Regulatory mechanism of LncRNAs in gonadal differentiation of hermaphroditic fish, Monopterus albus
Abstract Background Monopterus albus is a hermaphroditic fish with sex reversal from ovaries to testes via the ovotestes in the process of gonadal development, but the molecular mechanism of the sex reversal was unknown. Methods We produced transcriptomes containing mRNAs and lncRNAs in the crucial...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-10-01
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| Series: | Biology of Sex Differences |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13293-023-00559-y |
| _version_ | 1797454086282412032 |
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| author | Qiaomu Hu Xueping Xia Zitong Lian Haifeng Tian Zhong Li |
| author_facet | Qiaomu Hu Xueping Xia Zitong Lian Haifeng Tian Zhong Li |
| author_sort | Qiaomu Hu |
| collection | DOAJ |
| description | Abstract Background Monopterus albus is a hermaphroditic fish with sex reversal from ovaries to testes via the ovotestes in the process of gonadal development, but the molecular mechanism of the sex reversal was unknown. Methods We produced transcriptomes containing mRNAs and lncRNAs in the crucial stages of the gonad, including the ovary, ovotestis and testis. The expression of the crucial lncRNAs and their target genes was detected using qRT‒PCR and in situ hybridization. The methylation level and activity of the lncRNA promoter were analysed by applying bisulfite sequencing PCR and dual-luciferase reporter assays, respectively. Results This effort revealed that gonadal development was a dynamic expression change. Regulatory networks of lncRNAs and their target genes were constructed through integrated analysis of lncRNA and mRNA data. The expression and DNA methylation of the lncRNAs MSTRG.38036 and MSTRG.12998 and their target genes Psmβ8 and Ptk2β were detected in developing gonads and sex reversal gonads. The results showed that lncRNAs and their target genes exhibited consistent expression profiles and that the DNA methylation levels were negatively regulated lncRNA expression. Furthermore, we found that Ptk2β probably regulates cyp19a1 expression via the Ptk2β/EGFR/STAT3 pathway to reprogram sex differentiation. Conclusions This study provides novel insight from lncRNA to explore the potential molecular mechanism by which DNA methylation regulates lncRNA expression to facilitate target gene transcription to reprogram sex differentiation in M. albus, which will also enrich the sex differentiation mechanism of teleosts. |
| first_indexed | 2024-03-09T15:32:11Z |
| format | Article |
| id | doaj.art-6e66f9c86c024f84bd95fd91fbb858dc |
| institution | Directory Open Access Journal |
| issn | 2042-6410 |
| language | English |
| last_indexed | 2024-03-09T15:32:11Z |
| publishDate | 2023-10-01 |
| publisher | BMC |
| record_format | Article |
| series | Biology of Sex Differences |
| spelling | doaj.art-6e66f9c86c024f84bd95fd91fbb858dc2023-11-26T12:09:47ZengBMCBiology of Sex Differences2042-64102023-10-0114111410.1186/s13293-023-00559-yRegulatory mechanism of LncRNAs in gonadal differentiation of hermaphroditic fish, Monopterus albusQiaomu Hu0Xueping Xia1Zitong Lian2Haifeng Tian3Zhong Li4Yangtze River Fisheries Research Institute, Chinese Academy of Fishery SciencesYangtze River Fisheries Research Institute, Chinese Academy of Fishery SciencesYangtze River Fisheries Research Institute, Chinese Academy of Fishery SciencesYangtze River Fisheries Research Institute, Chinese Academy of Fishery SciencesYangtze River Fisheries Research Institute, Chinese Academy of Fishery SciencesAbstract Background Monopterus albus is a hermaphroditic fish with sex reversal from ovaries to testes via the ovotestes in the process of gonadal development, but the molecular mechanism of the sex reversal was unknown. Methods We produced transcriptomes containing mRNAs and lncRNAs in the crucial stages of the gonad, including the ovary, ovotestis and testis. The expression of the crucial lncRNAs and their target genes was detected using qRT‒PCR and in situ hybridization. The methylation level and activity of the lncRNA promoter were analysed by applying bisulfite sequencing PCR and dual-luciferase reporter assays, respectively. Results This effort revealed that gonadal development was a dynamic expression change. Regulatory networks of lncRNAs and their target genes were constructed through integrated analysis of lncRNA and mRNA data. The expression and DNA methylation of the lncRNAs MSTRG.38036 and MSTRG.12998 and their target genes Psmβ8 and Ptk2β were detected in developing gonads and sex reversal gonads. The results showed that lncRNAs and their target genes exhibited consistent expression profiles and that the DNA methylation levels were negatively regulated lncRNA expression. Furthermore, we found that Ptk2β probably regulates cyp19a1 expression via the Ptk2β/EGFR/STAT3 pathway to reprogram sex differentiation. Conclusions This study provides novel insight from lncRNA to explore the potential molecular mechanism by which DNA methylation regulates lncRNA expression to facilitate target gene transcription to reprogram sex differentiation in M. albus, which will also enrich the sex differentiation mechanism of teleosts.https://doi.org/10.1186/s13293-023-00559-yMonopterus albusLncRNADNA methylationSex reversalGene expression |
| spellingShingle | Qiaomu Hu Xueping Xia Zitong Lian Haifeng Tian Zhong Li Regulatory mechanism of LncRNAs in gonadal differentiation of hermaphroditic fish, Monopterus albus Biology of Sex Differences Monopterus albus LncRNA DNA methylation Sex reversal Gene expression |
| title | Regulatory mechanism of LncRNAs in gonadal differentiation of hermaphroditic fish, Monopterus albus |
| title_full | Regulatory mechanism of LncRNAs in gonadal differentiation of hermaphroditic fish, Monopterus albus |
| title_fullStr | Regulatory mechanism of LncRNAs in gonadal differentiation of hermaphroditic fish, Monopterus albus |
| title_full_unstemmed | Regulatory mechanism of LncRNAs in gonadal differentiation of hermaphroditic fish, Monopterus albus |
| title_short | Regulatory mechanism of LncRNAs in gonadal differentiation of hermaphroditic fish, Monopterus albus |
| title_sort | regulatory mechanism of lncrnas in gonadal differentiation of hermaphroditic fish monopterus albus |
| topic | Monopterus albus LncRNA DNA methylation Sex reversal Gene expression |
| url | https://doi.org/10.1186/s13293-023-00559-y |
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