A single‐nucleus transcriptomic atlas characterizes cell types and their molecular features in the ovary of adult Nile tilapia
In fish species, there is limited analysis of signature transcriptome profiles at the single‐cell level in gonadal cells. Here, the molecular signatures of distinct ovarian cell categories in adult Nile tilapia (Oreochromis niloticus) were analysed using single‐nucleus RNA sequencing (snRNA‐seq). We...
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creator | Yao, Zhi Lei Wang, Xiao Hu, Chun Lei Chen, Fu Xiao Chen, Hong Ju Jiang, Shi‐Jin Zhao, Yan Ji, Xiang Shan |
description | In fish species, there is limited analysis of signature transcriptome profiles at the single‐cell level in gonadal cells. Here, the molecular signatures of distinct ovarian cell categories in adult Nile tilapia (Oreochromis niloticus) were analysed using single‐nucleus RNA sequencing (snRNA‐seq). We identified four cell types (oogonia, oocytes, granulosa cell, and thecal cell) based on their specifically expressed genes and biological functions. Similarly, we found some key pathways involved in ovarian development that may affect germline–somatic interactions. A cell‐to‐cell communication network between the distinct cell types was constructed. We found that the bidirectional communication is mandatory for the development of germ cells and somatic cells in fish ovaries, and the granulosa cells and thecal cells play a central regulating role in the cell network in fish ovary. Additionally, we identified some novel candidate marker genes for various types of ovarian cells and also validated them using in situ hybridization. Our work reveals an ovarian atlas at the cellular and molecular levels and contributes to providing insights into oogenesis and gonad development in fish. |
doi_str_mv | 10.1111/jfb.15911 |
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Here, the molecular signatures of distinct ovarian cell categories in adult Nile tilapia (Oreochromis niloticus) were analysed using single‐nucleus RNA sequencing (snRNA‐seq). We identified four cell types (oogonia, oocytes, granulosa cell, and thecal cell) based on their specifically expressed genes and biological functions. Similarly, we found some key pathways involved in ovarian development that may affect germline–somatic interactions. A cell‐to‐cell communication network between the distinct cell types was constructed. We found that the bidirectional communication is mandatory for the development of germ cells and somatic cells in fish ovaries, and the granulosa cells and thecal cells play a central regulating role in the cell network in fish ovary. Additionally, we identified some novel candidate marker genes for various types of ovarian cells and also validated them using in situ hybridization. Our work reveals an ovarian atlas at the cellular and molecular levels and contributes to providing insights into oogenesis and gonad development in fish.</description><identifier>ISSN: 0022-1112</identifier><identifier>ISSN: 1095-8649</identifier><identifier>EISSN: 1095-8649</identifier><identifier>DOI: 10.1111/jfb.15911</identifier><identifier>PMID: 39235098</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>adults ; Animals ; cell communication ; Cell interactions ; Cells ; Cichlids - genetics ; Cichlids - growth & development ; Female ; Fish ; Gametocytes ; Gene sequencing ; Genes ; Germ cells ; Gonads ; Granulosa cells ; Hybridization ; Marine fishes ; Nile tilapia ; Nuclei (cytology) ; Nucleus ; Oocytes ; Oogenesis ; Oogonia ; Oreochromis niloticus ; ovarian development ; Ovaries ; ovary ; Ovary - cytology ; RNA ; RNA sequencing ; Sequence Analysis, RNA ; Single-Cell Analysis ; single‐nucleus RNA sequencing ; snRNA ; Somatic cells ; Tilapia ; Transcriptome ; Transcriptomes ; Transcriptomics ; Whitefish</subject><ispartof>Journal of fish biology, 2024-12, Vol.105 (6), p.1800-1810</ispartof><rights>2024 Fisheries Society of the British Isles.