Genome-Wide Scanning for Signatures of Selection Revealed Karakul Sheep Breed in Compared to other Iranian Breeds

محورهای موضوعی : Genetics and Breeding

A.  Mirzapour-Abibagloo ¹ (Department of Animal Science, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran)
N.  Hedayat ² (Department of Animal Science, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran)
R.  Khalkhali-Evrigh ³ (Department of Animal Science, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran)
R.  Seyedsharifi ⁴ (Department of Animal Science, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran)
H.  Abdi-Benemar ⁵ (Department of Animal Science, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran)
R.  Hassanzadeh ⁶ (Department of Engineering Mathematics, Faculty of New Technologies, University of Mohaghegh Ardabili, Ardabil, Iran)
A.  Tanveer Hussain ⁷ (Department of Biological Sciences, Virtual University of Pakistan, Islamabad, Pakistan)

تاریخ دریافت : 1402/06/09 تاریخ پذیرش : 1402/10/10 تاریخ انتشار : 1402/12/11

کلید واژه: Karakul sheep, pigmentation, signature of selection, whole-genome sequencing,

چکیده مقاله :

Karakul (KAR) is one of the resistant sheep breeds to harsh desert conditions, which is also known for its excelent lamb pelt quality. This study was performed to identify the signature of selections in the KAR breed using whole-genome sequencing data (WGS) compared with five other Iranian native sheep. Three methods, including population differentiation index (Fst), nucleotide diversity (π), and cross-population extended haplotype homozygosity (XP-EHH) applied to detect the genomic signature of selection. Data analysis leads to identifying 38 shared genes among three methods as positively selected genes for the KAR breed. The most of mentioned genes were associated with coat color (KIT, DVL3, YPEL3, ERBB4, ZNF451, and CTSO), fat and energy metabolism (GDPD3, STARD13, ZNF106, MAPK3, RGS6, PHYH, AP2M1, SPAG9, DNAH9, NDUFAF6, and ARSK), muscle function (MYOCD and MCTP1), growth (CPNE4), altitude adaptation (DNAH9 and SERGEF), and reproduction (TBX6, PHYH, SPAG9, and ARSK). Based on our results, these candidate genes may have a positive effect on the adaptation of the KAR breed to a desert environment.

چکیده انگلیسی:

Karakul (KAR) is one of the resistant sheep breeds to harsh desert conditions, which is also known for its excelent lamb pelt quality. This study was performed to identify the signature of selections in the KAR breed using whole-genome sequencing data (WGS) compared with five other Iranian native sheep. Three methods, including population differentiation index (Fst), nucleotide diversity (π), and cross-population extended haplotype homozygosity (XP-EHH) applied to detect the genomic signature of selection. Data analysis leads to identifying 38 shared genes among three methods as positively selected genes for the KAR breed. The most of mentioned genes were associated with coat color (KIT, DVL3, YPEL3, ERBB4, ZNF451, and CTSO), fat and energy metabolism (GDPD3, STARD13, ZNF106, MAPK3, RGS6, PHYH, AP2M1, SPAG9, DNAH9, NDUFAF6, and ARSK), muscle function (MYOCD and MCTP1), growth (CPNE4), altitude adaptation (DNAH9 and SERGEF), and reproduction (TBX6, PHYH, SPAG9, and ARSK). Based on our results, these candidate genes may have a positive effect on the adaptation of the KAR breed to a desert environment.

منابع و مأخذ:

Alexander D.H., Novembre J. and Lange K. (2009). Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655-1664.

Alpy F. and Tomasetto C. (2014). START ships lipids across in-terorganelle space. Biochimie. 96, 85-95.

Anthérieu S., Rogue A., Fromenty B., Guillouzo A. and Robin M.A. (2011). Induction of vesicular steatosis by amiodarone and tetracycline is associated with up‐regulation of lipogenic genes in heparg cells. Hepatology. 53, 1895-1905.

