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Single-cell transcriptome analysis and in vitro differentiation of testicular cells reveal novel insights into male sterility of the interspecific hybrid cattle-yak

BACKGROUND: Interspecific hybridization plays vital roles in enriching animal diversity, while male hybrid sterility (MHS) of the offspring commonly suffered from spermatogenic arrest constitutes the postzygotic reproductive isolation. Cattle-yak, the hybrid offspring of cattle (Bos taurus) and yak...

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Autores principales: Mipam, TserangDonko, Chen, Xuemei, Zhao, Wangsheng, Zhang, Peng, Chai, Zhixin, Yue, Binglin, Luo, Hui, Wang, Jikun, Wang, Haibo, Wu, Zhijuan, Wang, Jiabo, Wang, Mingxiu, Wang, Hui, Zhang, Ming, Wang, Hongying, Jing, Kemin, Zhong, Jincheng, Cai, Xin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10045231/
https://www.ncbi.nlm.nih.gov/pubmed/36973659
http://dx.doi.org/10.1186/s12864-023-09251-2
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author Mipam, TserangDonko
Chen, Xuemei
Zhao, Wangsheng
Zhang, Peng
Chai, Zhixin
Yue, Binglin
Luo, Hui
Wang, Jikun
Wang, Haibo
Wu, Zhijuan
Wang, Jiabo
Wang, Mingxiu
Wang, Hui
Zhang, Ming
Wang, Hongying
Jing, Kemin
Zhong, Jincheng
Cai, Xin
author_facet Mipam, TserangDonko
Chen, Xuemei
Zhao, Wangsheng
Zhang, Peng
Chai, Zhixin
Yue, Binglin
Luo, Hui
Wang, Jikun
Wang, Haibo
Wu, Zhijuan
Wang, Jiabo
Wang, Mingxiu
Wang, Hui
Zhang, Ming
Wang, Hongying
Jing, Kemin
Zhong, Jincheng
Cai, Xin
author_sort Mipam, TserangDonko
collection PubMed
description BACKGROUND: Interspecific hybridization plays vital roles in enriching animal diversity, while male hybrid sterility (MHS) of the offspring commonly suffered from spermatogenic arrest constitutes the postzygotic reproductive isolation. Cattle-yak, the hybrid offspring of cattle (Bos taurus) and yak (Bos grunniens) can serve as an ideal MHS animal model. Although meiotic arrest was found to contribute to MHS of cattle-yak, yet the cellular characteristics and developmental potentials of male germline cell in pubertal cattle-yak remain to be systematically investigated. RESULTS: Single-cell RNA-seq analysis of germline and niche cell types in pubertal testis of cattle-yak and yak indicated that dynamic gene expression of developmental germ cells was terminated at late primary spermatocyte (meiotic arrest) and abnormal components of niche cell in pubertal cattle-yak. Further in vitro proliferation and differentially expressed gene (DEG) analysis of specific type of cells revealed that undifferentiated spermatogonia of cattle-yak exhibited defects in viability and proliferation/differentiation potentials. CONCLUSION: Comparative scRNA-seq and in vitro proliferation analysis of testicular cells indicated that not only meiotic arrest contributed to MHS of cattle-yak. Spermatogenic arrest of cattle-yak may originate from the differentiation stage of undifferentiated spermatogonia and niche cells of cattle-yak may provide an adverse microenvironment for spermatogenesis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09251-2.
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spelling pubmed-100452312023-03-29 Single-cell transcriptome analysis and in vitro differentiation of testicular cells reveal novel insights into male sterility of the interspecific hybrid cattle-yak Mipam, TserangDonko Chen, Xuemei Zhao, Wangsheng Zhang, Peng Chai, Zhixin Yue, Binglin Luo, Hui Wang, Jikun Wang, Haibo Wu, Zhijuan Wang, Jiabo Wang, Mingxiu Wang, Hui Zhang, Ming Wang, Hongying Jing, Kemin Zhong, Jincheng Cai, Xin BMC Genomics Research Article BACKGROUND: Interspecific hybridization plays vital roles in enriching animal diversity, while male hybrid sterility (MHS) of the offspring commonly suffered from spermatogenic arrest constitutes the postzygotic reproductive isolation. Cattle-yak, the hybrid offspring of cattle (Bos taurus) and yak (Bos grunniens) can serve as an ideal MHS animal model. Although meiotic arrest was found to contribute to MHS of cattle-yak, yet the cellular characteristics and developmental potentials of male germline cell in pubertal cattle-yak remain to be systematically investigated. RESULTS: Single-cell RNA-seq analysis of germline and niche cell types in pubertal testis of cattle-yak and yak indicated that dynamic gene expression of developmental germ cells was terminated at late primary spermatocyte (meiotic arrest) and abnormal components of niche cell in pubertal cattle-yak. Further in vitro proliferation and differentially expressed gene (DEG) analysis of specific type of cells revealed that undifferentiated spermatogonia of cattle-yak exhibited defects in viability and proliferation/differentiation potentials. CONCLUSION: Comparative scRNA-seq and in vitro proliferation analysis of testicular cells indicated that not only meiotic arrest contributed to MHS of cattle-yak. Spermatogenic arrest of cattle-yak may originate from the differentiation stage of undifferentiated spermatogonia and niche cells of cattle-yak may provide an adverse microenvironment for spermatogenesis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09251-2. BioMed Central 2023-03-27 /pmc/articles/PMC10045231/ /pubmed/36973659 http://dx.doi.org/10.1186/s12864-023-09251-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Mipam, TserangDonko
Chen, Xuemei
Zhao, Wangsheng
Zhang, Peng
Chai, Zhixin
Yue, Binglin
Luo, Hui
Wang, Jikun
Wang, Haibo
Wu, Zhijuan
Wang, Jiabo
Wang, Mingxiu
Wang, Hui
Zhang, Ming
Wang, Hongying
Jing, Kemin
Zhong, Jincheng
Cai, Xin
Single-cell transcriptome analysis and in vitro differentiation of testicular cells reveal novel insights into male sterility of the interspecific hybrid cattle-yak
title Single-cell transcriptome analysis and in vitro differentiation of testicular cells reveal novel insights into male sterility of the interspecific hybrid cattle-yak
title_full Single-cell transcriptome analysis and in vitro differentiation of testicular cells reveal novel insights into male sterility of the interspecific hybrid cattle-yak
title_fullStr Single-cell transcriptome analysis and in vitro differentiation of testicular cells reveal novel insights into male sterility of the interspecific hybrid cattle-yak
title_full_unstemmed Single-cell transcriptome analysis and in vitro differentiation of testicular cells reveal novel insights into male sterility of the interspecific hybrid cattle-yak
title_short Single-cell transcriptome analysis and in vitro differentiation of testicular cells reveal novel insights into male sterility of the interspecific hybrid cattle-yak
title_sort single-cell transcriptome analysis and in vitro differentiation of testicular cells reveal novel insights into male sterility of the interspecific hybrid cattle-yak
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10045231/
https://www.ncbi.nlm.nih.gov/pubmed/36973659
http://dx.doi.org/10.1186/s12864-023-09251-2
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