{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,14]],"date-time":"2026-09-14T15:14:07Z","timestamp":1789398847303,"version":"build-2803163510"},"reference-count":70,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,11,22]],"date-time":"2021-11-22T00:00:00Z","timestamp":1637539200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Genet."],"abstract":"<jats:p>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 <jats:italic>via<\/jats:italic> 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 <jats:italic>Bovine<\/jats:italic> 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\u00a0years and 3\u00a0months of developmental age. In total, 17,013 circRNAs were identified, of which 681 circRNAs (<jats:italic>p<\/jats:italic>-adjust &amp;lt; 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 <jats:italic>ATM<\/jats:italic>, <jats:italic>CCNA1<\/jats:italic>, <jats:italic>GSK3B<\/jats:italic>, <jats:italic>KMT2C<\/jats:italic>, <jats:italic>KMT2E<\/jats:italic>, <jats:italic>NSD2<\/jats:italic>, <jats:italic>SUCLG2, QKI<\/jats:italic>, <jats:italic>HOMER1<\/jats:italic>, and <jats:italic>SNAP91<\/jats:italic> 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 <jats:italic>Bovine<\/jats:italic> testes in the current study provides a suitable framework for understanding the mechanism of circRNAs in the development of testes and spermatogenesis.<\/jats:p>","DOI":"10.3389\/fgene.2021.685541","type":"journal-article","created":{"date-parts":[[2021,11,30]],"date-time":"2021-11-30T10:06:39Z","timestamp":1638266799000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":19,"title":["Circular RNA Expression and Regulation Profiling in Testicular Tissues of Immature and Mature Wandong Cattle (Bos taurus)"],"prefix":"10.3389","volume":"12","author":[{"given":"Ibrar Muhammad","family":"Khan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongyu","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jingyi","family":"Zhuang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nazir Muhammad","family":"Khan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dandan","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jingmeng","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tengteng","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lourdes Felicidad C\u00f3rdova","family":"Avalos","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinqi","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yunhai","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,11,22]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1038\/75556","article-title":"Gene Ontology: Tool for the Unification of Biology","volume":"25","author":"Ashburner","year":"2000","journal-title":"Nat. Genet."},{"key":"B2","doi-asserted-by":"publisher","first-page":"D138","DOI":"10.1093\/nar\/gkh121","article-title":"The Pfam Protein Families Database","volume":"32","author":"Bateman","year":"2004","journal-title":"Nucleic Acids Res."},{"key":"B3","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1007\/978-981-13-1426-1_7","article-title":"Regulation of Transcription by Circular RNAs","volume":"1087","author":"Bose","year":"2018","journal-title":"Circular RNAs"},{"key":"B4","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1016\/j.theriogenology.2016.09.047","article-title":"Comparative Analysis of Testis Transcriptomes Associated with Male Infertility in Cattleyak","volume":"88","author":"Cai","year":"2017","journal-title":"Theriogenology"},{"key":"B5","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1095\/biolreprod.112.103788","article-title":"Cryopreserved Bovine Spermatozoal Transcript Profile as Revealed by High-Throughput Ribonucleic Acid Sequencing","volume":"88","author":"Card","year":"2013","journal-title":"Biol. Reprod."},{"key":"B6","doi-asserted-by":"publisher","first-page":"135","DOI":"10.3389\/fgene.2020.00135","article-title":"Pituitary-Derived Circular RNAs Expression and Regulatory Network Prediction during the Onset of Puberty in Landrace \u00d7 Yorkshire Crossbred Pigs","volume":"11","author":"Chen","year":"2020","journal-title":"Front. Genet."},{"key":"B7","doi-asserted-by":"publisher","first-page":"435","DOI":"10.3389\/fendo.2019.00435","article-title":"Expression Patterns of Circular RNAs in High Quality and Poor Quality Human Spermatozoa","volume":"10","author":"Chioccarelli","year":"2019","journal-title":"Front. Endocrinol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"476","DOI":"10.1093\/molehr\/gau018","article-title":"The Human Testis-specific Proteome Defined by Transcriptomics and Antibody-Based Profiling","volume":"20","author":"Djureinovic","year":"2014","journal-title":"Mol. Hum. Reprod."