Ardlie K.G., Kruglyak L. and Seielstad M. (2002). Patterns of linkage disequilibrium in the human genome. Nat. Rev. Genet. 3, 299-309.
Bertolini F., Moscatelli G., Schiavo G., Bovo S., Ribani A., Ballan M., Bonacini M., Prandi M., Dall’Olio S. and Fontanesi L. (2021). Signatures of selection are present in the genome of two close autochthonous cattle breeds raised in the North of Italy and mainly distinguished for their coat colours. J. Anim. Breed Genet. 3, 307-319.

Bolger A.M., Lohse M. and Usadel B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 30, 2114-2120.
Browning B.L., Tian X., Zhou Y. and Browning S.R. (2021). Fast two-stage phasing of large-scale sequence data. Am. J. Hum. Genet. 108, 1880-1890.

Chapman D.L., Cooper-Morgan A., Harrelson Z. and Papaioannou V.E. (2003). Critical role for Tbx6 in mesoderm specification in the mouse embryo. Mech. Dev. 120, 837-847.

Chen M., Pan D., Ren H., Fu J., Li J., Su G., Wang A., Jiang L., Zhang Q. and Liu J.F. (2016). Identification of selective sweeps reveals divergent selection between Chinese Holstein and Simmental cattle populations. Genet. Sel. Evol. 48, 1-12.

Chen Z.H., Xu Y.X., Xie X.L., Wang D.F., Aguilar-Gómez D., Liu G.J., Li X., Esmailizadeh A., Rezaei V., Kantanen J. and Ammosov I. (2021). Whole-genome sequence analysis unveils different origins of European and Asiatic mouflon and domes-tication-related genes in sheep. Commun. Biol. 4, 1307-1314.

Çilek S. and Petkova M. (2016a). Phenotypic correlations between some body measurements and prediction of body weight of Malya sheep. Bulgarian J. Agric. Sci. 22, 99-105.

Çilek S. and Petkova M. (2016b). Impact of age and gender on head measurements of Malya sheep. Bulgarian J. Agric. Sci. 22, 106-109.
Cingolani P., Platts A., Wang L.L., Coon M., Nguyen T., Wang L., Land S.J., Lu X. and Ruden D.M. (2012). A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly. 6, 80-92.

Danecek P., Auton A., Abecasis G., Albers C.A., Banks E., De-Pristo M.A., Handsaker R.E., Lunter G., Marth G.T., Sherry S.T. and McVean G. (2011). The variant call format and VCFtools. Bioinformatics. 27, 2156-2158.

Degen A.A. (2013). Karakul sheep production in Kazakhstan: an efficient collective enterprise under the state farm (sovkhoz) system and its collapse with the break-up of the Soviet Union. World Rev. Entrepren., Manag. Sustain. Dev. 9, 1-9.

Eydivandi S., Roudbar M.A., Karimi M.O. and Sahana G. (2021). Genomic scans for selective sweeps through haplotype homo-zygosity and allelic fixation in 14 indigenous sheep breeds from Middle East and South Asia. Sci. Rep. 11, 2834-2841.

Gao N., Chen Y., Liu X., Zhao Y., Zhu L., Liu A., Jiang W., Peng X., Zhang C., Tang Z. and Li X. (2019). Weighted single-step GWAS identified candidate genes associated with semen traits in a Duroc boar population. BMC Genom. 20, 1-10.

Gobeil S., Zhu X., Doillon C.J. and Green M.R. (2008). A ge-nome-wide shRNA screen identifies GAS1 as a novel mela-noma metastasis suppressor gene. Genes Dev. 22, 2932-2940.

Guo B., Kongsuwan K., Greenwood P.L., Zhou G., Zhang W. and Dalrymple B.P. (2014). A gene expression estimator of intra-muscular fat percentage for use in both cattle and sheep. J. Anim. Sci. Biotechnol. 5, 1-12.

Guo J., Tao H., Li P., Li L.I., Zhong T., Wang L., Ma J., Chen X., Song T. and Zhang H. (2018). Whole-genome sequencing re-veals selection signatures associated with important traits in six goat breeds. Sci. Rep. 8, 10405-10412.

Haase B., Brooks S.A., Tozaki T., Burger D., Poncet P.A., Rieder S., Hasegawa T., Penedo C. and Leeb T. (2009). Seven novel KIT mutations in horses with white coat colour phenotypes. Anim. Genet. 40, 623-629.

