Circular RNA Expression and Regulation Profiling in Testicular Tissues of Immature and Mature Wandong Cattle (Bos taurus)

Wandong cattle are an autochthonous Chinese breed used extensively for beef production. The breed tolerates extreme weather conditions and raw feed and is resistant to tick-borne diseases. However, the genetic basis of testis development and sperm production as well as breeding management is not wel...

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Autores principales: Ibrar Muhammad Khan, Hongyu Liu, Jingyi Zhuang, Nazir Muhammad Khan, Dandan Zhang, Jingmeng Chen, Tengteng Xu, Lourdes Felicidad Córdova Avalos, Xinqi Zhou, Yunhai Zhang
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Publicado: Frontiers Media S.A. 2021
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spelling oai:doaj.org-article:70fa4bd4e588498abd415bc0b4516d942021-11-30T10:06:33ZCircular RNA Expression and Regulation Profiling in Testicular Tissues of Immature and Mature Wandong Cattle (Bos taurus)1664-802110.3389/fgene.2021.685541https://doaj.org/article/70fa4bd4e588498abd415bc0b4516d942021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fgene.2021.685541/fullhttps://doaj.org/toc/1664-8021Wandong cattle are an autochthonous Chinese breed used extensively for beef production. The breed tolerates extreme weather conditions and raw feed and is resistant to tick-borne diseases. However, the genetic basis of testis development and sperm production as well as breeding management is not well established in local cattle. Therefore, improving the reproductive efficiency of bulls via genetic selection is crucial as a single bull can breed thousands of cows through artificial insemination (AI). Testis development and spermatogenesis are regulated by hundreds of genes and transcriptomes. However, circular RNAs (circRNAs) are the key players in many biological developmental processes that have not been methodically described and compared between immature and mature stages in Bovine testes. In this study, we performed total RNA-seq and comprehensively analyzed the circRNA expression profiling of the testis samples of six bulls at 3 years and 3 months of developmental age. In total, 17,013 circRNAs were identified, of which 681 circRNAs (p-adjust < 0.05) were differentially expressed (DE). Among these DE circRNAs, 579 were upregulated and 103 were downregulated in calf and bull testes. The Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses revealed that the identified target genes were classified into three broad functional categories, including biological process, cellular component, and molecular function, and were enriched in the lysine degradation, cell cycle, and cell adhesion molecule pathways. The binding interactions between DE circRNAs and microRNAs (miRNAs) were subsequently constructed using bioinformatics approaches. The source genes ATM, CCNA1, GSK3B, KMT2C, KMT2E, NSD2, SUCLG2, QKI, HOMER1, and SNAP91 were found to be actively associated with bull sexual maturity and spermatogenesis. In addition, a real-time quantitative polymerase chain reaction (RT-qPCR) analysis showed a strong correlation with the sequencing data. Moreover, the developed model of Bovine testes in the current study provides a suitable framework for understanding the mechanism of circRNAs in the development of testes and spermatogenesis.Ibrar Muhammad KhanHongyu LiuJingyi ZhuangNazir Muhammad KhanDandan ZhangJingmeng ChenTengteng XuLourdes Felicidad Córdova AvalosXinqi ZhouYunhai ZhangFrontiers Media S.A.articlewandong cattletesticular growthspermatogenesiscircRNAstotal RNA sequencingGeneticsQH426-470ENFrontiers in Genetics, Vol 12 (2021)
institution DOAJ
collection DOAJ
language EN
topic wandong cattle
testicular growth
spermatogenesis
circRNAs
total RNA sequencing
Genetics
QH426-470
spellingShingle wandong cattle
testicular growth
spermatogenesis
circRNAs
total RNA sequencing
Genetics
QH426-470
Ibrar Muhammad Khan
Hongyu Liu
Jingyi Zhuang
Nazir Muhammad Khan
Dandan Zhang
Jingmeng Chen
Tengteng Xu
Lourdes Felicidad Córdova Avalos
Xinqi Zhou
Yunhai Zhang
Circular RNA Expression and Regulation Profiling in Testicular Tissues of Immature and Mature Wandong Cattle (Bos taurus)
description Wandong cattle are an autochthonous Chinese breed used extensively for beef production. The breed tolerates extreme weather conditions and raw feed and is resistant to tick-borne diseases. However, the genetic basis of testis development and sperm production as well as breeding management is not well established in local cattle. Therefore, improving the reproductive efficiency of bulls via genetic selection is crucial as a single bull can breed thousands of cows through artificial insemination (AI). Testis development and spermatogenesis are regulated by hundreds of genes and transcriptomes. However, circular RNAs (circRNAs) are the key players in many biological developmental processes that have not been methodically described and compared between immature and mature stages in Bovine testes. In this study, we performed total RNA-seq and comprehensively analyzed the circRNA expression profiling of the testis samples of six bulls at 3 years and 3 months of developmental age. In total, 17,013 circRNAs were identified, of which 681 circRNAs (p-adjust < 0.05) were differentially expressed (DE). Among these DE circRNAs, 579 were upregulated and 103 were downregulated in calf and bull testes. The Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses revealed that the identified target genes were classified into three broad functional categories, including biological process, cellular component, and molecular function, and were enriched in the lysine degradation, cell cycle, and cell adhesion molecule pathways. The binding interactions between DE circRNAs and microRNAs (miRNAs) were subsequently constructed using bioinformatics approaches. The source genes ATM, CCNA1, GSK3B, KMT2C, KMT2E, NSD2, SUCLG2, QKI, HOMER1, and SNAP91 were found to be actively associated with bull sexual maturity and spermatogenesis. In addition, a real-time quantitative polymerase chain reaction (RT-qPCR) analysis showed a strong correlation with the sequencing data. Moreover, the developed model of Bovine testes in the current study provides a suitable framework for understanding the mechanism of circRNAs in the development of testes and spermatogenesis.
format article
author Ibrar Muhammad Khan
Hongyu Liu
Jingyi Zhuang
Nazir Muhammad Khan
Dandan Zhang
Jingmeng Chen
Tengteng Xu
Lourdes Felicidad Córdova Avalos
Xinqi Zhou
Yunhai Zhang
author_facet Ibrar Muhammad Khan
Hongyu Liu
Jingyi Zhuang
Nazir Muhammad Khan
Dandan Zhang
Jingmeng Chen
Tengteng Xu
Lourdes Felicidad Córdova Avalos
Xinqi Zhou
Yunhai Zhang
author_sort Ibrar Muhammad Khan
title Circular RNA Expression and Regulation Profiling in Testicular Tissues of Immature and Mature Wandong Cattle (Bos taurus)
title_short Circular RNA Expression and Regulation Profiling in Testicular Tissues of Immature and Mature Wandong Cattle (Bos taurus)
title_full Circular RNA Expression and Regulation Profiling in Testicular Tissues of Immature and Mature Wandong Cattle (Bos taurus)
title_fullStr Circular RNA Expression and Regulation Profiling in Testicular Tissues of Immature and Mature Wandong Cattle (Bos taurus)
title_full_unstemmed Circular RNA Expression and Regulation Profiling in Testicular Tissues of Immature and Mature Wandong Cattle (Bos taurus)
title_sort circular rna expression and regulation profiling in testicular tissues of immature and mature wandong cattle (bos taurus)
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/70fa4bd4e588498abd415bc0b4516d94
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