</rights><rights>Journal of Fish Biology © 2024 The Fisheries Society of the British Isles</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3461-2c1321471b8b13f2ef23877d3fd7c67fdeed04dc7fac023b96ab9bd9cb4ebc3</cites><orcidid>0009-0000-4784-6423 ; 0000-0002-3285-7952</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fjfb.15911$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fjfb.15911$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39235098$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yao, Zhi Lei</creatorcontrib><creatorcontrib>Wang, Xiao</creatorcontrib><creatorcontrib>Hu, Chun Lei</creatorcontrib><creatorcontrib>Chen, Fu Xiao</creatorcontrib><creatorcontrib>Chen, Hong Ju</creatorcontrib><creatorcontrib>Jiang, Shi‐Jin</creatorcontrib><creatorcontrib>Zhao, Yan</creatorcontrib><creatorcontrib>Ji, Xiang Shan</creatorcontrib><title>A single‐nucleus transcriptomic atlas characterizes cell types and their molecular features in the ovary of adult Nile tilapia</title><title>Journal of fish biology</title><addtitle>J Fish Biol</addtitle><description>In fish species, there is limited analysis of signature transcriptome profiles at the single‐cell level in gonadal cells. Here, the molecular signatures of distinct ovarian cell categories in adult Nile tilapia (Oreochromis niloticus) were analysed using single‐nucleus RNA sequencing (snRNA‐seq). We identified four cell types (oogonia, oocytes, granulosa cell, and thecal cell) based on their specifically expressed genes and biological functions. Similarly, we found some key pathways involved in ovarian development that may affect germline–somatic interactions. A cell‐to‐cell communication network between the distinct cell types was constructed. We found that the bidirectional communication is mandatory for the development of germ cells and somatic cells in fish ovaries, and the granulosa cells and thecal cells play a central regulating role in the cell network in fish ovary. Additionally, we identified some novel candidate marker genes for various types of ovarian cells and also validated them using in situ hybridization. Our work reveals an ovarian atlas at the cellular and molecular levels and contributes to providing insights into oogenesis and gonad development in fish.</description><subject>adults</subject><subject>Animals</subject><subject>cell communication</subject><subject>Cell interactions</subject><subject>Cells</subject><subject>Cichlids - genetics</subject><subject>Cichlids - growth & development</subject><subject>Female</subject><subject>Fish</subject><subject>Gametocytes</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Germ cells</subject><subject>Gonads</subject><subject>Granulosa cells</subject><subject>Hybridization</subject><subject>Marine fishes</subject><subject>Nile tilapia</subject><subject>Nuclei (cytology)</subject><subject>Nucleus</subject><subject>Oocytes</subject><subject>Oogenesis</subject><subject>Oogonia</subject><subject>Oreochromis niloticus</subject><subject>ovarian development</subject><subject>Ovaries</subject><subject>ovary</subject><subject>Ovary - cytology</subject><subject>RNA</subject><subject>RNA sequencing</subject><subject>Sequence Analysis, RNA</subject><subject>Single-Cell Analysis</subject><subject>single‐nucleus RNA sequencing</subject><subject>snRNA</subject><subject>Somatic cells</subject><subject>Tilapia</subject><subject>Transcriptome</subject><subject>Transcriptomes</subject><subject>Transcriptomics</subject><subject>Whitefish</subject><issn>0022-1112</issn><issn>1095-8649</issn><issn>1095-8649</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkbtuFDEUhi1ERJZAwQsgSzRQTOLb7IzLECVAFEEB_ciXY-KV54IvoE2VR-AZeRK8bEIRCQk3tnU-_dL5P4ReUHJM6znZOH1MW0npI7SiRLZNvxbyMVoRwlhTAXaInqa0IYRILvkTdMgl4y2R_QrdnuLkp68Bft3-nIoJUBLOUU3JRL_kefQGqxxUwuZaRWUyRH8D9Qch4Lxd6lNNFudr8BGPcwBTgorYgcol1qGfdjM8f1dxi2eHlS0h448-AM4-qMWrZ-jAqZDg-d19hD5fnH85e99cfXr34ez0qjFcrGnDDOWMio7qXlPuGDjG-66z3NnOrDtnASwR1nROGcK4lmulpbbSaAHa8CP0ep-6xPlbgZSH0afdEmqCuaSB01awjnDC_wOtNVIpWlrRVw_QzVziVNeolGirEdmLSr3ZUybOKUVwwxL9WAsZKBl2_obqb_jjr7Iv7xKLHsH-Je-FVeBkD_yoHW7_nTRcXrzdR_4GrUGnEw</recordid><startdate>202412</startdate><enddate>202412</enddate><creator>Yao, Zhi Lei</creator><creator>Wang, Xiao</creator><creator>Hu, Chun Lei</creator><creator>Chen, Fu Xiao</creator><creator>Chen, Hong Ju</creator><creator>Jiang, Shi‐Jin</creator><creator>Zhao, Yan</creator><creator>Ji, Xiang Shan</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7SN</scope><scope>7TN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0009-0000-4784-6423</orcidid><orcidid>https://orcid.org/0000-0002-3285-7952</orcidid></search><sort><creationdate>202412</creationdate><title>A single‐nucleus transcriptomic atlas characterizes cell types and their molecular features in the ovary of adult Nile tilapia</title><author>Yao, Zhi Lei ; Wang, Xiao ; Hu, Chun Lei ; Chen, Fu Xiao ; Chen, Hong Ju ; Jiang, Shi‐Jin ; Zhao, Yan ; Ji, Xiang Shan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3461-2c1321471b8b13f2ef23877d3fd7c67fdeed04dc7fac023b96ab9bd9cb4ebc3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>adults</topic><topic>Animals</topic><topic>cell