Haplotype Block Analysis Reveals Candidate Genes and Qtls for Meat Quality and Disease Resistance in Chinese Jiangquhai Pig Breed

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Haplotype Block Analysis Reveals Candidate Genes and Qtls for Meat Quality and Disease Resistance in Chinese Jiangquhai Pig Breed fgene-11-00752 September 2, 2020 Time: 16:48 # 1 ORIGINAL RESEARCH published: 04 September 2020 doi: 10.3389/fgene.2020.00752 Haplotype Block Analysis Reveals Candidate Genes and QTLs for Meat Quality and Disease Resistance in Chinese Jiangquhai Pig Breed Favour Oluwapelumi Oyelami1, Qingbo Zhao1, Zhong Xu1, Zhe Zhang2, Hao Sun1, Zhenyang Zhang1, Peipei Ma1, Qishan Wang1,2* and Yuchun Pan1,2* 1 Department of Animal Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China, 2 Department of Animal Breeding and Reproduction, College of Animal Science, Zhejiang University, Hangzhou, China The Jiangquhai (JQ) pig breed is one of the most widely recognized pig populations Edited by: in China due to its unique and dominant characteristics. In this study, we examined Marco Milanesi, University of Tuscia, Italy the extent of Linkage disequilibrium (LD) and haplotype block structure of the JQ pig Reviewed by: breed, and scanned the blocks for possible genes underlying important QTLs that could Zhe Zhang, either be responsible for some adaptive features in these pigs or might have undergone South China Agricultural University, some selection pressure. We compared some of our results with other Chinese and China Xiangdong Ding, Western pig breeds. The results show that the JQ breed had the highest total block China Agricultural University, China length (349.73 Mb ≈ 15% of its genome), and the coverage rate of blocks in most of its Christian H. U. W. Reimer, University of Göttingen, Germany chromosomes was larger than those of other breeds except for Sus scrofa chromosome *Correspondence: 4 (SSC4), SSC6, SSC7, SSC8, SSC10, SSC12, SSC13, SSC14, SSC17, SSC18, and Qishan Wang SSCX. Moreover, the JQ breed had more SNPs that were clustered into haplotype [email protected] blocks than the other breeds examined in this study. Our shared and unique haplotype Yuchun Pan [email protected] block analysis revealed that the Hongdenglong (HD) breed had the lowest percentage of shared haplotype blocks while the Shanzhu (SZ) breed had the highest. We found that Specialty section: the JQ breed had an average r2 > 0.2 at SNPs distances 10–20 kb and concluded that This article was submitted to Livestock Genomics, about 120,000–240,000 SNPs would be needed for a successful GWAS in the breed. a section of the journal Finally, we detected a total of 88 genes harbored by selected haplotype blocks in the Frontiers in Genetics JQ breed, of which only 4 were significantly enriched (p-value ≤ 0.05). These genes Received: 01 December 2019 Accepted: 23 June 2020 were significantly enriched in 2 GO terms (p-value < 0.01), and 2 KEGG pathways (p- Published: 04 September 2020 value < 0.02). Most of these enriched genes were related to health. Also, most of the Citation: overlapping QTLs detected in the haplotype blocks were related to meat and carcass Oyelami FO, Zhao Q, Xu Z, quality, as well as health, with a few of them relating to reproduction and production. Zhang Z, Sun H, Zhang Z, Ma P, Wang Q and Pan Y (2020) Haplotype These results provide insights into the genetic architecture of some adaptive and meat Block Analysis Reveals Candidate quality traits observed in the JQ pig breed and also revealed the pattern of LD in the Genes and QTLs for Meat Quality and Disease Resistance in Chinese genome of the pig. Our result provides significant guidance for improving the statistical Jiangquhai Pig Breed. power of GWAS and optimizing the conservation strategy for this JQ pig breed. Front. Genet. 11:752. doi: 10.3389/fgene.2020.00752 Keywords: linkage disequilibrium, haplotypes, conservation, complex traits, Chinese pigs Frontiers in Genetics| www.frontiersin.org 1 September 2020| Volume 11| Article 752 fgene-11-00752 September 2, 2020 Time: 16:48 # 2 Oyelami et al. Haplotype Block Analysis of Jiangquhai Pigs INTRODUCTION admixture, and mutations (Phillips et al., 2003; Guryev et al., 2006). Previous studies have reported a low level of admixture The pig population in China (435 million) accounts for 45% in the JQ pig breed, however, the degree of admixture of of the total population of pigs in the world (FAOSTAT, 2017) this breed by possible sources of admixtures is unknown. and the Jiangquhai (JQ) pig breed is one of the most widely Therefore, the identification of the percentage of foreign recognized pig populations in the country due to its unique and haplotypes in the JQ breed could serve as a useful framework dominant characters. This pig breed is found in Jiangsu Province, of future breeding actions and decisions when setting up in the eastern part of China where the giant Taihu lake is located. a conservation program for the breed. Moreover, since the The JQ breed is known for its high performing economic traits evolutionary history of a breed can be inferred from the like reproduction, adaptability, disease resistance, and the