Transcriptomic Analysis Reveals Functional Interaction of mRNA–lncRNA–miRNA in Steroidogenesis and Spermatogenesis of Gynogenetic Japanese Flounder (<i>Paralichthys olivaceus</i>)
Teleost fishes exhibit extraordinary diversity, plasticity and adaptability with their sex determination and sexual development, and there is growing evidence that non-coding RNAs (ncRNAs) are emerging as critical regulators of reproduction. Japanese flounder (<i>Paralichthys olivaceus</i&g...
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MDPI AG
2022-01-01
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| author | Jie Cheng Fan Yang Saisai Liu Haitao Zhao Wei Lu Quanqi Zhang |
| author_facet | Jie Cheng Fan Yang Saisai Liu Haitao Zhao Wei Lu Quanqi Zhang |
| author_sort | Jie Cheng |
| collection | DOAJ |
| description | Teleost fishes exhibit extraordinary diversity, plasticity and adaptability with their sex determination and sexual development, and there is growing evidence that non-coding RNAs (ncRNAs) are emerging as critical regulators of reproduction. Japanese flounder (<i>Paralichthys olivaceus</i>) is an important marine cultured fish that presents significant sexual dimorphism with bigger females, in which gynogenesis has been applied for aquaculture industry. In order to reveal the regulatory mechanisms of sexual development in gynogenetic female and sex-reversed neo-male <i>P. olivaceus</i>, the lncRNA–miRNA–mRNA interactions were investigated using high-throughput sequencing. A total of 6772 differentially expressed mRNAs (DEmRNAs), 2284 DElncRNAs, and 244 DEmiRNAs were obtained between gynogenetic female ovaries and sex-reversed neo-male testes. Genes in the steroid hormone biosynthesis and secretion pathway were enriched and mostly significantly upregulated in neo-male testes. Subsequently, network analysis uncovered high functional specificity for gynogenetic <i>P. olivaceus</i> sperm motility, as co-expressed DEmRNAs were significantly enriched in microtubule and cytoskeleton-related biological processes. Clustered miRNAs were characterized in the <i>P. olivaceus</i> genome with examples of the largest conserved <i>let-7</i> clusters. The 20 <i>let-7</i> members are distributed in 11 clusters and may not transcribe together with their neighboring <i>miR-125b</i>, with <i>let-7</i> repressing <i>cyp11a</i> and <i>miR-125b</i> repressing <i>esr2b</i>, both as key steroidogenesis pathway genes. In summary, this study provides comprehensive insights into the mRNA–miRNA–lncRNA functional crosstalk in teleost sexual development and gametogenesis and will expand our understanding of ncRNA biology in teleost gynogenesis. |
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| spelling | doaj.art-b7e9ad4022cc4e8b8cc9f26adb661c3b2023-11-23T18:49:48ZengMDPI AGBiology2079-77372022-01-0111221310.3390/biology11020213Transcriptomic Analysis Reveals Functional Interaction of mRNA–lncRNA–miRNA in Steroidogenesis and Spermatogenesis of Gynogenetic Japanese Flounder (<i>Paralichthys olivaceus</i>)Jie Cheng0Fan Yang1Saisai Liu2Haitao Zhao3Wei Lu4Quanqi Zhang5Key Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, 5 Yushan Road, Qingdao 266003, ChinaKey Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, 5 Yushan Road, Qingdao 266003, ChinaKey Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, 5 Yushan Road, Qingdao 266003, ChinaKey Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, 5 Yushan Road, Qingdao 266003, ChinaKey Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, 5 Yushan Road, Qingdao 266003, ChinaKey Laboratory of Marine Genetics and Breeding (Ocean University of China), Ministry of Education, 5 Yushan Road, Qingdao 266003, ChinaTeleost