Transcriptome-Wide m6A Analysis Provides Novel Insights Into Testicular Development and Spermatogenesis in Xia-Nan Cattle
Testis is the primary organ of the male reproductive tract in mammals that plays a substantial role in spermatogenesis. Improvement of our knowledge regarding the molecular mechanisms in testicular development and spermatogenesis will be reflected in producing spermatozoa of superior fertility. Evid...
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| Published in | Frontiers in cell and developmental biology Vol. 9; p. 791221 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Switzerland
Frontiers Media S.A
22.12.2021
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| Online Access | Get full text |
| ISSN | 2296-634X 2296-634X |
| DOI | 10.3389/fcell.2021.791221 |
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| Abstract | Testis is the primary organ of the male reproductive tract in mammals that plays a substantial role in spermatogenesis. Improvement of our knowledge regarding the molecular mechanisms in testicular development and spermatogenesis will be reflected in producing spermatozoa of superior fertility. Evidence showed that N6-Methyladenosine (m6A) plays a dynamic role in post-transcription gene expression regulation and is strongly associated with production traits. However, the role of m6A in bovine testis has not been investigated yet. In this study, we conducted MeRIP-Seq analysis to explore the expression profiles of the m6A and its potential mechanism underlying spermatogenesis in nine bovine testes at three developmental stages (prepuberty, puberty and postpuberty). The experimental animals with triplicate in each stage were chosen based on their semen volume and sperm motility except for the prepuberty bulls and used for testes collection. By applying MeRIP-Seq analysis, a total of 8,774 m6A peaks and 6,206 m6A genes among the studied groups were identified. All the detected peaks were found to be mainly enriched in the coding region and 3′- untranslated regions. The cross-analysis of m6A and mRNA expression exhibited 502 genes with concomitant changes in the mRNA expression and m6A modification. Notably, 30 candidate genes were located in the largest network of protein-protein interactions. Interestingly, four key node genes (
PLK4, PTEN, EGR1
, and
PSME4
) were associated with the regulation of mammal testis development and spermatogenesis. This study is the first to present a map of RNA m6A modification in bovine testes at distinct ages, and provides new insights into m6A topology and related molecular mechanisms underlying bovine spermatogenesis, and establishes a basis for further studies on spermatogenesis in mammals. |
|---|---|
| AbstractList | Testis is the primary organ of the male reproductive tract in mammals that plays a substantial role in spermatogenesis. Improvement of our knowledge regarding the molecular mechanisms in testicular development and spermatogenesis will be reflected in producing spermatozoa of superior fertility. Evidence showed that N6-Methyladenosine (m6A) plays a dynamic role in post-transcription gene expression regulation and is strongly associated with production traits. However, the role of m6A in bovine testis has not been investigated yet. In this study, we conducted MeRIP-Seq analysis to explore the expression profiles of the m6A and its potential mechanism underlying spermatogenesis in nine bovine testes at three developmental stages (prepuberty, puberty and postpuberty). The experimental animals with triplicate in each stage were chosen based on their semen volume and sperm motility except for the prepuberty bulls and used for testes collection. By applying MeRIP-Seq analysis, a total of 8,774 m6A peaks and 6,206 m6A genes among the studied groups were identified. All the detected peaks were found to be mainly enriched in the coding region and 3'- untranslated regions. The cross-analysis of m6A and mRNA expression exhibited 502 genes with concomitant changes in the mRNA expression and m6A modification. Notably, 30 candidate genes were located in the largest network of protein-protein interactions. Interestingly, four key node genes (PLK4, PTEN, EGR1, and PSME4) were associated with the regulation of mammal testis development and spermatogenesis. This study is the first to present a map of RNA m6A modification in bovine testes at distinct ages, and provides new insights into m6A topology and related molecular mechanisms underlying bovine spermatogenesis, and establishes a basis for further studies on spermatogenesis in mammals.Testis is the primary organ of the male reproductive tract in mammals that plays a substantial role in spermatogenesis. Improvement of our knowledge regarding the molecular mechanisms in testicular development and spermatogenesis will be reflected in producing spermatozoa of superior fertility. Evidence showed that N6-Methyladenosine (m6A) plays a dynamic role in post-transcription gene expression regulation and is strongly associated with production traits. However, the role of m6A in bovine testis has not been investigated yet. In this study, we conducted MeRIP-Seq analysis to explore the expression profiles of the m6A and its potential mechanism underlying spermatogenesis in nine bovine testes at