Identification of the crucial circ-mi-mRNA interaction networks regulating testicular development and spermatogenesis in ganders

Semen quality has an important impact on the reproductive performance of ganders, and the quantity and quality of spermatozoa in semen are the determinants of semen quality. In our practical work, a small number of azoospermic ganders were observed in adult goose breeding populations, but the underl...

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Main Authors: Xiaopeng Li, Xiaoyong He, Guibi Li, Zhujun Wang, Fuli Huang, Jiasen Chen, Yang Song, Tanze Liu, Zhaoyan Chen, Xiangfeng Wang, Jiwei Hu, Hua He, Hehe Liu, Liang Li, Jiwen Wang, Shenqiang Hu
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Language:English
Published: Elsevier 2025-03-01
Series:Poultry Science
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Online Access:http://www.sciencedirect.com/science/article/pii/S0032579125001002
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author Xiaopeng Li
Xiaoyong He
Guibi Li
Zhujun Wang
Fuli Huang
Jiasen Chen
Yang Song
Tanze Liu
Zhaoyan Chen
Xiangfeng Wang
Jiwei Hu
Hua He
Hehe Liu
Liang Li
Jiwen Wang
Shenqiang Hu
author_facet Xiaopeng Li
Xiaoyong He
Guibi Li
Zhujun Wang
Fuli Huang
Jiasen Chen
Yang Song
Tanze Liu
Zhaoyan Chen
Xiangfeng Wang
Jiwei Hu
Hua He
Hehe Liu
Liang Li
Jiwen Wang
Shenqiang Hu
author_sort Xiaopeng Li
collection DOAJ
description Semen quality has an important impact on the reproductive performance of ganders, and the quantity and quality of spermatozoa in semen are the determinants of semen quality. In our practical work, a small number of azoospermic ganders were observed in adult goose breeding populations, but the underlying regulatory mechanisms remain unknown. In the present study, we firstly compared the morphological and histological differences in the testes of ganders from normozoospermic group (NG) and azoospermic group (AG), and then analyzed the testicular expression patterns of circRNAs, miRNAs, and mRNAs between the two groups by using whole-transcriptome sequencing technology. Results from histomorphological analysis demonstrated that the body weight alone was not accountable for the occurrence of gander azoospermia, and the possible cause might be the observed testicular abnormalities. At the morphological level, the left, right, and bilateral testicular weights, the right and bilateral testicular organ indexes, and the long, short, and dorsoventral diameters of the left, right and bilateral testes were significantly lower in AG than in NG (P < 0.05). At the histological level, most testicular histological parameters, such as the testicular parenchymal area, the diameter of seminiferous tubules, and the number of germ cells, were significantly higher (P < 0.05) in NG than in AG. The RNA-seq results showed that a total of 683 differentially expressed circRNAs (DEcircRNAs), 24 differentially expressed miRNAs (DEmiRNAs), and 1,118 differentially expressed Genes (DEGs) were identified in the gander testes between NG and AG. Subsequent functional enrichment analysis revealed that most of the DEGs and the target genes of DEcircRNAs and DEmiRNAs were significantly enriched in either the biological processes related to male gonad development, spermatid development, and regulation of cell differentiation or the KEGG terms including the MAPK, TGF-beta, Wnt, and cell cycle signaling pathways. By constructing the core ceRNA regulatory networks, several key DEcircRNAs, including 1:98100313|98104995, 1:171413706|171419341, 6:3414226|3418193, and 2:115876735|115880760, were identified to regulate the expression of TGFB2 and BCL2 through interactions with specific miRNAs such as novel-miR-265 and novel-miR-266, and such interactions could play crucial roles in regulating the gander testicular cell apoptosis, proliferation, and spermatogenesis. This study provides novel insights into the function and molecular mechanisms of ceRNAs in regulating the gander testicular development and semen quality.