quality pattern of LD in the genome (Hayes et al., 2003), the of its meat (China National Commission of Animal Genetic characterization of the patterns of LD across the genome Resources, 2011). The JQ pig breed has existed since the early 19th century of JQ pigs could potentially improve our understanding and has many characteristics such as strong fat deposition of the biological pathway of recombination in the breed, and excellent tasting, high-quality meat. It is a well known and also help to detect some selection footprints in the local pig breed used in producing ham in China (China genome. Furthermore, characterizing the LD structure in National Commission of Animal Genetic Resources, 2011), the genome is particularly important for the interpretation where there are three popular types of ham: Yun ham, and application of results of genome-wide association studies Jinhua ham, and Rugao ham. While Yun hams are produced (GWAS) (Meuwissen and Goddard, 2000). from three Yunnan province pig breeds, Jinhua ham is Over the years, haplotypes have proven to be more powerful produced from Jinhua pig, and Rugao ham is produced in association studies than single-marker methods (Lin et al., from Jiangquhai (JQ) pig (Miao et al., 2009; Toldrá et al., 2009). Thus, they have a point of reference in GWAS, especially 2014). Apart from JQ pigs, other pig populations such as in the case of ungenotyped SNPs. Haplotype blocks can be Huaibei (HB), Hongdenglong (HD), Shanzhu (SZ), Dongchuan, used to identify significant variants in GWAS and also for Erhualian, Fengjing, Huai, Mi, and Shawutou are also distributed predicting the genomic breeding values (GEBV) of animals throughout Jiangsu province. in genomic selection (GS) programs (Meuwissen et al., 2001; Recent studies had revealed high genetic diversity within Calus et al., 2008; Cuyabano et al., 2015; Chen et al., 2018). the JQ pig breed (Hua et al., 2014; Xiao et al., 2017b; Therefore, the characterization of LD patterns in the genome of Xu et al., 2019). Genomic analysis also revealed that this JQ pigs has a potential application in future studies of complex breed might have undergone selection in the past, which could account for some adaptive traits in the breed (Meng traits and the development of genomic tools for the breed et al., 2018; Xu et al., 2019). However, there is still a (Corbin et al., 2010). dearth of information on the genetic architecture of some Since the extent of LD and haplotype blocks are of critical economically important traits in this pig breed. Moreover, importance for genomic selection, marker-assisted selection, and the adaptation of this breed to its environment is strongly conservation of animal genetic resources, the importance of supported by empirical evidence indicating that the genetic constructing the haplotype blocks in the JQ pig breed and basis of its population differentiation is non-additive for identifying the genes involved in them, especially those associated fitness trait and that its adaptive gene complexes would be with economically important traits, cannot be overemphasized. different from those of other breeds (Crnokrak and Roff, 1995). Such information would help in understanding the genetic Therefore, it is imperative to understand the non-random basis of breed distinction and adaptation and guide against genetic relationship between loci within the JQ pig population. incorporating haplotype blocks with deleterious gene effects into This relationship is usually reflected by the pattern and extent selection programs (Salem et al., 2018). To our knowledge, no of linkage disequilibrium (LD) that are inferred from the haplotype block study has been conducted on this pig breed haplotypes in the genome. despite its unique characteristics and there is still a knowledge Advancement in high-throughput genotyping technologies gap on the genetic basis of its phenotypic distinction. To this enables the use of large numbers of single nucleotide end, this research was conducted to (1) analyze the haplotype polymorphism (SNPs) in detecting haplotypes, which are block structure of the JQ pig breed and compare it with seven products of introgression or selection during the domestication process of pigs (Amaral et al., 2008). These haplotypes can other pig breeds (five Chinese and two western breeds), (2) be inherited from one generation to the other as single units examine the pattern of linkage disequilibrium (LD) in the JQ called haplotype blocks (Gabriel et al., 2002). Haplotype breed, and (3) scan the blocks for possible genes underlying blocks are sections of the chromosome with high LD, low important QTLs that span across the blocks. Our result provides haplotype diversity, and low recombination rate (Luikart a theoretical basis for designing breeding programs aimed et al., 2003; Phillips et al., 2003). Many haplotype blocks at conserving economically important traits in the JQ breed may arise as a result of several factors such as chromosomal and potential genetic improvement programs for this breed in recombination, selection, population bottlenecks, population the future.
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