Abstract
The present study analyzed ROH and consensus ROH regions in 102 animals of eleven diverse Indian goat (Capra hircus) breeds using whole genome sequencing. A total of 51,705 ROH and 21,271 consensus regions were identified. The mean number of ROH per animal was highest in the meat breed, Jharkhand Black (2693) and lowest in the pashmina breed, Changthangi (60). The average length of ROH (ALROH) was maximum in Kanniadu (974.11 Kb) and minimum in Tellicherry (146.98 Kb). Long ROH is typically associated with more recent inbreeding, whereas short ROH is connected to more ancient inbreeding. The overall ROH-based genomic inbreeding (FROH) was highest for Jharkhand Black (0.602) followed by Kanniadu (0.120) and Sangamneri (0.108) among all breeds. FROH of Jharkhand Black was higher than Kanniadu up to 5 Mb ROH length category. However, in > 20 Mb ROH length category, Kanniadu (0.98) exhibited significantly higher FROH than Jharkhand Black (0.46). This implies that Kanniadu had higher levels of recent inbreeding than Jharkhand Black. Despite this, due to the presence of both recent and ancient inbreeding, Jharkhand Black demonstrated higher overall FROH compared to Kanniadu. ROH patterns revealed dual purpose (meat and dairy) and pashmina breeds as less consanguineous while recent inbreeding was apparent in meat breeds. Analysis of ROH consensus regions identified selection sweeps in key genes governing intramuscular fat deposition, meat tenderisation, lean meat production and carcass weight (CDK4, ALOX15, CASP9, PRDM16, DVL1) in meat breeds; milk fat percentage and mammary gland development (POLD1, NOTCH2, ARHGAP35) in dual purpose (meat and dairy) breeds; while cold adaptation and hair follicle development (APOBEC1, DNAJC3, F2RL1, FGF9) in pashmina breed. MAPK, RAS, BMP and Wnt signaling pathways associated with hair follicle morphogenesis in Changthangi were also identified. PCA analysis based on ROH consensus regions revealed that meat breeds are more diverse than other goat breeds/populations.
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The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Almeida OAC, Moreira GCM, Rezende FM, Boschiero C, de Oliveira Peixoto J, Ibelli AMG, Ledur MC, de Novais FJ, Coutinho LL (2019) Identification of selection signatures involved in performance traits in a paternal broiler line. BMC Genomics 20:449. https://doi.org/10.1186/s12864-019-5811-1
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data, Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastq.
Bhat B, Singh A, Iqbal Z, Kaushik JK, Rao AR, Ahmad SM, Ganai NA (2019) Comparative transcriptome analysis reveals the genetic basis of coat color variation in Pashmina goat. Sci Rep 9(1):1–9
Bonadeo N, Becu-Villalobos D, Cristina C, Lacau-Mengido IM (2019) The Notch system during pubertal development of the bovine mammary gland. Sci Rep 9(1):1. https://doi.org/10.1038/s41598-019-45406-6
Bosse M, Megens H-J, Madsen O, Paudel Y, Frantz LA, Schook LB, Crooijmans RP, Groenen MA (2012) Regions of homozygosity in the porcine genome: consequence of demography and the recombination landscape. PLoS Genet 8:e1003100
Braverman JM, Hudson RR, Kaplan NL, Langley CH, Stephan W (1995) The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140:783–796
Chang C-Y, Pasolli HA, Giannopoulou EG, Guasch G, Gronostajski RM, Elemento O, Fuchs E (2013) NFIB is a governor of epithelial–melanocyte stem cell behaviour in a shared niche. Nature 495(7439):98–102. https://doi.org/10.1038/nature11847
Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ (2015) Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 4:7. https://doi.org/10.1186/s13742-015-0047-8
Chen M, Wang J, Wang Y, Wu Y, Fu J, Liu J (2018) Genome-wide detection of selection signatures in Chinese indigenous Laiwu pigs revealed candidate genes regulating fat deposition in muscle. BMC Genet 19:31. https://doi.org/10.1186/s12863-018-0622