Howard J.T., Jiao S., Tiezzi F., Huang Y., Gray K.A. and Mal-tecca C. (2015). Genome-wide association study on legendre random regression coefficients for the growth and feed intake trajectory on Duroc boars. BMC Genet. 16, 1-11.

Huang H., Cao J., Hanif Q., Wang Y., Yu Y., Zhang S. and Zhang Y. (2019a). Genome‐wide association study identifies energy metabolism genes for resistance to ketosis in Chinese Holstein cattle. Anim. Genet. 50, 376-380.

Huang M., Zhang H., Wu Z.P., Wang X.P., Li D.S., Liu S.J., Zheng S.M., Yang L.J., Liu B.B., Li G.X. and Jiang Y.C. (2021). Whole-genome resequencing reveals genetic structure and introgression in Pudong White pigs. Animal. 15, 100354-100365.

Huang T., Zhang M., Yan G., Huang X., Chen H., Zhou L., Deng W., Zhang Z., Qiu H., Ai H. and Huang L. (2019b). Genome-wide association and evolutionary analyses reveal the forma-tion of swine facial wrinkles in Chinese Erhualian pigs. Aging. 11, 4672-4687.

Illa S.K., Mukherjee S., Nath S. and Mukherjee A. (2021). Ge-nome-wide scanning for signatures of selection revealed the putative genomic regions and candidate genes controlling milk composition and coat color traits in Sahiwal cattle. Front. Genet. 12, 699422-699428.
Jiang L., Kon T., Chen C., Ichikawa R., Zheng Q., Pei L., Takemura I., Nsobi L.H., Tabata H., Pan H. and Omori Y. (2021). Whole-genome sequencing of endangered Zhoushan cattle suggests its origin and the association of MC1R with black coat colour. Sci. Rep. 11, 17359-17368.

Key C.C., Bishop A.C., Wang X., Zhao Q., Chen G.Y., Quinn M.A., Zhu X., Zhang Q. and Parks J.S. (2020). Human GDPD3 overexpression promotes liver steatosis by increasing lysophosphatidic acid production and fatty acid uptake. J. Lipid Res. 61, 1075-1086.

Kumar C., Song S., Dewani P., Kumar M., Parkash O., Ma Y., Malhi K.K., Yang N., Mwacharo J.M., He X. and Jiang L. (2018). Population structure, genetic diversity and selection signatures within seven indigenous Pakistani goat populations. Anim. Genet. 49, 592-604.

Li H. and Durbin R. (2009). Fast and accurate short read align-ment with Burrows-Wheeler transform. Bioinformatics. 25, 1754-1760.

Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G. and Durbin R. (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics. 25, 2078-2079.

Liu J., Luo C., Yin Z., Li P., Wang S., Chen J., He Q. and Zhou J. (2016). Downregulation of let-7b promotes COL1A1 and COL1A2 expression in dermis and skin fibroblasts during heat wound repair. Mol. Med. Rep. 13, 2683-2688.

Liu X., Liu L., Wang J., Cui H., Chu H., Bi H., Zhao G. and Wen J. (2020). Genome-wide association study of muscle glycogen in jingxing yellow chicken. Genes. 11, 497-505.

Lomas‐Soria C., Reyes‐Castro L.A., Rodríguez‐González G.L., Ibáñez C.A., Bautista C.J., Cox L.A., Nathanielsz P.W. and Zambrano E. (2018). Maternal obesity has sex-dependent ef-fects on insulin, glucose and lipid metabolism and the liver transcriptome in young adult rat offspring. J. Physiol. 596, 4611-4628.

López S. and Alonso S. (2014). Encyclopedia of Life Sciences (ELS). John Wiley and Sons, Chichester, United Kingdom.
Manichaikul A., Mychaleckyj J.C., Rich S.S., Daly K., Sale M. and Chen W.M. (2010). Robust relationship inference in ge-nome-wide association studies. Bioinformatics. 26, 2867-2873.

Manzari Z., Mehrabani‐Yeganeh H., Nejati‐Javaremi A., Moradi M.H. and Gholizadeh M. (2019). Detecting selection signa-tures in three Iranian sheep breeds. Anim. Genet. 50, 298-302.

