Comprehensive Genome and Transcriptome Analysis Identifies SLCO3A1 Associated with Aggressive Behavior in Pigs

Copy number variation (CNV) represents a significant reservoir of genetic diversity within the genome and exhibits a strong association with economically valuable traits in livestock. The manifestation of aggressive behavior in pigs has detrimental effects on production efficiency, immune competency...

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Main Authors: Chunlei Zhang, Huan Yang, Qinglei Xu, Mingzheng Liu, Xiaohuan Chao, Jiahao Chen, Bo Zhou, Yang Liu
Format: Article
Language:English
Published: MDPI AG 2023-09-01
Series:Biomolecules
Subjects:
Online Access:https://www.mdpi.com/2218-273X/13/9/1381
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author Chunlei Zhang
Huan Yang
Qinglei Xu
Mingzheng Liu
Xiaohuan Chao
Jiahao Chen
Bo Zhou
Yang Liu
author_facet Chunlei Zhang
Huan Yang
Qinglei Xu
Mingzheng Liu
Xiaohuan Chao
Jiahao Chen
Bo Zhou
Yang Liu
author_sort Chunlei Zhang
collection DOAJ
description Copy number variation (CNV) represents a significant reservoir of genetic diversity within the genome and exhibits a strong association with economically valuable traits in livestock. The manifestation of aggressive behavior in pigs has detrimental effects on production efficiency, immune competency, and meat quality. Nevertheless, the impact of CNV on the aggressive behavior of pigs remains elusive. In this investigation, we employed an integrated analysis of genome and transcriptome data to investigate the interplay between CNV, gene expression changes, and indicators of aggressive behavior in weaned pigs. Specifically, a subset of pigs comprising the most aggressive pigs (MAP, <i>n</i> = 12) and the least aggressive pigs (LAP, <i>n</i> = 11) was purposefully selected from a herd of 500 weaned pigs following a mixing procedure based on their composite aggressive score (CAS). Subsequently, we thoroughly analyzed copy number variation regions (CNVRs) across the entire genome using next-generation sequencing techniques, ultimately revealing the presence of 6869 CNVRs. Using genome-wide association study (GWAS) analysis and evaluating variance-stabilizing transformation (V<sub>ST</sub>) values, we successfully identified distinct CNVRs that distinguished the MAP and LAP counterparts. Among the prioritized CNVRs, CNVR-4962 (designated as the top-ranked <i>p</i>-value and V<sub>ST</sub> value, No. 1) was located within the Solute Carrier Organic Anion Transporter Family Member 3A1 (SLCO3A1) gene. The results of our analyses indicated a significantly higher (<i>p</i> < 0.05) copy number of <i>SLCO3A1</i> in the MAP compared to the LAP. Furthermore, this increased copy number exhibited a positive correlation with the CAS of the pigs (<i>p</i> < 0.05). Furthermore, we integrated genomic data with transcriptomic data from the temporal lobe to facilitate the examination of expression quantitative trait loci (eQTL). Importantly, these observations were consistent with the mRNA expression pattern of <i>SLCO3A1</i> in the temporal lobe of both MAP and LAP (<i>p</i> < 0.05). Consequently, our findings strongly suggest that CNVs affecting <i>SLCO3A1</i> may influence gene expression through a dosage effect. These results highlight the potential of <i>SLCO3A1</i> as a candidate gene associated with aggressive traits in pig breeding programs.
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spelling doaj.art-760b117232ec4929abc308e42795bad82023-11-19T09:46:13ZengMDPI AGBiomolecules2218-273X2023-09-01139138110.3390/biom13091381Comprehensive Genome and Transcriptome Analysis Identifies SLCO3A1 Associated with Aggressive Behavior in PigsChunlei Zhang0Huan Yang1Qinglei Xu2Mingzheng Liu3Xiaohuan Chao4Jiahao Chen5Bo Zhou6Yang Liu7College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaCollege of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaCopy number variation (CNV) represents a significant reservoir of genetic diversity within the genome and exhibits a strong association with economically valuable traits in livestock. The manifestation of aggressive behavior in pigs has detrimental effects on production efficiency, immune competency, and meat quality. Nevertheless, the impact of CNV on the aggressive behavior of pigs remains elusive. In this investigation, we employed an integrated analysis of genome and transcriptome data to investigate the interplay between CNV, gene expression changes, and indicators of aggressive behavior in weaned pigs. Specifically, a subset of pigs comprising the most aggressive pigs (MAP, <i>n</i> = 12) and the least aggressive pigs (LAP, <i>n</i> = 11) was purposefully selected from a herd of 500 weaned pigs following a mixing procedure based on their composite aggressive score (CAS). Subsequently, we thoroughly analyzed copy number variation regions (CNVRs) across the entire genome using next-generation sequencing techniques, ultimately revealing the presence of 6869 CNVRs. Using genome-wide association study (GWAS) analysis and evaluating variance-stabilizing transformation (V<sub>ST</sub>) values, we successfully identified distinct CNVRs that distinguished the MAP and LAP counterparts. Among the prioritized CNVRs, CNVR-4962 (designated as the top-ranked <i>p</i>-value and V<sub>ST</sub> value, No. 1) was located within the Solute Carrier Organic Anion Transporter Family Member 3A1 (SLCO3A1) gene. The results of our analyses indicated a significantly higher (<i>p</i> < 0.05) copy number of <i>SLCO3A1</i> in the MAP compared to the LAP. Furthermore, this increased copy number exhibited a positive correlation with the CAS of the pigs (<i>p</i> < 0.05). Furthermore, we integrated genomic data with transcriptomic data from the temporal lobe to facilitate the examination of expression quantitative trait loci (eQTL). Importantly, these observations were consistent with the mRNA expression pattern of <i>SLCO3A1</i> in the temporal lobe of both MAP and LAP (<i>p</i> < 0.05). Consequently, our findings strongly suggest that CNVs affecting <i>SLCO3A1</i> may influence gene expression through a dosage effect. These results highlight the potential of <i>SLCO3A1</i> as a candidate gene associated with aggressive traits in pig breeding programs.https://www.mdpi.com/2218-273X/13/9/1381CNVaggressive behavior<i>SLCO3A1</i>animal welfaredosage effect
spellingShingle Chunlei Zhang
Huan Yang
Qinglei Xu
Mingzheng Liu
Xiaohuan Chao
Jiahao Chen
Bo Zhou
Yang Liu
Comprehensive Genome and Transcriptome Analysis Identifies SLCO3A1 Associated with Aggressive Behavior in Pigs
Biomolecules
CNV
aggressive behavior
<i>SLCO3A1</i>
animal welfare
dosage effect
title Comprehensive Genome and Transcriptome Analysis Identifies SLCO3A1 Associated with Aggressive Behavior in Pigs
title_full Comprehensive Genome and Transcriptome Analysis Identifies SLCO3A1 Associated with Aggressive Behavior in Pigs
title_fullStr Comprehensive Genome and Transcriptome Analysis Identifies SLCO3A1 Associated with Aggressive Behavior in Pigs
title_full_unstemmed Comprehensive Genome and Transcriptome Analysis Identifies SLCO3A1 Associated with Aggressive Behavior in Pigs
title_short Comprehensive Genome and Transcriptome Analysis Identifies SLCO3A1 Associated with Aggressive Behavior in Pigs
title_sort comprehensive genome and transcriptome analysis identifies slco3a1 associated with aggressive behavior in pigs
topic CNV
aggressive behavior
<i>SLCO3A1</i>
animal welfare
dosage effect
url https://www.mdpi.com/2218-273X/13/9/1381
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