},{"key":"B9","doi-asserted-by":"publisher","first-page":"39080","DOI":"10.1038\/srep39080","article-title":"Identification and Characterization of Human Testis Derived Circular RNAs and Their Existence in Seminal Plasma","volume":"6","author":"Dong","year":"2016","journal-title":"Sci. Rep."},{"key":"B10","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1016\/s0070-2153(08)60174-x","article-title":"5 Gene Expression during Mammalian Meiosis","volume":"37","author":"Eddy","year":"1997","journal-title":"Curr. Top. Dev. Biol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"D222","DOI":"10.1093\/nar\/gkt1223","article-title":"Pfam: the Protein Families Database","volume":"42","author":"Finn","year":"2014","journal-title":"Nucl. Acids Res."},{"key":"B12","doi-asserted-by":"publisher","first-page":"pdb.prot4986","DOI":"10.1101\/pdb.prot4986","article-title":"Hematoxylin and Eosin Staining of Tissue and Cell Sections","volume":"2008","author":"Fischer","year":"2008","journal-title":"Cold Spring harbor Protoc."},{"key":"B13","doi-asserted-by":"publisher","first-page":"e0205295","DOI":"10.1371\/journal.pone.0205295","article-title":"Combining Multi-OMICs Information to Identify Key-Regulator Genes for Pleiotropic Effect on Fertility and Production Traits in Beef Cattle","volume":"13","author":"Fonseca","year":"2018","journal-title":"PLoS One"},{"key":"B14","doi-asserted-by":"publisher","first-page":"646","DOI":"10.3389\/fgene.2019.00646","article-title":"Analysis of Long Non-coding RNA and mRNA Expression Profiling in Immature and Mature Bovine (Bos taurus) Testes","volume":"10","author":"Gao","year":"2019","journal-title":"Front. Genet."},{"key":"B15","doi-asserted-by":"publisher","first-page":"180413","DOI":"10.1098\/rsos.180413","article-title":"Identification and Characterization of Circular RNAs in Qinchuan Cattle Testis","volume":"5","author":"Gao","year":"2018","journal-title":"Royal society open science"},{"key":"B16","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1038\/nature04917","article-title":"A Germline-specific Class of Small RNAs Binds Mammalian Piwi Proteins","volume":"442","author":"Girard","year":"2006","journal-title":"Nature"},{"key":"B17","doi-asserted-by":"publisher","first-page":"1666","DOI":"10.1261\/rna.043687.113","article-title":"circBase: a Database for Circular RNAs","volume":"20","author":"Gla\u017ear","year":"2014","journal-title":"Rna"},{"key":"B18","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1152\/physrev.00013.2015","article-title":"Spermatogenesis: The Commitment to Meiosis","volume":"96","author":"Griswold","year":"2016","journal-title":"Physiol. Rev."},{"key":"B19","doi-asserted-by":"publisher","first-page":"409","DOI":"10.1186\/s13059-014-0409-z","article-title":"Expanded Identification and Characterization of Mammalian Circular RNAs","volume":"15","author":"Guo","year":"2014","journal-title":"Genome Biol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"384","DOI":"10.1038\/nature11993","article-title":"Natural RNA Circles Function as Efficient microRNA Sponges","volume":"495","author":"Hansen","year":"2013","journal-title":"Nature"},{"key":"B21","doi-asserted-by":"publisher","first-page":"555","DOI":"10.1002\/(sici)1521-1878(199807)20:7<555:aid-bies6>3.0.co;2-j","article-title":"Molecular Mechanisms of Male Germ Cell Differentiation","volume":"20","author":"Hecht","year":"1998","journal-title":"Bioessays"},{"key":"B22","doi-asserted-by":"publisher","first-page":"203","DOI":"10.3390\/genes12020203","article-title":"Characterization of Breed Specific Differences in Spermatozoal Transcriptomes of Sheep in Australia","volume":"12","author":"Hodge","year":"2021","journal-title":"Genes"},{"key":"B23","doi-asserted-by":"publisher","first-page":"403","DOI":"10.3390\/ani9070403","article-title":"Characterization of Circular RNAs in Chinese Buffalo (Bubalus Bubalis) Adipose Tissue: a Focus on Circular RNAs Involved in Fat Deposition","volume":"9","author":"Huang","year":"2019","journal-title":"Animals"},{"key":"B24","doi-asserted-by":"publisher","first-page":"e30244","DOI":"10.1371\/journal.pone.0030244","article-title":"Characterization and Comparison of the Leukocyte Transcriptomes of Three Cattle Breeds","volume":"7","author":"Huang","year":"2012","journal-title":"PLoS