Genome-Wide Signal Selection Analysis Revealing Genes Potentially Related to Sheep-Milk-Production Traits

Natural selection and domestication have shaped modern sheep populations into a vast range of phenotypically diverse breeds. Among these breeds, dairy sheep have a smaller population than meat sheep and wool sheep, and less research is performed on them, but the lactation mechanism in dairy sheep is...

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Main Authors: Ruonan Li, Yuhetian Zhao, Benmeng Liang, Yabin Pu, Lin Jiang, Yuehui Ma
Format: Article
Language:English
Published: MDPI AG 2023-05-01
Series:Animals
Subjects:
Online Access:https://www.mdpi.com/2076-2615/13/10/1654
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author Ruonan Li
Yuhetian Zhao
Benmeng Liang
Yabin Pu
Lin Jiang
Yuehui Ma
author_facet Ruonan Li
Yuhetian Zhao
Benmeng Liang
Yabin Pu
Lin Jiang
Yuehui Ma
author_sort Ruonan Li
collection DOAJ
description Natural selection and domestication have shaped modern sheep populations into a vast range of phenotypically diverse breeds. Among these breeds, dairy sheep have a smaller population than meat sheep and wool sheep, and less research is performed on them, but the lactation mechanism in dairy sheep is critically important for improving animal-production methods. In this study, whole-genome sequences were generated from 10 sheep breeds, including 57 high-milk-yield sheep and 44 low-milk-yield sheep, to investigate the genetic signatures of milk production in dairy sheep, and 59,864,820 valid SNPs (Single Nucleotide Polymorphisms) were kept after quality control to perform population-genetic-structure analyses, gene-detection analyses, and gene-function-validation analyses. For the population-genetic-structure analyses, we carried out PCA (Principal Component Analysis), as well as neighbor-joining tree and structure analyses to classify different sheep populations. The sheep used in our study were well distributed in ten groups, with the high-milk-yield-group populations close to each other and the low-milk-yield-group populations showing similar classifications. To perform an exact signal-selection analysis, we used three different methods to find SNPs to perform gene-annotation analyses within the 995 common regions derived from the fixation index (F<sub>ST</sub>), nucleotide diversity (Ɵπ), and heterozygosity rate (ZHp) results. In total, we found 553 genes that were located in these regions. These genes mainly participate in the protein-binding pathway and the nucleoplasm-interaction pathway, as revealed by the GO- and KEGG-function-enrichment analyses. After the gene selection and function analyses, we found that <i>FCGR3A</i>, <i>CTSK</i>, <i>CTSS</i>, <i>ARNT</i>, <i>GHR</i>, <i>SLC29A4</i>, <i>ROR1</i>, and <i>TNRC18</i> were potentially related to sheep-milk-production traits. We chose the strongly selected genes, <i>FCGR3A</i>, <i>CTSK</i>, <i>CTSS</i>, and <i>ARNT</i> during the signal-selection analysis to perform a RT-qPCR (Reale time Quantitative Polymerase Chain Reaction) experiment to validate their expression-level relationship with milk production, and the results showed that <i>FCGR3A</i> has a significant negative relationship with sheep-milk production, while other three genes did not show any positive or negative relations. In this study, it was discovered and proven that the candidate gene <i>FCGR3A</i> potentially contributes to the milk production of dairy sheep and a basis was laid for the further study of the genetic mechanism underlying the strong milk-production traits of sheep.