three developmental stages (prepuberty, puberty and postpuberty). The experimental animals with triplicate in each stage were chosen based on their semen volume and sperm motility except for the prepuberty bulls and used for testes collection. By applying MeRIP-Seq analysis, a total of 8,774 m6A peaks and 6,206 m6A genes among the studied groups were identified. All the detected peaks were found to be mainly enriched in the coding region and 3'- untranslated regions. The cross-analysis of m6A and mRNA expression exhibited 502 genes with concomitant changes in the mRNA expression and m6A modification. Notably, 30 candidate genes were located in the largest network of protein-protein interactions. Interestingly, four key node genes (PLK4, PTEN, EGR1, and PSME4) were associated with the regulation of mammal testis development and spermatogenesis. This study is the first to present a map of RNA m6A modification in bovine testes at distinct ages, and provides new insights into m6A topology and related molecular mechanisms underlying bovine spermatogenesis, and establishes a basis for further studies on spermatogenesis in mammals. Testis is the primary organ of the male reproductive tract in mammals that plays a substantial role in spermatogenesis. Improvement of our knowledge regarding the molecular mechanisms in testicular development and spermatogenesis will be reflected in producing spermatozoa of superior fertility. Evidence showed that N6-Methyladenosine (m6A) plays a dynamic role in post-transcription gene expression regulation and is strongly associated with production traits. However, the role of m6A in bovine testis has not been investigated yet. In this study, we conducted MeRIP-Seq analysis to explore the expression profiles of the m6A and its potential mechanism underlying spermatogenesis in nine bovine testes at three developmental stages (prepuberty, puberty and postpuberty). The experimental animals with triplicate in each stage were chosen based on their semen volume and sperm motility except for the prepuberty bulls and used for testes collection. By applying MeRIP-Seq analysis, a total of 8,774 m6A peaks and 6,206 m6A genes among the studied groups were identified. All the detected peaks were found to be mainly enriched in the coding region and 3′- untranslated regions. The cross-analysis of m6A and mRNA expression exhibited 502 genes with concomitant changes in the mRNA expression and m6A modification. Notably, 30 candidate genes were located in the largest network of protein-protein interactions. Interestingly, four key node genes ( PLK4, PTEN, EGR1 , and PSME4 ) were associated with the regulation of mammal testis development and spermatogenesis. This study is the first to present a map of RNA m6A modification in bovine testes at distinct ages, and provides new insights into m6A topology and related molecular mechanisms underlying bovine spermatogenesis, and establishes a basis for further studies on spermatogenesis in mammals. Testis is the primary organ of the male reproductive tract in mammals that plays a substantial role in spermatogenesis. Improvement of our knowledge regarding the molecular mechanisms in testicular development and spermatogenesis will be reflected in producing spermatozoa of superior fertility. Evidence showed that N6-Methyladenosine (m6A) plays a dynamic role in post-transcription gene expression regulation and is strongly associated with production traits. However, the role of m6A in bovine testis has not been investigated yet. In this study, we conducted MeRIP-Seq analysis to explore the expression profiles of the m6A and its potential mechanism underlying spermatogenesis in nine bovine testes at three developmental stages (prepuberty, puberty and postpuberty). The experimental animals with triplicate in each stage were chosen based on their semen volume and sperm motility except for the prepuberty bulls and used for testes collection. By applying MeRIP-Seq analysis, a total of 8,774 m6A peaks and 6,206 m6A genes among the studied groups were identified. All the detected peaks were found to be mainly enriched in the coding region and 3′- untranslated regions. The cross-analysis of m6A and mRNA expression exhibited 502 genes with concomitant changes in the mRNA expression and m6A modification. Notably, 30 candidate genes were located in the largest network of protein-protein interactions. Interestingly, four key node genes (PLK4, PTEN, EGR1, and PSME4) were associated with the regulation of mammal testis development and spermatogenesis. This study is the first to present a map of RNA m6A modification in bovine testes at distinct ages, and provides new insights into m6A topology and related molecular mechanisms underlying bovine spermatogenesis, and establishes a basis for further studies on spermatogenesis in mammals. Testis is the primary organ of the male reproductive tract in mammals that plays a substantial role in spermatogenesis. Improvement of our knowledge regarding the molecular mechanisms in testicular development and spermatogenesis will be reflected in producing spermatozoa of superior fertility. Evidence showed that N6-Methyladenosine (m6A) plays a dynamic role in post-transcription gene expression regulation and is strongly associated with production traits. However, the