ONE"},{"key":"B25","doi-asserted-by":"publisher","first-page":"66709","DOI":"10.18632\/oncotarget.19640","article-title":"Progress and Future prospect of In Vitro Spermatogenesis","volume":"8","author":"Ibtisham","year":"2017","journal-title":"Oncotarget"},{"key":"B26","doi-asserted-by":"publisher","first-page":"R36","DOI":"10.1186\/gb-2013-14-4-r36","article-title":"TopHat2: Accurate Alignment of Transcriptomes in the Presence of Insertions, Deletions and Gene Fusions","volume":"14","author":"Kim","year":"2013","journal-title":"Genome Biol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"W345","DOI":"10.1093\/nar\/gkm391","article-title":"CPC: Assess the Protein-Coding Potential of Transcripts Using Sequence Features and Support Vector Machine","volume":"35","author":"Kong","year":"2007","journal-title":"Nucleic Acids Res."},{"key":"B28","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1016\/j.jbiotec.2016.09.011","article-title":"Circular RNAs Are miRNA Sponges and Can Be Used as a New Class of Biomarker","volume":"238","author":"Kulcheski","year":"2016","journal-title":"J. Biotechnol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast Gapped-Read Alignment with Bowtie 2","volume":"9","author":"Langmead","year":"2012","journal-title":"Nat. Methods"},{"key":"B30","doi-asserted-by":"publisher","first-page":"1829","DOI":"10.1261\/rna.047126.114","article-title":"Circular RNAs: Diversity of Form and Function","volume":"20","author":"Lasda","year":"2014","journal-title":"Rna."},{"key":"B31","doi-asserted-by":"publisher","first-page":"843","DOI":"10.1016\/0092-8674(93)90529-y","article-title":"The C. elegans Heterochronic Gene Lin-4 Encodes Small RNAs with Antisense Complementarity to Lin-14","volume":"75","author":"Lee","year":"1993","journal-title":"cell"},{"key":"B33","doi-asserted-by":"publisher","first-page":"523","DOI":"10.1093\/dnares\/dsx022","article-title":"Genome-wide Profiling of Sus scrofa Circular RNAs across Nine Organs and Three Developmental Stages","volume":"24","author":"Liang","year":"2017","journal-title":"DNA Res."},{"key":"B34","doi-asserted-by":"publisher","first-page":"1011","DOI":"10.1080\/15476286.2016.1218588","article-title":"Expression Dynamics, Relationships, and Transcriptional Regulations of Diverse Transcripts in Mouse Spermatogenic Cells","volume":"13","author":"Lin","year":"2016","journal-title":"RNA Biol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"e0182602","DOI":"10.1371\/journal.pone.0182602","article-title":"Identification of Differentially Expressed Genes through RNA Sequencing in Goats (Capra hircus) at Different Postnatal Stages","volume":"12","author":"Lin","year":"2017","journal-title":"PloS one"},{"key":"B36","doi-asserted-by":"publisher","first-page":"638","DOI":"10.2527\/jas1982.553638x","article-title":"Puberty in Beef Bulls: Acrosome Morphology and Semen Quality in Bulls of Different Breeds1","volume":"55","author":"Lunstra","year":"1982","journal-title":"J. Anim. Sci."},{"key":"B37","doi-asserted-by":"publisher","first-page":"3787","DOI":"10.1093\/bioinformatics\/bti430","article-title":"Automated Genome Annotation and Pathway Identification Using the KEGG Orthology (KO) as a Controlled Vocabulary","volume":"21","author":"Mao","year":"2005","journal-title":"Bioinformatics"},{"key":"B38","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1038\/nature11928","article-title":"Circular RNAs Are a Large Class of Animal RNAs with Regulatory Potency","volume":"495","author":"Memczak","year":"2013","journal-title":"Nature"},{"key":"B39","doi-asserted-by":"publisher","first-page":"786","DOI":"10.1111\/rda.13426","article-title":"Comparative Proteomic Analysis of High- and Low-fertile buffalo Bull Spermatozoa for Identification of Fertility-Associated Proteins","volume":"54","author":"M. K","year":"2019","journal-title":"Reprod. Domest. Anim."},{"key":"B40","doi-asserted-by":"publisher","first-page":"360","DOI":"10.1111\/j.2047-2927.2014.00183.x","article-title":"Regulatory Non-coding Transcripts in Spermatogenesis: Shedding Light on 'dark Matter'","volume":"2","author":"Mukherjee","year":"2014","journal-title":"Andrology"},{"key":"B41","doi-asserted-by":"publisher","first-page":"857","DOI":"10.1038\/s41467-020-14654-w","article-title":"ATM and PRDM9 Regulate SPO11-Bound Recombination Intermediates during Meiosis","volume":"11","author":"Paiano","year":"2020","journal-title":"Nat. Commun."