Single-Cell Atlas of the Chinese Tongue Sole (Cynoglossus semilaevis) Ovary Reveals Transcriptional Programs of Oogenesis in Fish
Oogenesis is a highly orchestrated process that depends on regulation by autocrine/paracrine hormones and growth factors. However, many details of the molecular mechanisms that regulate fish oogenesis remain elusive. Here, we performed a single-cell RNA sequencing (scRNA-seq) analysis of the molecul...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-03-01
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| Series: | Frontiers in Cell and Developmental Biology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2022.828124/full |
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| author | Xiang Liu Xiang Liu Yingyi Huang Yingyi Huang Fujian Tan Fujian Tan Hong-Yan Wang Hong-Yan Wang Jian-Yang Chen Jian-Yang Chen Jian-Yang Chen Xianghui Zhang Xianghui Zhang Xiaona Zhao Xiaona Zhao Kaiqiang Liu Kaiqiang Liu Qian Wang Qian Wang Shanshan Liu Shanshan Liu Shanshan Liu Francesc Piferrer Guangyi Fan Guangyi Fan Changwei Shao Changwei Shao |
| author_facet | Xiang Liu Xiang Liu Yingyi Huang Yingyi Huang Fujian Tan Fujian Tan Hong-Yan Wang Hong-Yan Wang Jian-Yang Chen Jian-Yang Chen Jian-Yang Chen Xianghui Zhang Xianghui Zhang Xiaona Zhao Xiaona Zhao Kaiqiang Liu Kaiqiang Liu Qian Wang Qian Wang Shanshan Liu Shanshan Liu Shanshan Liu Francesc Piferrer Guangyi Fan Guangyi Fan Changwei Shao Changwei Shao |
| author_sort | Xiang Liu |
| collection | DOAJ |
| description | Oogenesis is a highly orchestrated process that depends on regulation by autocrine/paracrine hormones and growth factors. However, many details of the molecular mechanisms that regulate fish oogenesis remain elusive. Here, we performed a single-cell RNA sequencing (scRNA-seq) analysis of the molecular signatures of distinct ovarian cell categories in adult Chinese tongue sole (Cynoglossus semilaevis). We characterized the successive stepwise development of three germ cell subtypes. Notably, we identified the cellular composition of fish follicle walls, including four granulosa cell types and one theca cell type, and we proposed important transcription factors (TFs) showing high activity in the regulation of cell identity. Moreover, we found that the extensive niche–germline bidirectional communications regulate fish oogenesis, whereas ovulation in fish is accompanied by the coordination of simultaneous and tightly sequential processes across different granulosa cells. Additionally, a systems biology analysis of the homologous genes shared by Chinese tongue sole and macaques revealed remarkably conserved biological processes in germ cells and granulosa cells across vertebrates. Our results provide key insights into the cell-type-specific mechanisms underlying fish oogenesis at a single-cell resolution, which offers important clues for exploring fish breeding mechanisms and the evolution of vertebrate reproductive systems. |
| first_indexed | 2024-12-21T00:01:10Z |
| format | Article |
| id | doaj.art-4c7711212880421a97750781ebb32842 |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-12-21T00:01:10Z |
| publishDate | 2022-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-4c7711212880421a97750781ebb328422022-12-21T19:22:35ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2022-03-011010.3389/fcell.2022.828124828124Single-Cell Atlas of the Chinese Tongue Sole (Cynoglossus semilaevis) Ovary Reveals Transcriptional Programs of Oogenesis in FishXiang Liu0Xiang Liu1Yingyi Huang2Yingyi Huang3Fujian Tan4Fujian Tan5Hong-Yan Wang6Hong-Yan Wang7Jian-Yang Chen8Jian-Yang Chen9Jian-Yang Chen10Xianghui Zhang11Xianghui Zhang12Xiaona Zhao13Xiaona Zhao14Kaiqiang Liu15Kaiqiang Liu16Qian Wang17Qian Wang18Shanshan Liu19Shanshan Liu20Shanshan Liu21Francesc Piferrer22Guangyi Fan23Guangyi Fan24Changwei Shao25Changwei Shao26College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, ChinaKey Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaCollege of Fisheries and Life Science, Shanghai Ocean University, Shanghai, ChinaKey Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaBGI-Qingdao, BGI-Shenzhen, Qingdao, ChinaBGI-Shenzhen, Shenzhen, ChinaKey Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaBGI-Qingdao, BGI-Shenzhen, Qingdao, ChinaBGI-Shenzhen, Shenzhen, ChinaQingdao-Europe