role of m6A in bovine testis has not been investigated yet. In this study, we conducted MeRIP-Seq analysis to explore the expression profiles of the m6A and its potential mechanism underlying spermatogenesis in nine bovine testes at three developmental stages (prepuberty, puberty and postpuberty). The experimental animals with triplicate in each stage were chosen based on their semen volume and sperm motility except for the prepuberty bulls and used for testes collection. By applying MeRIP-Seq analysis, a total of 8,774 m6A peaks and 6,206 m6A genes among the studied groups were identified. All the detected peaks were found to be mainly enriched in the coding region and 3'- untranslated regions. The cross-analysis of m6A and mRNA expression exhibited 502 genes with concomitant changes in the mRNA expression and m6A modification. Notably, 30 candidate genes were located in the largest network of protein-protein interactions. Interestingly, four key node genes ( , and ) were associated with the regulation of mammal testis development and spermatogenesis. This study is the first to present a map of RNA m6A modification in bovine testes at distinct ages, and provides new insights into m6A topology and related molecular mechanisms underlying bovine spermatogenesis, and establishes a basis for further studies on spermatogenesis in mammals. |
| Author | Liu, Shen-he Wang, Zi-chen Li, Ming Han, Xue-lei Yang, Li-guo Lin, Feng Ma, Xiao-ya Yue, Ting-ting Deng, Ting-xian Qi, Kun-long Gao, Teng-yun Gao, Yu-yang Fu, Tong Li, Ji-chao Rushdi, Hossam E. |
| AuthorAffiliation | 6 China Ministry of Education, Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Huazhong Agricultural University , Wuhan , China 3 Henan Dairy Herd Improvement Co., Ltd , Zhengzhou , China 5 Henan Dingyuan Cattle Breeding Co., Ltd. , Wuhan , China 1 College of Animal Science and Technology, Henan Agricultural University , Zhengzhou , China 4 Department of Animal Production, Faculty of Agriculture, Cairo University , Giza , Egypt 2 Guangxi Provincial Key Laboratory of Buffalo Genetics, Breeding and Reproduction Technology, Buffalo Research Institute, Chinese Academy of Agricultural Sciences , Nanning , China |
| AuthorAffiliation_xml | – name: 6 China Ministry of Education, Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Huazhong Agricultural University , Wuhan , China – name: 1 College of Animal Science and Technology, Henan Agricultural University , Zhengzhou , China – name: 4 Department of Animal Production, Faculty of Agriculture, Cairo University , Giza , Egypt – name: 5 Henan Dingyuan Cattle Breeding Co., Ltd. , Wuhan , China – name: 3 Henan Dairy Herd Improvement Co., Ltd , Zhengzhou , China – name: 2 Guangxi Provincial Key Laboratory of Buffalo Genetics, Breeding and Reproduction Technology, Buffalo Research Institute, Chinese Academy of Agricultural Sciences , Nanning , China |
| Author_xml | – sequence: 1 givenname: Shen-he surname: Liu fullname: Liu, Shen-he – sequence: 2 givenname: Xiao-ya surname: Ma fullname: Ma, Xiao-ya – sequence: 3 givenname: Ting-ting surname: Yue fullname: Yue, Ting-ting – sequence: 4 givenname: Zi-chen surname: Wang fullname: Wang, Zi-chen – sequence: 5 givenname: Kun-long surname: Qi fullname: Qi, Kun-long – sequence: 6 givenname: Ji-chao surname: Li fullname: Li, Ji-chao – sequence: 7 givenname: Feng surname: Lin fullname: Lin, Feng – sequence: 8 givenname: Hossam E. surname: Rushdi fullname: Rushdi, Hossam E. – sequence: 9 givenname: Yu-yang surname: Gao fullname: Gao, Yu-yang – sequence: 10 givenname: Tong surname: Fu fullname: Fu, Tong – sequence: 11 givenname: Ming surname: Li fullname: Li, Ming – sequence: 12 givenname: Teng-yun surname: Gao fullname: Gao, Teng-yun – sequence: 13 givenname: Li-guo surname: Yang fullname: Yang, Li-guo – sequence: 14 givenname: Xue-lei surname: Han fullname: Han, Xue-lei – sequence: 15 givenname: Ting-xian surname: Deng fullname: Deng, Ting-xian |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35004687$$D View this record in MEDLINE/PubMed |
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| Copyright | Copyright © 2021 Liu, Ma, Yue, Wang, Qi, Li, Lin, Rushdi, Gao, Fu, Li, Gao, Yang, Han and Deng. Copyright © 2021 Liu, Ma, Yue, Wang, Qi, Li, Lin, Rushdi, Gao, Fu, Li, Gao, Yang, Han and Deng. 2021 Liu, Ma, Yue, Wang, Qi, Li, Lin, Rushdi, Gao, Fu, Li, Gao, Yang, Han and Deng |
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| Keywords | spermatogenesis m6A modification cattle semen quality testis sequencing |
| Language | English |
| License | Copyright © 2021 Liu, Ma, Yue, Wang, Qi, Li, Lin, Rushdi, Gao, Fu, Li, Gao, Yang, Han and Deng. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Borhan Shokrollahi, Islamic Azad University, Iran Faizul Hassan, University of Agriculture, Pakistan Edited by: A. Rasim Barutcu, University of Toronto, Canada Reviewed by: Jiangbo Wei, University of Chicago, United States This article was submitted to Epigenomics and Epigenetics, a section of the journal Frontiers in Cell and Developmental Biology |
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| Title | Transcriptome-Wide m6A Analysis Provides Novel Insights Into Testicular Development and Spermatogenesis in Xia-Nan Cattle |
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