Single-Nucleus RNA Sequencing Reveals the Transcriptome Profiling of Ovarian Cells in Adolescent <i>Cyprinus carpio</i>

The common carp (<i>Cyprinus carpio</i>) is a crucial freshwater species cultivated worldwide for food consumption. Female carp have better growth performance than males, which fascinates scholars to uncover the mechanism of gonadal differentiation and produce mono-sex populations. Howev...

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Main Authors: Mingxi Hou, Jin Zhang, Qi Wang, Ran Zhao, Yiming Cao, Yingjie Chen, Kaikuo Wang, Ning Ding, Yingjie Qi, Xiaoqing Sun, Yan Zhang, Jiongtang Li
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Animals
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Online Access:https://www.mdpi.com/2076-2615/14/22/3263
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author Mingxi Hou
Jin Zhang
Qi Wang
Ran Zhao
Yiming Cao
Yingjie Chen
Kaikuo Wang
Ning Ding
Yingjie Qi
Xiaoqing Sun
Yan Zhang
Jiongtang Li
author_facet Mingxi Hou
Jin Zhang
Qi Wang
Ran Zhao
Yiming Cao
Yingjie Chen
Kaikuo Wang
Ning Ding
Yingjie Qi
Xiaoqing Sun
Yan Zhang
Jiongtang Li
author_sort Mingxi Hou
collection DOAJ
description The common carp (<i>Cyprinus carpio</i>) is a crucial freshwater species cultivated worldwide for food consumption. Female carp have better growth performance than males, which fascinates scholars to uncover the mechanism of gonadal differentiation and produce mono-sex populations. However, the mechanism of ovarian development at single-cell resolution is limited. Here, we conducted single-nucleus RNA sequencing in adolescent common carp ovaries. Our study obtained transcriptional profiles of 13,155 nuclei and revealed 13 distinct cell clusters in the ovaries, including three subtypes of germ cells and four subtypes of granulosa cells. We subsequently performed pseudotime trajectory analysis to delineate potential mechanisms underlying the development of germ cells and granulosa cells. We identified 1250 dynamic expression genes in germ cells and 1815 in granulosa cells (<i>q</i>-value < 0.01), including <i>zp3</i>, <i>eif4a2</i> and <i>aspm</i> in germ cells and <i>fshr</i> and <i>esr1</i> in granulosa cells. The functional annotation showed that dynamic expression genes in germ cells were involved in sperm–egg recognition and some terms related to meiosis, such as sister chromatid segregation and homologous recombination. Genes expressed dynamically in granulosa cells were related to the TGF-β signaling pathway, response to gonadotropin, and development of primary female sexual characteristics. In addition, the dynamic genes expressed in granulosa cells might relate to the complex communication between different cell types. In summary, our study provided a transcriptome profile of common carp ovaries at single-nucleus resolution, and we further revealed the potential cell type-specific mechanisms underlying oogenesis and the differentiation of granulosa cells, which will facilitate breeding all-female common carp populations.
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spelling doaj-art-5a1569c9777546e9a3c6d0cf0fbbded12024-11-26T17:45:59ZengMDPI AGAnimals2076-26152024-11-011422326310.3390/ani14223263Single-Nucleus RNA Sequencing Reveals the Transcriptome Profiling of Ovarian Cells in Adolescent <i>Cyprinus carpio</i>Mingxi Hou0Jin Zhang1Qi Wang2Ran Zhao3Yiming Cao4Yingjie Chen5Kaikuo Wang6Ning Ding7Yingjie Qi8Xiaoqing Sun9Yan Zhang10Jiongtang Li11Key Laboratory of Aquatic Genomics, Ministry of Agriculture and Rural Affairs, Beijing Key Laboratory of Fishery Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, ChinaKey Laboratory of Aquatic Genomics, Ministry of Agriculture and Rural Affairs, Beijing Key Laboratory of Fishery Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, ChinaKey Laboratory of Aquatic Genomics, Ministry of Agriculture and Rural Affairs, Beijing Key Laboratory of Fishery Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, ChinaKey Laboratory of Aquatic Genomics, Ministry of Agriculture and Rural Affairs, Beijing Key Laboratory of Fishery Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, ChinaKey Laboratory of Aquatic Genomics, Ministry of Agriculture and Rural Affairs, Beijing Key Laboratory of Fishery Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, ChinaNational