McKenna A., Hanna M., Banks E., Sivachenko A., Cibulskis K., Kernytsky A., Garimella K., Altshuler D., Gabriel S., Daly M. and DePristo M.A. (2010). The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303.

Murai M., Tsuji G., Hashimoto-Hachiya A., Kawakami Y., Furue M. and Mitoma C. (2018). An endogenous tryptophan photo-product, FICZ, is potentially involved in photo-aging by re-ducing TGF-β-regulated collagen homeostasis. J. Dermatol. Sci. 89, 19-26.

Näsholm A. and Eythorsdottir E. (2011). Characteristics and utili-zation of sheep pelts. Small Rumin. Res. 101, 182-187.

Nazari-Ghadikolaei A., Mehrabani-Yeganeh H., Miarei-Aashtiani S.R., Staiger E.A., Rashidi A. and Huson H.J. (2018). Ge-nome-wide association studies identify candidate genes for coat color and mohair traits in the Iranian Markhoz Goat. Front. Genet. 9, 105-112.

Nigenda‐Morales S.F., Hu Y., Beasley J.C., Ruiz‐Piña H.A., Valenzuela‐Galván D. and Wayne R.K. (2018). Transcrip-tomic analysis of skin pigmentation variation in the Virginia opossum (Didelphis virginiana). Mol. Ecol. 27, 2680-2697.

Oliver K.F., Geary T.W., Kiser J.N., Galliou J.M., Van Emon M.L., Seabury C.M., Spencer T.E. and Neibergs H.L. (2020). Loci associated with conception rate in crossbred beef heifers. PLoS One. 15, e0230422.

Pampouille E., Berri C., Boitard S., Hennequet-Antier C., Beau-clercq S.A., Godet E., Praud C., Jégo Y. and Le Bihan-Duval E. (2018). Mapping QTL for white striping in relation to breast muscle yield and meat quality traits in broiler chickens. BMC Genomics. 19, 1-14.

Pérot G., Derré J., Coindre J.M., Tirode F., Lucchesi C., Mariani O., Gibault L., Guillou L., Terrier P. and Aurias A. (2009). Strong smooth muscle differentiation is dependent on myocar-din gene amplification in most human retroperitoneal leiomy-osarcomas. Cancer Res. 69, 2269-2278.

Pielberg G., Olsson C., Syvänen A.C. and Andersson L. (2002). Unexpectedly high allelic diversity at the KIT locus causing dominant white color in the domestic pig. Genetics. 160, 305-311.

Purcell S., Neale B., Todd-Brown K., Thomas L., Ferreira M.A., Bender D., Maller J., Sklar P., De Bakker P.I., Daly M.J. and Sham P.C. (2007). PLINK: A tool set for whole-genome asso-ciation and population-based linkage analyses. Am. J. Hum. Genet. 81, 559-575.

Qanbari S. and Simianer H. (2014). Mapping signatures of posi-tive selection in the genome of livestock. Livest. Sci. 166, 133-143.

Quinlan A.R. and Hall I.M. (2010). BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics. 26, 841-842.

Reimand J., Arak T., Adler P., Kolberg L., Reisberg S., Peterson H. and Vilo J. (2016). g:Profiler—a web server for functional interpretation of gene lists (2016 update). Nucleic Acids Res. 44, 83-89.

Sabeti P.C., Varilly P., Fry B., Lohmueller J., Hostetter E., Cotsa-pas C., Xie X., Byrne E.H., McCarroll S.A., Gaudet R. and Schaffner S.F. (2007). Genome-wide detection and characteri-zation of positive selection in human populations. Nature. 449, 913-918.

Safdarian M., Kafi M. and Hashemi M. (2006). Reproductive performance of Karakul ewes following different oestrous synchronisation treatments outside the natural breeding sea-son. South African J. Anim. Sci. 36, 229-234.

Salek Ardestani S., Aminafshar M., Zandi Baghche M., Banabazi M.H., Sargolzaei M. and Miar Y. (2019). Whole-genome sig-natures of selection in sport horses revealed selection foot-prints related to musculoskeletal system development proc-esses. Animals. 10, 53-67.

