Single-cell RNA sequencing reveals the critical role of alternative splicing in cattle testicular spermatagonia

Abstract Spermatogonial stem cells (SSCs) form haploid gametes through the precisely regulated process of spermatogenesis. Within the testis, SSCs undergo self-renewal through mitosis, differentiation, and then enter meiosis to generate mature spermatids. This study utilized single-cell RNA sequenci...

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Main Authors: Xiuge Wang, Chunhong Yang, Xiaochao Wei, Yaran Zhang, Yao Xiao, Jinpeng Wang, Qiang Jiang, Zhihua Ju, Yaping Gao, Yanqin Li, Yundong Gao, Jinming Huang
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Biology Direct
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Online Access:https://doi.org/10.1186/s13062-024-00579-7
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author Xiuge Wang
Chunhong Yang
Xiaochao Wei
Yaran Zhang
Yao Xiao
Jinpeng Wang
Qiang Jiang
Zhihua Ju
Yaping Gao
Yanqin Li
Yundong Gao
Jinming Huang
author_facet Xiuge Wang
Chunhong Yang
Xiaochao Wei
Yaran Zhang
Yao Xiao
Jinpeng Wang
Qiang Jiang
Zhihua Ju
Yaping Gao
Yanqin Li
Yundong Gao
Jinming Huang
author_sort Xiuge Wang
collection DOAJ
description Abstract Spermatogonial stem cells (SSCs) form haploid gametes through the precisely regulated process of spermatogenesis. Within the testis, SSCs undergo self-renewal through mitosis, differentiation, and then enter meiosis to generate mature spermatids. This study utilized single-cell RNA sequencing on 26,888 testicular cells obtained from five Holstein bull testes, revealing the presence of five distinct germ cell types and eight somatic cell types in cattle testes. Gene expression profiling and enrichment analysis were utilized to uncover the varied functional roles of different cell types involved in cattle spermatogenesis. Additionally, unique gene markers specific to each testicular cell type were identified. Moreover, differentially expressed genes in spermatogonia exhibited notable enrichment in GO terms and KEGG pathway linked to alternative splicing. Notably, our study has shown that the activity of the YY1 regulation displays distinct expression patterns in spermatogonia, specifically targeting spliceosome proteins including RBM39, HNRNPA2B1, HNRNPH3, CPSF1, PCBP1, SRRM1, and SRRM2, which play essential roles in mRNA splicing. These results emphasize the importance of mRNA processing in spermatogonia within cattle testes, providing a basis for further investigation into their involvement in spermatogonial development.
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spelling doaj-art-4e9cf8f7ce904041adfa1fed83a9d2812025-08-20T02:43:32ZengBMCBiology Direct1745-61502024-12-0119111410.1186/s13062-024-00579-7Single-cell RNA sequencing reveals the critical role of alternative splicing in cattle testicular spermatagoniaXiuge Wang0Chunhong Yang1Xiaochao Wei2Yaran Zhang3Yao Xiao4Jinpeng Wang5Qiang Jiang6Zhihua Ju7Yaping Gao8Yanqin Li9Yundong Gao10Jinming Huang11Key Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesKey Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesKey Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesKey Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesKey Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesKey Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesKey Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesKey Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesKey Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesKey Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesKey Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesKey Laboratory of Livestock and Poultry Multi-omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesAbstract Spermatogonial stem cells (SSCs) form haploid gametes through the precisely regulated process of spermatogenesis. Within the testis, SSCs undergo self-renewal through mitosis, differentiation, and then enter meiosis to generate mature spermatids. This study utilized single-cell RNA sequencing on 26,888 testicular cells obtained from five Holstein bull testes, revealing the presence of five distinct germ cell types and eight somatic cell types in cattle testes. Gene expression profiling and enrichment analysis were utilized to uncover the varied functional roles of different cell types involved in cattle spermatogenesis. Additionally, unique gene markers specific to each testicular cell type were identified. Moreover, differentially expressed genes in spermatogonia exhibited notable enrichment in GO terms and KEGG pathway linked to alternative splicing. Notably, our study has shown that the activity of the YY1 regulation displays distinct expression patterns in spermatogonia, specifically targeting spliceosome proteins including RBM39, HNRNPA2B1, HNRNPH3, CPSF1, PCBP1, SRRM1, and SRRM2, which play essential roles in mRNA splicing. These results emphasize the importance of mRNA processing in spermatogonia within cattle testes, providing a basis for further investigation into their involvement in spermatogonial development.https://doi.org/10.1186/s13062-024-00579-7Alternative splicingCattleSingle-cell RNA sequencingSpermatogonia
spellingShingle Xiuge Wang
Chunhong Yang
Xiaochao Wei
Yaran Zhang
Yao Xiao
Jinpeng Wang
Qiang Jiang
Zhihua Ju
Yaping Gao
Yanqin Li
Yundong Gao
Jinming Huang
Single-cell RNA sequencing reveals the critical role of alternative splicing in cattle testicular spermatagonia
Biology Direct
Alternative splicing
Cattle
Single-cell RNA sequencing
Spermatogonia
title Single-cell RNA sequencing reveals the critical role of alternative splicing in cattle testicular spermatagonia
title_full Single-cell RNA sequencing reveals the critical role of alternative splicing in cattle testicular spermatagonia
title_fullStr Single-cell RNA sequencing reveals the critical role of alternative splicing in cattle testicular spermatagonia
title_full_unstemmed Single-cell RNA sequencing reveals the critical role of alternative splicing in cattle testicular spermatagonia
title_short Single-cell RNA sequencing reveals the critical role of alternative splicing in cattle testicular spermatagonia
title_sort single cell rna sequencing reveals the critical role of alternative splicing in cattle testicular spermatagonia
topic Alternative splicing
Cattle
Single-cell RNA sequencing
Spermatogonia
url https://doi.org/10.1186/s13062-024-00579-7
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