Demonstration Center for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai 201306, ChinaNational Demonstration Center for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai 201306, ChinaKey Laboratory of Aquatic Genomics, Ministry of Agriculture and Rural Affairs, Beijing Key Laboratory of Fishery Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, ChinaNational Demonstration Center for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai 201306, ChinaKey Laboratory of Aquatic Genomics, Ministry of Agriculture and Rural Affairs, Beijing Key Laboratory of Fishery Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, ChinaKey Laboratory of Aquatic Genomics, Ministry of Agriculture and Rural Affairs, Beijing Key Laboratory of Fishery Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, ChinaKey Laboratory of Aquatic Genomics, Ministry of Agriculture and Rural Affairs, Beijing Key Laboratory of Fishery Biotechnology, Chinese Academy of Fishery Sciences, Beijing 100141, ChinaThe common carp (<i>Cyprinus carpio</i>) is a crucial freshwater species cultivated worldwide for food consumption. Female carp have better growth performance than males, which fascinates scholars to uncover the mechanism of gonadal differentiation and produce mono-sex populations. However, the mechanism of ovarian development at single-cell resolution is limited. Here, we conducted single-nucleus RNA sequencing in adolescent common carp ovaries. Our study obtained transcriptional profiles of 13,155 nuclei and revealed 13 distinct cell clusters in the ovaries, including three subtypes of germ cells and four subtypes of granulosa cells. We subsequently performed pseudotime trajectory analysis to delineate potential mechanisms underlying the development of germ cells and granulosa cells. We identified 1250 dynamic expression genes in germ cells and 1815 in granulosa cells (<i>q</i>-value < 0.01), including <i>zp3</i>, <i>eif4a2</i> and <i>aspm</i> in germ cells and <i>fshr</i> and <i>esr1</i> in granulosa cells. The functional annotation showed that dynamic expression genes in germ cells were involved in sperm–egg recognition and some terms related to meiosis, such as sister chromatid segregation and homologous recombination. Genes expressed dynamically in granulosa cells were related to the TGF-β signaling pathway, response to gonadotropin, and development of primary female sexual characteristics. In addition, the dynamic genes expressed in granulosa cells might relate to the complex communication between different cell types. In summary, our study provided a transcriptome profile of common carp ovaries at single-nucleus resolution, and we further revealed the potential cell type-specific mechanisms underlying oogenesis and the differentiation of granulosa cells, which will facilitate breeding all-female common carp populations.https://www.mdpi.com/2076-2615/14/22/3263common carpsingle-nucleus sequencinggene expressionoogenesisgranulosa cell
spellingShingle Mingxi Hou
Jin Zhang
Qi Wang
Ran Zhao
Yiming Cao
Yingjie Chen
Kaikuo Wang
Ning Ding
Yingjie Qi
Xiaoqing Sun
Yan Zhang
Jiongtang Li
Single-Nucleus RNA Sequencing Reveals the Transcriptome Profiling of Ovarian Cells in Adolescent <i>Cyprinus carpio</i>
Animals
common carp
single-nucleus sequencing
gene expression
oogenesis
granulosa cell
title Single-Nucleus RNA Sequencing Reveals the Transcriptome Profiling of Ovarian Cells in Adolescent <i>Cyprinus carpio</i>
title_full Single-Nucleus RNA Sequencing Reveals the Transcriptome Profiling of Ovarian Cells in Adolescent <i>Cyprinus carpio</i>
title_fullStr Single-Nucleus RNA Sequencing Reveals the Transcriptome Profiling of Ovarian Cells in Adolescent <i>Cyprinus carpio</i>
title_full_unstemmed Single-Nucleus RNA Sequencing Reveals the Transcriptome Profiling of Ovarian Cells in Adolescent <i>Cyprinus carpio</i>
title_short Single-Nucleus RNA Sequencing Reveals the Transcriptome Profiling of Ovarian Cells in Adolescent <i>Cyprinus carpio</i>
title_sort single nucleus rna sequencing reveals the transcriptome profiling of ovarian cells in adolescent i cyprinus carpio i
topic common carp
single-nucleus sequencing
gene expression
oogenesis
granulosa cell
url https://www.mdpi.com/2076-2615/14/22/3263
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