},{"key":"B42","doi-asserted-by":"publisher","first-page":"e123","DOI":"10.1093\/nar\/gkp596","article-title":"Transcriptome Analysis by Strand-specific Sequencing of Complementary DNA","volume":"37","author":"Parkhomchuk","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"B43","doi-asserted-by":"publisher","first-page":"1650","DOI":"10.1038\/nprot.2016.095","article-title":"Transcript-level Expression Analysis of RNA-Seq Experiments with HISAT, StringTie and Ballgown","volume":"11","author":"Pertea","year":"2016","journal-title":"Nat. Protoc."},{"key":"B44","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1186\/s13048-018-0381-4","article-title":"Circular RNAs: Biogenesis, Expression and Their Potential Roles in Reproduction","volume":"11","author":"Quan","year":"2018","journal-title":"J. Ovarian Res."},{"key":"B45","doi-asserted-by":"publisher","first-page":"e1000598","DOI":"10.1371\/journal.pcbi.1000598","article-title":"An Abundance of Ubiquitously Expressed Genes Revealed by Tissue Transcriptome Sequence Data","volume":"5","author":"Ramsk\u00f6ld","year":"2009","journal-title":"Plos Comput. Biol."},{"key":"B46","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1111\/j.1439-0531.2008.01177.x","article-title":"Sexual Maturation in the Bull","volume":"43","author":"Rawlings","year":"2008","journal-title":"Reprod. Domest. Anim."},{"key":"B47","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1016\/j.ygcen.2016.04.026","article-title":"Molecular Basis of Spermatogenesis and Sperm Quality","volume":"245","author":"Robles","year":"2017","journal-title":"Gen. Comp. Endocrinol."},{"key":"B48","doi-asserted-by":"publisher","first-page":"3852","DOI":"10.1073\/pnas.73.11.3852","article-title":"Viroids Are Single-Stranded Covalently Closed Circular RNA Molecules Existing as Highly Base-Paired Rod-like Structures","volume":"73","author":"Sanger","year":"1976","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B49","doi-asserted-by":"publisher","first-page":"489","DOI":"10.3390\/genes11050489","article-title":"Transcriptome Analysis of circRNA and mRNA in Theca Cells during Follicular Development in Chickens","volume":"11","author":"Shen","year":"2020","journal-title":"Genes"},{"key":"B50","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1038\/nprot.2008.211","article-title":"Systematic and Integrative Analysis of Large Gene Lists Using DAVID Bioinformatics Resources","volume":"4","author":"Sherman","year":"2009","journal-title":"Nat. Protoc."},{"key":"B51","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1016\/j.gene.2015.07.057","article-title":"Exploiting RNA-Sequencing Data from the Porcine Testes to Identify the Key Genes Involved in Spermatogenesis in Large White Pigs","volume":"573","author":"Song","year":"2015","journal-title":"Gene"},{"key":"B52","doi-asserted-by":"publisher","first-page":"2179","DOI":"10.1016\/j.celrep.2013.05.031","article-title":"Cellular Source and Mechanisms of High Transcriptome Complexity in the Mammalian Testis","volume":"3","author":"Soumillon","year":"2013","journal-title":"Cel Rep."},{"key":"B53","doi-asserted-by":"publisher","first-page":"e166","DOI":"10.1093\/nar\/gkt646","article-title":"Utilizing Sequence Intrinsic Composition to Classify Protein-Coding and Long Non-coding Transcripts","volume":"41","author":"Sun","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"B54","doi-asserted-by":"publisher","first-page":"2409","DOI":"10.1101\/gad.228080.113","article-title":"Building the Mammalian Testis: Origins, Differentiation, and Assembly of the Component Cell Populations","volume":"27","author":"Svingen","year":"2013","journal-title":"Genes Develop."},{"key":"B55","doi-asserted-by":"publisher","first-page":"824","DOI":"10.1038\/s41556-019-0342-1","article-title":"Whsc1 Links Pluripotency Exit with Mesendoderm Specification","volume":"21","author":"Tian","year":"2019","journal-title":"Nat. Cel Biol"},{"key":"B56","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1016\/j.theriogenology.2016.10.020","article-title":"The Value of Trans-scrotal Ultrasonography at Bull Breeding Soundness Evaluation (BBSE): The Relationship between Testicular Parenchymal Pixel Intensity and Semen Quality","volume":"89","author":"Tomlinson","year":"2017","journal-title":"Theriogenology"},{"key":"B57","doi-asserted-by":"publisher","first-page":"511","DOI":"10.1038\/nbt.1621","article-title":"Transcript Assembly and Quantification by RNA-Seq Reveals Unannotated Transcripts and Isoform Switching during Cell Differentiation","volume":"28","author":"Trapnell","year":"2010","journal-title":"Nat. Biotechnol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1186\/1477-7827-12-85","article-title":"MicroRNA-34 Family Expression in Bovine Gametes and Preimplantation Embryos","volume":"12","author":"Tscherner","year":"2014","journal-title":"Reprod. Biol. Endocrinol."