fishes exhibit extraordinary diversity, plasticity and adaptability with their sex determination and sexual development, and there is growing evidence that non-coding RNAs (ncRNAs) are emerging as critical regulators of reproduction. Japanese flounder (<i>Paralichthys olivaceus</i>) is an important marine cultured fish that presents significant sexual dimorphism with bigger females, in which gynogenesis has been applied for aquaculture industry. In order to reveal the regulatory mechanisms of sexual development in gynogenetic female and sex-reversed neo-male <i>P. olivaceus</i>, the lncRNA–miRNA–mRNA interactions were investigated using high-throughput sequencing. A total of 6772 differentially expressed mRNAs (DEmRNAs), 2284 DElncRNAs, and 244 DEmiRNAs were obtained between gynogenetic female ovaries and sex-reversed neo-male testes. Genes in the steroid hormone biosynthesis and secretion pathway were enriched and mostly significantly upregulated in neo-male testes. Subsequently, network analysis uncovered high functional specificity for gynogenetic <i>P. olivaceus</i> sperm motility, as co-expressed DEmRNAs were significantly enriched in microtubule and cytoskeleton-related biological processes. Clustered miRNAs were characterized in the <i>P. olivaceus</i> genome with examples of the largest conserved <i>let-7</i> clusters. The 20 <i>let-7</i> members are distributed in 11 clusters and may not transcribe together with their neighboring <i>miR-125b</i>, with <i>let-7</i> repressing <i>cyp11a</i> and <i>miR-125b</i> repressing <i>esr2b</i>, both as key steroidogenesis pathway genes. In summary, this study provides comprehensive insights into the mRNA–miRNA–lncRNA functional crosstalk in teleost sexual development and gametogenesis and will expand our understanding of ncRNA biology in teleost gynogenesis.https://www.mdpi.com/2079-7737/11/2/213<i>Paralichthys olivaceus</i>gynogenesisnon-coding RNAmicroRNA clustergametogenesis |
| spellingShingle | Jie Cheng Fan Yang Saisai Liu Haitao Zhao Wei Lu Quanqi Zhang Transcriptomic Analysis Reveals Functional Interaction of mRNA–lncRNA–miRNA in Steroidogenesis and Spermatogenesis of Gynogenetic Japanese Flounder (<i>Paralichthys olivaceus</i>) Biology <i>Paralichthys olivaceus</i> gynogenesis non-coding RNA microRNA cluster gametogenesis |
| title | Transcriptomic Analysis Reveals Functional Interaction of mRNA–lncRNA–miRNA in Steroidogenesis and Spermatogenesis of Gynogenetic Japanese Flounder (<i>Paralichthys olivaceus</i>) |
| title_full | Transcriptomic Analysis Reveals Functional Interaction of mRNA–lncRNA–miRNA in Steroidogenesis and Spermatogenesis of Gynogenetic Japanese Flounder (<i>Paralichthys olivaceus</i>) |
| title_fullStr | Transcriptomic Analysis Reveals Functional Interaction of mRNA–lncRNA–miRNA in Steroidogenesis and Spermatogenesis of Gynogenetic Japanese Flounder (<i>Paralichthys olivaceus</i>) |
| title_full_unstemmed | Transcriptomic Analysis Reveals Functional Interaction of mRNA–lncRNA–miRNA in Steroidogenesis and Spermatogenesis of Gynogenetic Japanese Flounder (<i>Paralichthys olivaceus</i>) |
| title_short | Transcriptomic Analysis Reveals Functional Interaction of mRNA–lncRNA–miRNA in Steroidogenesis and Spermatogenesis of Gynogenetic Japanese Flounder (<i>Paralichthys olivaceus</i>) |
| title_sort | transcriptomic analysis reveals functional interaction of mrna lncrna mirna in steroidogenesis and spermatogenesis of gynogenetic japanese flounder i paralichthys olivaceus i |
| topic | <i>Paralichthys olivaceus</i> gynogenesis non-coding RNA microRNA cluster gametogenesis |
| url | https://www.mdpi.com/2079-7737/11/2/213 |
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