.org/10.3390/ani10030524
  35. Bosse M, Megens HJ, Madsen O, et al. Regions of homozygosity in the porcine genome: consequence of demography and the recombination landscape. PLoS Genet 2012;8:e1003100. https://doi.org/10.1371/journal.pgen.1003100
  36. Marras G, Gaspa G, Sorbolini S, et al. Analysis of runs of homozygosity and their relationship with inbreeding in five cattle breeds farmed in Italy. Anim Genet 2015;46:110-21. https://doi.org/10.1111/age.12259
  37. Gomez-Raya L, Rauw WM, Dunkeiberger JR, Dekkers JCM. Autozygosity and genetic differentiation of landrace and large white pigs as revealed by the genetic analyses of crossbreds. Front Genet 2019;10. https://doi.org/10.3389/fgene.2019.00739
  38. McQuillan R, Leutenegger A-L, Abdel-Rahman R, et al. Runs of homozygosity in european populations. Am J Hum Genet 2008;83:658. https://doi.org/10.1016/j.ajhg.2008.10.009
  39. Szmatola T, Jasielczuk I, Semik-Gurgul E, et al. Detection of runs of homozygosity in conserved and commercial pig breeds in Poland. J Anim Breed Genet 2020. https://doi.org/10.1111/jbg.12482
  40. Li Q, Wang C, Yang J, et al. Genetic diversity analysis based on microsatellite markers in 5 Anhui local and 5 introduced pig breeds. Swine Prod 2018;3:67-72.
  41. Woolliams J. Genetic contributions and inbreeding. Pages in 147-165 In: Oldenbroek K, editor. Utilization and conservation of farm animal genetic resources. Wageningen, the Netherlands: Wageningen Academic Publishers; 2007. pp. 147-65.
  42. Abdelmohsen K, Srikantan S, Yang X, et al. Ubiquitin-mediated proteolysis of HuR by heat shock. EMBO J 2009;28:1271-82. https://doi.org/10.1038/emboj.2009.67
  43. Ma X, Guan L, Xuan J, et al. Effect of polymorphisms in the CAMKMT gene on growth traits in Ujumqin sheep. Anim Genet 2016;47:618-22. https://doi.org/10.1111/age.12455
  44. Meng Q, Wang K, Liu X, et al. Identification of growth trait related genes in a Yorkshire purebred pig population by genome-wide association studies. Asian-Australas J Anim Sci 2017;30:462-9. https://doi.org/10.5713/ajas.16.0548
  45. Bao X, Zeng Y, Wei S, et al. Developmental changes of Col3a1 mRNA expression in muscle and their association with intramuscular collagen in pigs. J Genet Genomics 2007;34: 223-8. https://doi.org/10.1016/s1673-8527(07)60023-x
  46. Maldonado L, Brait M, Begum S, et al. GULP1, a potential tumor suppressor gene in ovarian tumors and its utility as a biomarker. Cancer Res 2010;70:4891. https://doi.org/10.1158/1538-7445.Am10-4891
  47. Luhrig S, Kolb S, Mellies N, Nolte J. The novel BTB-kelch protein, KBTBD8, is located in the Golgi apparatus and translocates to the spindle apparatus during mitosis. Cell Div 2013;8:3. https://doi.org/10.1186/1747-1028-8-3
  48. Avila-Arcos MC, McManus KF, Sandoval K, et al. Population history and gene divergence in native Mexicans inferred from 76 human exomes. Mol Biol Evol 2020;37:994-1006. https://doi.org/10.1093/molbev/msz282