Schluter A., Giralt M., Iglesias R. and Villarroya F. (2002). Phy-tanic acid, but not pristanic acid, mediates the positive effects of phytol derivatives on brown adipocyte differentiation. FEBS Lett. 517, 83-86.

Sevillano C.A., Ten Napel J., Guimarães S.E., Silva F.F. and Calus M.P. (2018). Effects of alleles in crossbred pigs esti-mated for genomic prediction depend on their breed-of-origin. BMC Genomics. 19, 1-15.

Shin O.H., Han W., Wang Y. and Südhof T.C. (2005). Evolution-arily conserved multiple C2 domain proteins with two trans-membrane regions (MCTPs) and unusual Ca2 binding proper-ties. J. Biol. Chem. 280, 1641-1651.

Showell C., Binder O. and Conlon F.L. (2004). T-box genes in early embryogenesis. Dev. Dyn. 229, 201-218.

Sun C., Lu J., Yi G., Yuan J., Duan Z., Qu L., Xu G., Wang K. and Yang N. (2015). Promising loci and genes for yolk and ovary weight in chickens revealed by a genome-wide associa-tion study. PLoS One. 10, e0137145.

Szpiech Z.A. and Hernandez R.D. (2014). Selscan: An efficient multithreaded program to perform EHH-based scans for posi-tive selection. Mol. Biol. Evol. 31, 2824-2827.

van Son M., Tremoen N.H., Gaustad A.H., Våge D.I., Zere-michael T.T., Myromslien F.D. and Grindflek E. (2020). Tran-scriptome profiling of porcine testis tissue reveals genes re-lated to sperm hyperactive motility. BMC Vet. Res. 16, 1-18.

Verdoni A.M., Ikeda S. and Ikeda A. (2010). Serum response factor is essential for the proper development of skin epithe-lium. Mamm. Genome. 21, 64-76.

Wang S., Yang C., Pan C., Feng X., Lei Z., Huang J., Wei X. and Ma Y. (2022). Identification of key genes and functional en-richment pathways involved in fat deposition in Xinyang buf-falo by WGCNA. Gene. 818, 1-12.

Wang Y., Ma C., Sun Y., Li Y., Kang L. and Jiang Y. (2017). Dynamic transcriptome and DNA methylome analyses on longissimus dorsi to identify genes underlying intramuscular fat content in pigs. BMC Genomics. 18, 1-18.

Xu P., Ni L., Tao Y., Ma Z., Hu T., Zhao X., Yu Z., Lu C., Zhao X. and Ren, J. (2020). Genome‐wide association study for growth and fatness traits in Chinese Sujiang pigs. Anim. Genet. 51, 314-318.

Yasuhiko Y., Hirabayashi Y. and Ono R. (2017). LTRs of En-dogenous Retroviruses as a Source of Tbx6 Binding Sites. Front. Chem. 5, 34-45.

Yi G., Qu L., Liu J., Yan Y., Xu G. and Yang N. (2014). Genome-wide patterns of copy number variation in the diversified chicken genomes using next-generation sequencing. BMC Ge-nomics. 15, 1-16.

Zhang C., Dong S.S., Xu J.Y., He W.M. and Yang T.L. (2019). PopLDdecay: A fast and effective tool for linkage disequilib-rium decay analysis based on variant call format files. Bioin-formatics. 35, 1786-1788.

Zhang H., Du Z.Q., Dong J.Q., Wang H.X., Shi H.Y., Wang N., Wang S.Z. and Li H. (2014). Detection of genome-wide copy number variations in two chicken lines divergently selected for abdominal fat content. BMC Genomics. 15, 517-525.

Zhang J., Wen X., Ren X.Y., Li Y.Q., Tang X.R., Wang Y.Q., He Q.M., Yang X.J., Sun Y., Liu N. and Ma J. (2016). YPEL3 suppresses epithelial–mesenchymal transition and metastasis of nasopharyngeal carcinoma cells through the Wnt/β-catenin signaling pathway. J. Exp. Clin. Cancer Res. 35, 109-118.