communication</topic><topic>Cell interactions</topic><topic>Cells</topic><topic>Cichlids - genetics</topic><topic>Cichlids - growth & development</topic><topic>Female</topic><topic>Fish</topic><topic>Gametocytes</topic><topic>Gene sequencing</topic><topic>Genes</topic><topic>Germ cells</topic><topic>Gonads</topic><topic>Granulosa cells</topic><topic>Hybridization</topic><topic>Marine fishes</topic><topic>Nile tilapia</topic><topic>Nuclei (cytology)</topic><topic>Nucleus</topic><topic>Oocytes</topic><topic>Oogenesis</topic><topic>Oogonia</topic><topic>Oreochromis niloticus</topic><topic>ovarian development</topic><topic>Ovaries</topic><topic>ovary</topic><topic>Ovary - cytology</topic><topic>RNA</topic><topic>RNA sequencing</topic><topic>Sequence Analysis, RNA</topic><topic>Single-Cell Analysis</topic><topic>single‐nucleus RNA sequencing</topic><topic>snRNA</topic><topic>Somatic cells</topic><topic>Tilapia</topic><topic>Transcriptome</topic><topic>Transcriptomes</topic><topic>Transcriptomics</topic><topic>Whitefish</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yao, Zhi Lei</creatorcontrib><creatorcontrib>Wang, Xiao</creatorcontrib><creatorcontrib>Hu, Chun Lei</creatorcontrib><creatorcontrib>Chen, Fu Xiao</creatorcontrib><creatorcontrib>Chen, Hong Ju</creatorcontrib><creatorcontrib>Jiang, Shi‐Jin</creatorcontrib><creatorcontrib>Zhao, Yan</creatorcontrib><creatorcontrib>Ji, Xiang Shan</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Ecology Abstracts</collection><collection>Oceanic Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Journal of fish biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yao, Zhi Lei</au><au>Wang, Xiao</au><au>Hu, Chun Lei</au><au>Chen, Fu Xiao</au><au>Chen, Hong Ju</au><au>Jiang, Shi‐Jin</au><au>Zhao, Yan</au><au>Ji, Xiang Shan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A single‐nucleus transcriptomic atlas characterizes cell types and their molecular features in the ovary of adult Nile tilapia</atitle><jtitle>Journal of fish biology</jtitle><addtitle>J Fish Biol</addtitle><date>2024-12</date><risdate>2024</risdate><volume>105</volume><issue>6</issue><spage>1800</spage><epage>1810</epage><pages>1800-1810</pages><issn>0022-1112</issn><issn>1095-8649</issn><eissn>1095-8649</eissn><abstract>In fish species, there is limited analysis of signature transcriptome profiles at the single‐cell level in gonadal cells. Here, the molecular signatures of distinct ovarian cell categories in adult Nile tilapia (Oreochromis niloticus) were analysed using single‐nucleus RNA sequencing (snRNA‐seq). We identified four cell types (oogonia, oocytes, granulosa cell, and thecal cell) based on their specifically expressed genes and biological functions. Similarly, we found some key pathways involved in ovarian development that may affect germline–somatic interactions. A cell‐to‐cell communication network between the distinct cell types was constructed. We found that the bidirectional communication is mandatory for the development of germ cells and somatic cells in fish ovaries, and the granulosa cells and thecal cells play a central regulating role in the cell network in fish ovary. Additionally, we identified some novel candidate marker genes for various types of ovarian cells and also validated them using in situ hybridization. Our work reveals an ovarian atlas at the cellular and molecular levels and contributes to providing insights into oogenesis and gonad development in fish.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>39235098</pmid><doi>10.1111/jfb.15911</doi><tpages>11</tpages><orcidid>https://orcid.org/0009-0000-4784-6423</orcidid><orcidid>https://orcid.org/0000-0002-3285-7952</orcidid></addata></record> |
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subjects | adults Animals cell communication Cell interactions Cells Cichlids - genetics Cichlids - growth & development Female Fish Gametocytes Gene sequencing Genes Germ cells Gonads Granulosa cells Hybridization Marine fishes Nile tilapia Nuclei (cytology) Nucleus Oocytes Oogenesis Oogonia Oreochromis niloticus ovarian development Ovaries ovary Ovary - cytology RNA RNA sequencing Sequence Analysis, RNA Single-Cell Analysis single‐nucleus RNA sequencing snRNA Somatic cells Tilapia Transcriptome Transcriptomes Transcriptomics Whitefish |
title | A single‐nucleus transcriptomic atlas characterizes cell types and their molecular features in the ovary of adult Nile tilapia |
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