Chowdhury SMdZH, Nazir KHMNH, Hasan S, Kabir A, Mahmud MdM, Robbani M, Tabassum T, Afroze T, Rahman A, Islam MdR, Hossain M (2019) Whole genome analysis of black bengal goat from savar goat farm, bangladesh. BMC Res Notes 12(1):687. https://doi.org/10.1186/s13104-019-4700-7
Colinet H, Siaussat D, Bozzolan F, Bowler K (2013) Rapid decline of cold tolerance at young age is associated with expression of stress genes in Drosophila melanogaster. J Exp Biol 216(2):253–259. https://doi.org/10.1242/jeb.076216
Curik I, Ferenčaković M, Sölkner J (2014) Inbreeding and runs of homozygosity: a possible solution to an old problem. Livest Sci 166:26–34. https://doi.org/10.1016/j.livsci.2014.05.034
Dixit SP, Singh S, Ganguly I, Bhatia AK, Sharma A, Kumar NA, Dang AK, Jayakumar S (2020) Genome-wide runs of homozygosity revealed selection signatures in bos indicus. Front Genet 11:92. https://doi.org/10.3389/fgene.2020.00092
Ferencakovic M, Hamzic E, Gredler B, Solberg TR, Klemetsdal G, Curik I, Solkner J (2013) Estimates of autozygosity derived € from runs of homozygosity: empirical evidence from selected cattle populations. J Anim Breed Genet 130:286–293
Fernández-Barroso MÁ, Silió L, Rodríguez C, Palma-Granados P, López A, Caraballo C, Sánchez-Esquiliche F, Gómez-Carballar F, García-Casco JM, Muñoz M (2020) Genetic parameter estimation and gene association analyses for meat quality traits in open-air free-range Iberian pigs. J Anim Breed Genet 137(6):581–598. https://doi.org/10.1111/jbg.12498
Forutan M, Ansari Mahyari S, Baes C, Melzer N, Schenkel FS, Sargolzaei M (2018) Inbreeding and runs of homozygosity before and after genomic selection in North American Holstein cattle. BMC Genomics 19:98. https://doi.org/10.1186/s12864-018-4453
Gibson J, Newton EM, Collins A (2006) Extended tracts of homozygosity in outbred human populations. Hum Mol Genet 15:789–795
Huang S, Zhu X, Liu Y, Tao Y, Feng G, He L, Guo X, Ma G (2012) Wls is expressed in the epidermis and regulates embryonic hair follicle induction in mice. PLoS ONE 7(9):e45904. https://doi.org/10.1371/journal.pone.0045904
Karimi S (2013) Runs of homozygosity patterns in taurine and indicine cattle breeds. Doctoral thesis, University of Natural Resources and Life Sciences, Vienna
Kim Y, Ryu J, Woo J, Kim JB, Kim CY, Lee C (2011) Genome-wide association study reveals five nucleotide sequence variants for carcass traits in beef cattle. Anim Genet 42(4):361–365. https://doi.org/10.1111/j.1365-2052.2010.02156.x
Kim E-S, Cole JB, Huson H, Wiggans GR, Van Tassell CP, Crooker BA, Liu G, Da Y, Sonstegard TS (2013) Effect of artificial selection on runs of homozygosity in US Holstein cattle. PLoS ONE 8:e80813
Kim E-S, Elbeltagy AR, Aboul-Naga AM, Rischkowsky B, Sayre B, Mwacharo JM, Rothschild MF (2016) Multiple genomic signatures of selection in goats and sheep indigenous to a hot arid environment. Heredity 116(3):3. https://doi.org/10.1038/hdy.2015.94
Kour A, Niranjan SK, Malayaperumal M, Surati U, Pukhrambam M, Sivalingam J, Kumar A, Sarkar M (2022) Genomic diversity profiling and breed-specific evolutionary signatures of selection in Arunachali Yak. Genes 13(2):254. https://doi.org/10.3390/genes13020254
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25(14):1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Li X, Liu Z, Ye S, Liu Y, Chen Q, Guan W, Pu Y, Jiang L, He X, Ma Y, Zhao Q (2021) Integrated analysis of lncRNA and mRNA reveals novel insights into wool bending in Zhongwei goat. Animals 11(11):11. https://doi.org/10.3390/ani11113326
Li L, Xu X, Xiao M, Huang C, Cao J, Zhan S, Guo J, Zhong T, Wang L, Yang L, Zhang H (2023) The profiles and functions of RNA editing sites associated with high-altitude adaptation in goats. Int J Mol Sci 24(4):4. https://doi.org/10.3390/ijms24043115
Marras G, Gaspa G, Sorbolini S, Dimauro C, Ajmone-Marsan P, Valentini A et al (2015) Analysis of runs of homozygosity and their relationship with inbreeding in five cattle breeds farmed in Italy. Anim Genet 46:110–121. https://doi.org/10.1111/age.12259
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20(9):1297–1303. https://doi.org/10.1101/gr.107524.110