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spelling doaj-art-e38327c921df4196a04b67cb5c2370052025-02-05T04:30:59ZengElsevierPoultry Science0032-57912025-03-011043104863Identification of the crucial circ-mi-mRNA interaction networks regulating testicular development and spermatogenesis in gandersXiaopeng Li0Xiaoyong He1Guibi Li2Zhujun Wang3Fuli Huang4Jiasen Chen5Yang Song6Tanze Liu7Zhaoyan Chen8Xiangfeng Wang9Jiwei Hu10Hua He11Hehe Liu12Liang Li13Jiwen Wang14Shenqiang Hu15State Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR ChinaState Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Key Laboratory of Livestock and Poultry Multi-omics Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, PR China; Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu, PR China; Key Laboratory of Agricultural Bioinformatics, Ministry of Education, Sichuan Agricultural University, Chengdu, Sichuan, PR China; Corresponding author at: State Key Laboratory of Swine and Poultry Breeding Industry, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, PR China.Semen quality has an important impact on the reproductive performance of ganders, and the quantity and quality of spermatozoa in semen are the determinants of semen quality. In our practical work, a small number of azoospermic ganders were observed in adult goose breeding populations, but the underlying regulatory mechanisms remain unknown. In the present study, we firstly compared the morphological and histological differences in the testes of ganders from normozoospermic group (NG) and azoospermic group (AG), and then analyzed the testicular expression patterns of circRNAs, miRNAs, and mRNAs between the two groups by using whole-transcriptome sequencing technology. Results from histomorphological analysis demonstrated that the body weight alone was not accountable for the occurrence of gander azoospermia, and the possible cause might be the observed testicular abnormalities. At the morphological level, the left, right, and bilateral testicular weights, the right and bilateral testicular organ indexes, and the long, short, and dorsoventral diameters of the left, right and bilateral testes were significantly lower in AG than in NG (P < 0.05). At the histological level, most testicular histological parameters, such as the testicular parenchymal area, the diameter of seminiferous tubules, and the number of germ cells, were significantly higher (P < 0.05) in NG than in AG. The RNA-seq results showed that a total of 683 differentially expressed circRNAs (DEcircRNAs), 24 differentially expressed miRNAs (DEmiRNAs), and 1,118 differentially expressed Genes (DEGs) were identified in the gander testes between NG and AG. Subsequent functional enrichment analysis revealed that most of the DEGs and the target genes of DEcircRNAs and DEmiRNAs were significantly enriched in either the biological processes related to male gonad development, spermatid development, and regulation of cell differentiation or the KEGG terms including the MAPK, TGF-beta, Wnt, and cell cycle signaling pathways. By constructing the core ceRNA regulatory networks, several key DEcircRNAs, including 1:98100313|98104995, 1:171413706|171419341, 6:3414226|3418193, and 2:115876735|115880760, were identified to regulate the expression of TGFB2 and BCL2 through interactions with specific miRNAs such as novel-miR-265 and novel-miR-266, and such interactions could play crucial roles in regulating the gander testicular cell apoptosis, proliferation, and spermatogenesis. This study provides novel insights into the function and molecular mechanisms of ceRNAs in regulating the gander testicular development and semen quality.http://www.sciencedirect.com/science/article/pii/S0032579125001002GooseAzoospermiaTesticular developmentSemen qualitySpermatogenesis
spellingShingle Xiaopeng Li
Xiaoyong He
Guibi Li
Zhujun Wang
Fuli Huang
Jiasen Chen
Yang Song
Tanze Liu
Zhaoyan Chen
Xiangfeng Wang
Jiwei Hu
Hua He
Hehe Liu
Liang Li
Jiwen Wang
Shenqiang Hu
Identification of the crucial circ-mi-mRNA interaction networks regulating testicular development and spermatogenesis in ganders
Poultry Science
Goose
Azoospermia
Testicular development
Semen quality
Spermatogenesis
title Identification of the crucial circ-mi-mRNA interaction networks regulating testicular development and spermatogenesis in ganders
title_full Identification of the crucial circ-mi-mRNA interaction networks regulating testicular development and spermatogenesis in ganders
title_fullStr Identification of the crucial circ-mi-mRNA interaction networks regulating testicular development and spermatogenesis in ganders
title_full_unstemmed Identification of the crucial circ-mi-mRNA interaction networks regulating testicular development and spermatogenesis in ganders
title_short Identification of the crucial circ-mi-mRNA interaction networks regulating testicular development and spermatogenesis in ganders
title_sort identification of the crucial circ mi mrna interaction networks regulating testicular development and spermatogenesis in ganders
topic Goose
Azoospermia
Testicular development
Semen quality
Spermatogenesis
url http://www.sciencedirect.com/science/article/pii/S0032579125001002
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