},{"key":"B59","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1016\/j.cell.2013.06.020","article-title":"lincRNAs: Genomics, Evolution, and Mechanisms","volume":"154","author":"Ulitsky","year":"2013","journal-title":"Cell"},{"key":"B60","doi-asserted-by":"publisher","first-page":"2602","DOI":"10.1093\/eurheartj\/ehv713","article-title":"A Circular RNA Protects the Heart from Pathological Hypertrophy and Heart Failure by Targeting miR-223","volume":"37","author":"Wang","year":"2016","journal-title":"Eur. Heart J."},{"key":"B61","doi-asserted-by":"publisher","first-page":"1468","DOI":"10.1093\/jas\/sky480","article-title":"Enhanced Sperm Production in Bulls Following Transient Induction of Hypothyroidism during Prepubertal Development","volume":"97","author":"Waqas","year":"2019","journal-title":"J. Anim. Sci."},{"key":"B62","doi-asserted-by":"publisher","first-page":"e0229503","DOI":"10.1371\/journal.pone.0229503","article-title":"Testis Transcriptome Profiling Identified Genes Involved in Spermatogenic Arrest of Cattleyak","volume":"15","author":"Wu","year":"2020","journal-title":"PloS one"},{"key":"B63","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1016\/j.mce.2013.04.015","article-title":"Small RNAs in Spermatogenesis","volume":"382","author":"Yadav","year":"2014","journal-title":"Mol. Cell. Endocrinol."},{"key":"B64","doi-asserted-by":"publisher","first-page":"603","DOI":"10.1038\/nn.3975","article-title":"Neural Circular RNAs Are Derived from Synaptic Genes and Regulated by Development and Plasticity","volume":"18","author":"You","year":"2015","journal-title":"Nat. Neurosci."},{"key":"B65","doi-asserted-by":"publisher","first-page":"94","DOI":"10.1016\/j.semcdb.2015.10.029","article-title":"TGF-\u03b2 Superfamily Signaling in Testis Formation and Early Male Germline Development","volume":"45","author":"Young","year":"2015","journal-title":"Semin. Cel. Dev. Biol."},{"key":"B66","doi-asserted-by":"publisher","first-page":"R14","DOI":"10.1186\/gb-2010-11-2-r14","article-title":"Gene Ontology Analysis for RNA-Seq: Accounting for Selection Bias","volume":"11","author":"Young","year":"2010","journal-title":"Genome Biol."},{"key":"B67","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1095\/biolreprod.102.012609","article-title":"Gene Expression Profiles in Different Stages of Mouse Spermatogenic Cells during Spermatogenesis1","volume":"69","author":"Yu","year":"2003","journal-title":"Biol. Reprod."},{"key":"B68","doi-asserted-by":"publisher","first-page":"1430","DOI":"10.3390\/ani11051430","article-title":"Expression Analysis of Circular RNAs in Young and Sexually Mature Boar Testes","volume":"11","author":"Zhang","year":"2021","journal-title":"Animals"},{"key":"B69","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1095\/biolreprod.114.126672","article-title":"TNP1 Functional SNPs in Bta-miR-532 and Bta-miR-204 Target Sites Are Associated with Semen Quality Traits in Chinese Holstein Bulls","volume":"92","author":"Zhang","year":"2015","journal-title":"Biol. Reprod."},{"key":"B70","doi-asserted-by":"publisher","first-page":"359","DOI":"10.1016\/s0309-1740(00)00160-1","article-title":"Productivity and Carcass Characteristics of Pure and Crossbred Chinese Yellow Cattle","volume":"58","author":"Zhou","year":"2001","journal-title":"Meat Sci."},{"key":"B71","doi-asserted-by":"publisher","first-page":"1443","DOI":"10.1261\/rna.067132.118","article-title":"Rat BodyMap Transcriptomes Reveal Unique Circular RNA Features across Tissue Types and Developmental Stages","volume":"24","author":"Zhou","year":"2018","journal-title":"Rna"}],"container-title":["Frontiers in Genetics"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fgene.2021.685541\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,11,30]],"date-time":"2021-11-30T10:06:43Z","timestamp":1638266803000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fgene.2021.685541\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,22]]},"references-count":70,"alternative-id":["10.3389\/fgene.2021.685541"],"URL":"https:\/\/doi.org\/10.3389\/fgene.2021.685541","relation":{},"ISSN":["1664-8021"],"issn-type":[{"value":"1664-8021","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,22]]},"article-number":"685541"}}