McQuillan R, Leutenegger A, Abdel-Rahman R et al (2008) Runs of homozygosity in European populations. Am J Hum Genet 83:359–372
Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197–218. https://doi.org/10.1146/annurev.genet.39.073003.112420
Otto SP (2000) Detecting the form of selection from DNA sequence data. Trends Genet 16:526–529. https://doi.org/10.1016/s0168-9525(00)02141-7
Pan C, Lei Z, Wang S, Wang X, Wei D, Cai X, Luoreng Z, Wang L, Ma Y (2021) Genome-wide identification of cyclin-dependent kinase (CDK) genes affecting adipocyte differentiation in cattle. BMC Genomics 22(1):532. https://doi.org/10.1186/s12864-021-07653-8
Pedrosa VB, Schenkel FS, Chen S-Y, Oliveira HR, Casey TM, Melka MG, Brito LF (2021) Genomewide association analyses of lactation persistency and milk production traits in holstein cattle based on imputed whole-genome sequence data. Genes 12(11):1830. https://doi.org/10.3390/genes12111830
Peripolli E, Munari DP, Silva MVGB, Lima ALF, Irgang R, Baldi F (2017) Runs of homozygosity: current knowledge and applications in livestock. Anim Genet 48(3):255–271. https://doi.org/10.1111/age.12526
Peripolli E, Stafuzza NB, Munari DP, Lima ALF, Irgang R, Machado MA et al (2018) Assessment of runs of homozygosity islands and estimates of genomic inbreeding in Gyr (Bos indicus) dairy cattle. BMC Genomics 19:34. https://doi.org/10.1186/s12864-017-4365-3
Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D et al (2007) PLINK: a tool set for whole-genome association and populationbased linkage analyses. Am J Hum Genet 81:559–575. https://doi.org/10.1086/51979
Purfield DC, Berry D, McParland S, Bradley DG (2012) Runs of homozygosity and population history in cattle. BMC Genet 13:70
Qiu W, Hu Y, Andersen TE, Jafari A, Li N, Chen W, Kassem M (2010) Tumor necrosis factor receptor superfamily member 19 (TNFRSF19) regulates differentiation fate of human mesenchymal (stromal) stem cells through canonical Wntsignaling and C/EBP. J Biol Chem 285(19):14438–14449
Rebelato AB, Caetano AR (2018) Runs of homozygosity for autozygosity estimation and genomic analysis in production animals. Pesqui Agropecu Bras 53:975–984. https://doi.org/10.1590/s0100-204x2018000900001
Rezaei R, Wu Z, Hou Y, Bazer FW, Wu G (2016) Amino acids and mammary gland development: nutritional implications for milk production and neonatal growth. J Animal Sci Biotechnol 7(1):20. https://doi.org/10.1186/s40104-016-0078-8
Rishikaysh P, Dev K, Diaz D, Qureshi WMS, Filip S, Mokry J (2014) Signaling Involved in hair follicle morphogenesis and development. Int J Mol Sci 15(1):1647–1670. https://doi.org/10.3390/ijms15011647
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Molecular cloning: a laboratory manual., Ed. 2. https://www.cabdirect.org/cabdirect/abstract/19901616061
Saravanan KA, Panigrahi M, Kumar H, Bhushan B, Dutt T, Mishra BP (2020) Selection signatures in livestock genome: a review of concepts, approaches and applications. Livest Sci 241:104257
Seale P, Kajimura S, Yang W, Chin S, Rohas LM, Uldry M, Tavernier G, Langin D, Spiegelman BM (2007) Transcriptional control of brown fat determination by PRDM16. Cell Metab 6(1):38–54. https://doi.org/10.1016/j.cmet.2007.06.001
Signer-Hasler H, Henkel J, Bangerter E, Bulut Z, Drögemüller C, Leeb T, Flury C, The VarGoats Consortium (2022) Runs of homozygosity in Swiss goats reveal genetic changes associated with domestication and modern selection. Genet Sel Evol 54(1):6. https://doi.org/10.1186/s12711-022-00695-w
Sun X, Guo J, Li L, Zhong T, Wang L, Zhan S, Lu J, Wang D, Dai D, Liu GE, Zhang H (2022) Genetic diversity and selection signatures in jianchang black goats revealed by whole-genome sequencing data. Animals 12(18):2365. https://doi.org/10.3390/ani12182365
Ueda S, Hosoda M, Kasamatsu K, Horiuchi M, Nakabayashi R, Kang B, Shinohara M, Nakanishi H, Ohto-Nakanishi T, Yamanoue M, Shirai Y (2022) Production of hydroxy fatty acids, precursors of γ-hexalactone, contributes to the characteristic sweet aroma of beef. Metabolites 12(4):332. https://doi.org/10.3390/metabo12040332