Advanced Institute for Life Sciences, BGI-Shenzhen, Qingdao, ChinaKey Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaCollege of Marine Technology and Environment, Dalian Ocean University, Dalian, ChinaKey Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaSchool of Marine Sciences, Ningbo University, Ningbo, ChinaKey Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaKey Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaBGI-Qingdao, BGI-Shenzhen, Qingdao, ChinaBGI-Shenzhen, Shenzhen, ChinaQingdao-Europe Advanced Institute for Life Sciences, BGI-Shenzhen, Qingdao, ChinaInstitut de Ciències Del Mar (ICM), Spanish National Research Council (CSIC), Barcelona, SpainBGI-Qingdao, BGI-Shenzhen, Qingdao, ChinaBGI-Shenzhen, Shenzhen, ChinaKey Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaOogenesis is a highly orchestrated process that depends on regulation by autocrine/paracrine hormones and growth factors. However, many details of the molecular mechanisms that regulate fish oogenesis remain elusive. Here, we performed a single-cell RNA sequencing (scRNA-seq) analysis of the molecular signatures of distinct ovarian cell categories in adult Chinese tongue sole (Cynoglossus semilaevis). We characterized the successive stepwise development of three germ cell subtypes. Notably, we identified the cellular composition of fish follicle walls, including four granulosa cell types and one theca cell type, and we proposed important transcription factors (TFs) showing high activity in the regulation of cell identity. Moreover, we found that the extensive niche–germline bidirectional communications regulate fish oogenesis, whereas ovulation in fish is accompanied by the coordination of simultaneous and tightly sequential processes across different granulosa cells. Additionally, a systems biology analysis of the homologous genes shared by Chinese tongue sole and macaques revealed remarkably conserved biological processes in germ cells and granulosa cells across vertebrates. Our results provide key insights into the cell-type-specific mechanisms underlying fish oogenesis at a single-cell resolution, which offers important clues for exploring fish breeding mechanisms and the evolution of vertebrate reproductive systems.https://www.frontiersin.org/articles/10.3389/fcell.2022.828124/fullscRNA-seqoogenesisChinese tongue solegerm cellgranulosa cell |
| spellingShingle | Xiang Liu Xiang Liu Yingyi Huang Yingyi Huang Fujian Tan Fujian Tan Hong-Yan Wang Hong-Yan Wang Jian-Yang Chen Jian-Yang Chen Jian-Yang Chen Xianghui Zhang Xianghui Zhang Xiaona Zhao Xiaona Zhao Kaiqiang Liu Kaiqiang Liu Qian Wang Qian Wang Shanshan Liu Shanshan Liu Shanshan Liu Francesc Piferrer Guangyi Fan Guangyi Fan Changwei Shao Changwei Shao Single-Cell Atlas of the Chinese Tongue Sole (Cynoglossus semilaevis) Ovary Reveals Transcriptional Programs of Oogenesis in Fish Frontiers in Cell and Developmental Biology scRNA-seq oogenesis Chinese tongue sole germ cell granulosa cell |
| title | Single-Cell Atlas of the Chinese Tongue Sole (Cynoglossus semilaevis) Ovary Reveals Transcriptional Programs of Oogenesis in Fish |
| title_full | Single-Cell Atlas of the Chinese Tongue Sole (Cynoglossus semilaevis) Ovary Reveals Transcriptional Programs of Oogenesis in Fish |
| title_fullStr | Single-Cell Atlas of the Chinese Tongue Sole (Cynoglossus semilaevis) Ovary Reveals Transcriptional Programs of Oogenesis in Fish |
| title_full_unstemmed | Single-Cell Atlas of the Chinese Tongue Sole (Cynoglossus semilaevis) Ovary Reveals Transcriptional Programs of Oogenesis in Fish |
| title_short | Single-Cell Atlas of the Chinese Tongue Sole (Cynoglossus semilaevis) Ovary Reveals Transcriptional Programs of Oogenesis in Fish |
| title_sort | single cell atlas of the chinese tongue sole cynoglossus semilaevis ovary reveals transcriptional programs of oogenesis in fish |
| topic | scRNA-seq oogenesis Chinese tongue sole germ cell granulosa cell |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2022.828124/full |
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