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Journal of Integrative Agriculture
Journal of Integrative Agriculture  2025, Vol. 24 Issue (11): 4355-4369    DOI: 10.1016/j.jia.2024.04.017
Animal Science · Veterinary Medicine Advanced Online Publication | Current Issue | Archive | Adv Search |
Genome-wide association studies of novel resilience traits identify important immune QTL regions and candidate genes in Duroc pigs

Mianyan Li1, 3, Lei Pu2, David E. MacHugh3, 4, Jingjing Tian1, Xiaoqing Wang1, Qingyao Zhao5, Lijun Shi1, Hongmei Gao1, Ying Yu5, Lixian Wang1#, Fuping Zhao1#

1 State Key Laboratory of Animal Biotech Breeding, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, China

2 Tianjin Key Laboratory of Agricultural Animal Breeding and Healthy Husbandry, College of Animal Science and Animal Medicine, Tianjin Agricultural University, Tianjin 300384, China

3 Animal Genomics Laboratory, UCD School of Agriculture and Food Science, University College Dublin, Belfield, Dublin D04 V1W8, Ireland

4 UCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Belfield, Dublin D04 V1W8, Ireland

5 College of Animal Science and Technology, China Agricultural University, Beijing 100193, China

 Highlights 
● Four novel resilience traits for pigs were developed from daily feed intake and feeding duration data.
● Twenty-seven loci associated with resilience traits were identified in Duroc pigs and mapped to 49 candidate genes.
● Multi-omic integration of eQTL, chromatin and Hi-C data prioritized GWAS signals underlying regulatory variants. 
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摘要  
猪群的恢复力特性使其能更好地应对传染病和次优的生产环境。在试验期内，通过仪器自动采集猪的日增重、采食量和摄食行为数据，以评价猪的恢复力性状。本研究采用普通最小二乘（ordinary least squares, OLS）的均方误差根（mean square error roots, RMSE）和分位数回归（quantile regression, QR）的负残差，利用90 ~ 180日龄的商品杜洛克猪日采食量和饲喂时间，构建4种新的恢复力性状。基于单性状和双性状混合模型的全基因组关联研究（genome-wide associate analysis study, GWAS）对550头猪进行了研究，利用48,603个单核苷酸多态性（single nucleotide polymorphisms, SNP）来确定与生长猪恢复力性状相关的基因组区域。我们进一步针对GWAS信号进行基因注释、PigGTEx多组织eQTL共定位汇总统计以及利用公开数据鉴定增强子和启动子。估计得出这些恢复力性状的基因组遗传力在0.09 ~ 0.41之间。遗传相关性和表型相关性分别为0.16 ~ 0.95和0.05 ~ 0.36。27个SNP被鉴定出与这些恢复力性状显著相关。它们分布在9条染色体上（SSC1、SSC2、SSC6、SSC7、SSC8、SSC12、SSC14、SSC16和SSC17）。经注释，共鉴定出39个数量性状基因座（quantitative trait locus, QTL）和49个候选基因。其中存在与功能相关的候选基因，包括OTUD4、TIFA和CARD14，它们参与宿主免疫反应、疾病易感性和信号转导。在15个组织的GWAS和eQTL分析中发现了8个独特的SNP存在因果关系。值得注意的是，一个SNP（rs80794541）与七种组织 / 细胞类型（包括巨噬细胞类型）中同时鉴定的eQTL相关。此外，在5种猪组织中，4个显著SNP（rs81467127、rs81356029、rs80794541和rs81305085）与引物增强子、活性元件和启动子的功能相关。利用猪成纤维细胞HiC数据，发现SSC2上的SNP（rs81356029）调控CARNS1和SSH3，SSC7上的SNP（rs80794541）调控H2AC6。在这项研究中，我们在杜洛克猪群体中产生了4种新的恢复力性状，并确定了与这些恢复力性状显著相关的SNP。GWAS信号与参与免疫性状的候选基因有关，也与关键的调控元件有关。我们的发现将有助于阐明遗传机制，并为进一步研究家猪的恢复力提供信息。


Abstract  

Resilience traits in pig populations allow animals to deal better with infectious disease and suboptimal production environments.  The data on daily weight, feed intake and feed behaviors in pigs are collected in test period by automated feeding stations, which facilitate to evaluate the resilience traits.  In this study, we adopted the root mean square error (RMSE) of ordinary least squares (OLS) and the negative residuals of quantile regression (QR) to generate four different novel resilience traits using daily records of feed intake and feed duration between 90 and 180 days of age in a population of commercial Duroc pigs.  The genome-wide association studies (GWAS) based on single- and two-trait mixed models were carried out on 550 pigs using 48,603 single nucleotide polymorphisms (SNPs) to identify genomic regions associated with resilience traits in growing pigs.  We further focused on the GWAS signals to conduct gene annotation, colocalization with multi-tissue eQTL summary statistics of PigGTEx project and identification of enhancers and promoters using the publicly available data.  The genomic heritabilities of four novel resilience traits ranged from 0.09 to 0.41.  The pairwise genetic and phenotypic correlations ranged from 0.16 to 0.95 and from 0.05 to 0.36, respectively.  Twenty-seven SNPs were identified to be significantly associated with these resilience traits.  They were distributed on nine chromosomes (SSC1, SSC2, SSC6, SSC7, SSC8, SSC12, SSC14, SSC16 and SSC17).  After annotation, 39 QTLs and 49 candidate genes were identified.  Several of these are functionally relevant candidate genes including OTUD4, TIFA and CARD14, which are involved in the host immune response, disease susceptibility and signal transduction.  Eight unique SNPs were found to be causal in both GWAS and eQTL analyses across 15 tissues.  Notably, one SNP (rs80794541) was associated with eQTLs identified concurrently across seven tissues/cell types, including the macrophage cell type.  Furthermore, four significant SNPs (rs81467127, rs81356029, rs80794541 and rs81305085) were linked to the function of the primed enhancer, active element, and poised promoter in five pig tissues.  Using the porcine fibroblast HiC dataset, SNP (rs81356029) on SSC2 regulates the CARNS1 and SSH3, while SNP (rs80794541) on SSC7 regulates the H2AC6.  In this study, we generated four novel resilience traits and identified SNPs significantly associated with these resilience traits in a Duroc pig population.  GWAS signals were associated with candidate genes involving in the immune traits, and were linked to the crucial regulatory elements as well.  Our findings will contribute to elucidating the genetic mechanism that can enhance genome-enabled breeding and inform further research on resilience in domestic pigs.

Keywords:  candidate gene       feed intake        genome-wide association study        pig       resilience  
Received: 22 August 2023   Accepted: 11 March 2024 Online: 13 April 2024  
Fund: This work was funded by the National Key Research and Development Program of China (2024YFF1000100 and 2021YFD1301102), the National Natural Science Foundations of China (32172702) and the National Agricultural Science and Technology Innovation Program, Chinese Academy of Agricultural Sciences (ASTIP-IAS02).  
About author:  Mianyan Li, Tel: +86-353-879266107, E-mail: mianyanli@outlook.com; #Correspondence Lixian Wang, E-mail: iaswlx@263.net; Fuping Zhao, E-mail: zhaofuping@caas.cn
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Mianyan Li, Lei Pu, David E. MacHugh, Jingjing Tian, Xiaoqing Wang, Qingyao Zhao, Lijun Shi, Hongmei Gao, Ying Yu, Lixian Wang, Fuping Zhao. 2025. Genome-wide association studies of novel resilience traits identify important immune QTL regions and candidate genes in Duroc pigs. Journal of Integrative Agriculture, 24(11): 4355-4369.

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