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Downloaded from NCBI Guo et al. BMC Genomics (2020) 21:840 https://doi.org/10.1186/s12864-020-07267-6 RESEARCH ARTICLE Open Access Identification and population genetic analyses of copy number variations in six domestic goat breeds and Bezoar ibexes using next-generation sequencing Jiazhong Guo1†, Jie Zhong1†, George E. Liu2, Liu Yang1,LiLi1, Guangling Chen3, Tianzeng Song4 and Hongping Zhang1* Abstract Background: Copy number variations (CNVs) are a major form of genetic variations and are involved in animal domestication and genetic adaptation to local environments. We investigated CNVs in the domestic goat (Capra hircus) using Illumina short-read sequencing data, by comparing our lab data for 38 goats from three Chinese breeds (Chengdu Brown, Jintang Black, and Tibetan Cashmere) to public data for 26 individuals from three other breeds (two Moroccan and one Chinese) and 21samples from Bezoar ibexes. Results: We obtained a total of 2394 CNV regions (CNVRs) by merging 208,649 high-confidence CNVs, which spanned ~ 267 Mb of total length and accounted for 10.80% of the goat autosomal genome. Functional analyses showed that 2322 genes overlapping with the CNVRs were significantly enriched in 57 functional GO terms and KEGG pathways, most related to the nervous system, metabolic process, and reproduction system. Clustering patterns of all 85 samples generated separately from duplications and deletions were generally consistent with the results from SNPs, agreeing with the geographical origins of these goats. Based on genome-wide FST at each CNV locus, some genes overlapping with the highly divergent CNVs between domestic and wild goats were mainly enriched for several immunity-related pathways, whereas the genes overlapping with the highly differentiated CNVs between highland and lowland goats were mainly related to vitamin and lipid metabolism. Remarkably, a 507-bp deletion at ~ 14 kb downstream of FGF5 on chromosome 6 showed highly divergent (FST = 0.973) between the highland and lowland goats. Together with an enhancer activity of this sequence shown previously, the function of this duplication in regulating fiber growth deserved to be further investigated in detail. Conclusion: We generated a comprehensive map of CNVs in goats. Many genetically differentiated CNVs among various goat populations might be associated with the population characteristics of domestic goat breeds. Keywords: Goat, Copy number variations, Short-read sequencing, Comparative genomics * Correspondence: [email protected] †Jiazhong Guo and Jie Zhong contributed equally to this work. 1College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Guo et al. BMC Genomics (2020) 21:840 Page 2 of 13 Background Compared to SNP chips and CGH arrays, next- As a major class of structural variations (SVs) that com- generation sequencing (NGS) or short-read sequencing plement to single nucleotide variations (SNVs), copy num- technologies have been matured rapidly in the past ber variations (CNVs) refer to duplications, deletions, and years, allowing us to identify and genotype CNVs more insertions of DNA sequences ≥50 bp in size between indi- comprehensively and precisely at the genome-wide level viduals within a species [1]. A growing body of work dem- [17, 18]. In this study, we aimed to investigate the gen- onstrates important effects of CNVs on phenotypic etic diversity, population structure, and population dif- variations of Mendelian and quantitative traits in domestic ferentiation in domestic goats, based on CNVs detected animals by various molecular mechanisms, such as gene using the whole-genome sequencing data from our pre- dosage, gene disruption, and gene fusion. For example, a vious work as well as the public data. previous work demonstrated that a massive amplification of a duplicated sequence in intron 1 of SOX5 causes Pea- Results comb in chickens [2]. An inverted duplication and junc- CNVs distribute ubiquitously in the goat genome tion of two distinct regions of the chicken genome disrupt Based on the short-read sequencing data for 85 goats long-range cis-regulatory elements of EDN3 and thereby with the coverage depth of 5.25× ~ 15.90× (Add- result in the Silkie phenotype (i.e., dermal hyperpigmenta- itional file 1), we identified a total of 208,649 CNVs, in- tion) [3]. A genome-wide association study and whole- cluding 17,876 duplications and 190,773 deletions across genome sequencing identified a significant