Wang A, Wang J, Mao M, Zhao X, Li Q, Xuan R, Li F, Chao T (2023) Analyses of lncRNAs, circRNAs, and the interactions between ncRNAs and mRNAs in goat submandibular glands reveal their potential function in immune regulation. Genes 14(1):187. https://doi.org/10.3390/genes14010187
Wu Z, Hai E, Di Z, Ma R, Shang F, Wang Y, Wang M, Liang L, Rong Y, Pan J, Wu W, Su R, Wang Z, Wang R, Zhang Y, Li J (2020) Using WGCNA (Weighted gene co-expression network analysis) to identify the hub genes of skin hair follicle development in fetus stage of Inner Mongolia cashmere goat. PLoS ONE 15(12):e0243507. https://doi.org/10.1371/journal.pone.0243507
Xiao L, Zhang X, Chen Z, Li Y, Li B, Li L (2020) ERK1/2 pathway is involved in the enhancement of fatty acids from phaeodactylumtricornutum extract (PTE) on hair follicle cell proliferation. Biomed Res Int 2020:1–11. https://doi.org/10.1155/2020/2916104
Xie S, Liu D, Wang L, Zhao F (2019) Genome-wide scan for runs of homozygosity identifies candidate genes in three pig breeds. Animals 9:518. https://doi.org/10.3390/ani9080518
Xu P, Wang C, Xiang W, Liang Y, Li Y, Zhang X, Guo C, Liu M, Shi Y, Ye X, Dang Y (2022) P2RY6 has a critical role in mouse skin carcinogenesis by regulating the YAP and β-catenin signaling pathways. J Investig Dermatol 142(9):2334-2342.e8. https://doi.org/10.1016/j.jid.2022.02.017
Xuan R, Chao T, Zhao X, Wang A, Chu Y, Li Q, Zhao Y, Ji Z, Wang J (2020) Identification of regulatory networks and hub genes controlling mammary gland development and lactation in dairy goats during the late lactation, dry period, and late gestation stages [Preprint]. Review. https://doi.org/10.21203/rs.3.rs-46961/v1
Yousuf S, Li A, Feng H, Lui T, Huang W, Zhang X, Xie L, Miao X (2022) Genome-wide expression profiling and networking reveals an imperative role of IMF-associated novel CircRNAs as ceRNA in pigs. Cells 11(17):2638. https://doi.org/10.3390/cells11172638
Zeder MA, Hesse B (2000) The initial domestication of goats (caprahircus) in the zagros mountains 10,000 years ago. Science 287(5461):2254–2257. https://doi.org/10.1126/science.287.5461.225
Zhang G, Wan Y, Zhang Y, Lan S, Jia R, Wang Z, Fan Y, Wang F (2015) Expression of mitochondria-associated genes (PPARGC1A, NRF-1, BCL-2 and BAX) in follicular development and atresia of goat ovaries. Reprod Domest Anim 50(3):465–473. https://doi.org/10.1111/rda.12514
Acknowledgements
The Authors are thankful to the Director, ICAR-NBAGR, Karnal, Incharges of various livestock farms and Veterinary Officers of the State Animal Husbandry Department for providing the necessary facilities/blood sample collection for the research work. The authors acknowledge the funding support received from the ICAR-National Bureau of Animal Genetic Resources, Karnal for the institute project (project code 7.75).
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SB: Investigation, Methodology, Software, IG: Conceptualization, Visualization, Investigation. Supervision, draft preparation, editing, SS: Investigation, Supervision, AKB: Script writing, Software and SPD: Conceptualization, Reviewing and Editing. All the authors have read and approved the final manuscript.
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Random blood samples were obtained from the goats with written informed consent from the owner by qualified Veterinarian in accordance with the guidelines issued by the Committee for the Purpose of Control and Supervision of Experiments on Animals (CPCSEA; http://cpcsea.nic.in/WriteReadData/userfiles/file/Compendium%20of%20CPCSEA.pdf) and approved by the Institutional Animal Ethics Committee (IAEC) of ICAR-National Bureau of Animal Genetics Resources (ICAR-NBAGR), Karnal.
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Kar, D., Ganguly, I., Singh, S. et al. Genome-wide runs of homozygosity signatures in diverse Indian goat breeds. 3 Biotech 14, 81 (2024). https://doi.org/10.1007/s13205-024-03921-y
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DOI: https://doi.org/10.1007/s13205-024-03921-y