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spelling doaj.art-3214e19e41bc41e5bd41fba1a7e3de712023-11-18T00:10:16ZengMDPI AGAnimals2076-26152023-05-011310165410.3390/ani13101654Genome-Wide Signal Selection Analysis Revealing Genes Potentially Related to Sheep-Milk-Production TraitsRuonan Li0Yuhetian Zhao1Benmeng Liang2Yabin Pu3Lin Jiang4Yuehui Ma5State Key Laboratory of Animal Biotech Breeding, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaState Key Laboratory of Animal Biotech Breeding, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaState Key Laboratory of Animal Biotech Breeding, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaState Key Laboratory of Animal Biotech Breeding, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaState Key Laboratory of Animal Biotech Breeding, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaState Key Laboratory of Animal Biotech Breeding, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing 100193, ChinaNatural selection and domestication have shaped modern sheep populations into a vast range of phenotypically diverse breeds. Among these breeds, dairy sheep have a smaller population than meat sheep and wool sheep, and less research is performed on them, but the lactation mechanism in dairy sheep is critically important for improving animal-production methods. In this study, whole-genome sequences were generated from 10 sheep breeds, including 57 high-milk-yield sheep and 44 low-milk-yield sheep, to investigate the genetic signatures of milk production in dairy sheep, and 59,864,820 valid SNPs (Single Nucleotide Polymorphisms) were kept after quality control to perform population-genetic-structure analyses, gene-detection analyses, and gene-function-validation analyses. For the population-genetic-structure analyses, we carried out PCA (Principal Component Analysis), as well as neighbor-joining tree and structure analyses to classify different sheep populations. The sheep used in our study were well distributed in ten groups, with the high-milk-yield-group populations close to each other and the low-milk-yield-group populations showing similar classifications. To perform an exact signal-selection analysis, we used three different methods to find SNPs to perform gene-annotation analyses within the 995 common regions derived from the fixation index (F<sub>ST</sub>), nucleotide diversity (Ɵπ), and heterozygosity rate (ZHp) results. In total, we found 553 genes that were located in these regions. These genes mainly participate in the protein-binding pathway and the nucleoplasm-interaction pathway, as revealed by the GO- and KEGG-function-enrichment analyses. After the gene selection and function analyses, we found that <i>FCGR3A</i>, <i>CTSK</i>, <i>CTSS</i>, <i>ARNT</i>, <i>GHR</i>, <i>SLC29A4</i>, <i>ROR1</i>, and <i>TNRC18</i> were potentially related to sheep-milk-production traits. We chose the strongly selected genes, <i>FCGR3A</i>, <i>CTSK</i>, <i>CTSS</i>, and <i>ARNT</i> during the signal-selection analysis to perform a RT-qPCR (Reale time Quantitative Polymerase Chain Reaction) experiment to validate their expression-level relationship with milk production, and the results showed that <i>FCGR3A</i> has a significant negative relationship with sheep-milk production, while other three genes did not show any positive or negative relations. In this study, it was discovered and proven that the candidate gene <i>FCGR3A</i> potentially contributes to the milk production of dairy sheep and a basis was laid for the further study of the genetic mechanism underlying the strong milk-production traits of sheep.https://www.mdpi.com/2076-2615/13/10/1654dairy sheepwhole-genome resequencingRT-qPCRmilk productiongene expression
spellingShingle Ruonan Li
Yuhetian Zhao
Benmeng Liang
Yabin Pu
Lin Jiang
Yuehui Ma
Genome-Wide Signal Selection Analysis Revealing Genes Potentially Related to Sheep-Milk-Production Traits
Animals
dairy sheep
whole-genome resequencing
RT-qPCR
milk production
gene expression
title Genome-Wide Signal Selection Analysis Revealing Genes Potentially Related to Sheep-Milk-Production Traits
title_full Genome-Wide Signal Selection Analysis Revealing Genes Potentially Related to Sheep-Milk-Production Traits
title_fullStr Genome-Wide Signal Selection Analysis Revealing Genes Potentially Related to Sheep-Milk-Production Traits
title_full_unstemmed Genome-Wide Signal Selection Analysis Revealing Genes Potentially Related to Sheep-Milk-Production Traits
title_short Genome-Wide Signal Selection Analysis Revealing Genes Potentially Related to Sheep-Milk-Production Traits
title_sort genome wide signal selection analysis revealing genes potentially related to sheep milk production traits
topic dairy sheep
whole-genome resequencing
RT-qPCR
milk production
gene expression
url https://www.mdpi.com/2076-2615/13/10/1654
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AT yabinpu genomewidesignalselectionanalysisrevealinggenespotentiallyrelatedtosheepmilkproductiontraits
AT linjiang genomewidesignalselectionanalysisrevealinggenespotentiallyrelatedtosheepmilkproductiontraits
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