correlation be- all autosomes (Additional file 2). As shown in Fig. 1a, tween the degree of white spotting and a 1 Mb copy num- the size of all the CNVs showed an L-shaped distribu- ber region harboring EDNRA in Boer goats [4]. A 12.1-kb tion (the median size = 179 bp, the average size = 15.17 large deletion at the HMGA2 locus results in small size in kb), and the CNVs with ≤50 kb in size accounted for dwarf rabbits [5]. A 660-Kb deletion harboring four genes 96.76% (201,898) of the total CNV number. At the indi- affects fertility and milk production traits antagonistically vidual level (Fig. 1b), we discovered, on average, 2455 in Nordic red cattle [6], illustrating the occurrence of bal- CNVs per goat genome with a range from 1145 to 4572, ancing selection in livestock. However, there are few stud- and the identified CNVs in each animal covered to 0.47 ies concerning genome-wide characteristics of CNVs in to 4.12% of the goat autosomal genome (2.47 Gb). It is goats so far [7, 8]. noted that the number of identified CNVs in each goat Similar to SNPs, the population genetic properties of appeared to increase with sequence depth in general. CNVs could reflect genomic changes driven by evolu- Based on a linear regression analysis, there was a strong − tionary factors (e.g., natural/artificial selection, demo- positive relationship (P < 2.0 × 10 16, F-test) between the graphic history, and genetic drift) [9–13]. A well-known number of CNV events on each chromosome and the example of positive selection is that the copy number chromosome length (Fig. 1c). We also constructed site of the salivary amylase (AMY1) gene highly differs be- frequency spectra of duplications and deletions in seven tween the human populations with high-starch diets goat populations as a whole (Fig. 1d). The loci with and those with traditionally low-starch diets [9]. Simi- MAF ≤ 0.05 accounted for 59.88 and 50.38% of the total larly, a genomic region harboring AMY2B was identi- duplication and deletion loci, respectively, suggesting fied as a signature of dog domestication and modern that many CNV loci were skewed towards rare CNVs. dogs show high AMY2B copy numbers compared to wolves [14], demonstrating important roles of CNVs The validation of CNVs by PCR and a second independent during animal domestication. A recent study of run of deep sequencing genome-wide CNVs in eight cattle breeds detected We performed quantitative real-time PCR (qPCR) to many lineage-differentiated CNVs that might be due to test the accuracy for the CNVs detected by next- the selection for different traits (e.g., parasite resistance, generation sequencing. The PCR results for all the body size, and fertility) [15]. In domestic goats, a gen- seven deletions (~ 14 kb downstream of FGF5, ~ 470 omic comparison with Bezoar showed that many copy kb downstream of GABRB3, FOXO3, IGLON5, number variable genes were associated with coat color, PRSS22, RARB,andKCNU1) and one duplication har- immune response, and production traits, which pro- boring the complete ASIP and AHCY genes were all vided a clue for goat domestication [16]. Based on the in agreement with our NGS prediction ADAPTmap data, Liu et al. reported a population dif- (Additional file 3). ferentiation in CNV across different geographical areas To validate the detection accuracy of CNVs, we also around the world, suggesting the population history of carried out a second independent run of whole- different domestic goat breeds [7]. However, it is still genome deep sequencing for nine sampled goats (i.e., limited with respect to the population genetic analyses three individuals in each of the CB, JT, and TC goat using large-scale CNV data in domestic goats. breeds). After alignment against the reference genome Guo et al. BMC Genomics (2020) 21:840 Page 3 of 13 Fig. 1 Genome-wide characteristics of CNVs in the goat genome. a A distribution histogram of the CNV length. b Total lengths and total numbers of CNVs identified in each goat samples. c The correlation between the number of CNVs on each chromosome and the chromosome length. d Frequency spectrum of all the deletions and duplications in seven goat populations as a whole group. Loci with the missing genotype rate > 10% were excluded (ARS1), the second runs of whole-genome sequencing CNVRs were enriched with genes mainly related to data of the nine goats showed coverage depth of 25× nervous system and immune system at least (Additional file 1).
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