Integration of Transcriptome and Methylome Highlights the Roles of Cell Cycle and Hippo Signaling Pathway in Flatfish Sexual Size Dimorphism

Sexual size dimorphism (SSD) is the difference in segments or body size between sexes prevalent in various species. Understanding the genetic architecture of SSD has remained a significant challenge owing to the complexity of growth mechanisms and the sexual influences among species. The Chinese ton...

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Autores principales:	Na Wang, Qian Yang, Jialin Wang, Rui Shi, Ming Li, Jin Gao, Wenteng Xu, Yingming Yang, Yadong Chen, Songlin Chen
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	cell cycle Chinese tongue sole (Cynoglossus semilaevis) hippo signaling pathway methylome sexual size dimorphism transcriptome Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/f7a9d8625b2d4555a9edbee8154420b4
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spelling	oai:doaj.org-article:f7a9d8625b2d4555a9edbee8154420b42021-12-02T11:26:19ZIntegration of Transcriptome and Methylome Highlights the Roles of Cell Cycle and Hippo Signaling Pathway in Flatfish Sexual Size Dimorphism2296-634X10.3389/fcell.2021.743722https://doaj.org/article/f7a9d8625b2d4555a9edbee8154420b42021-12-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fcell.2021.743722/fullhttps://doaj.org/toc/2296-634XSexual size dimorphism (SSD) is the difference in segments or body size between sexes prevalent in various species. Understanding the genetic architecture of SSD has remained a significant challenge owing to the complexity of growth mechanisms and the sexual influences among species. The Chinese tongue sole (Cynoglossus semilaevis), which exhibits a female-biased SSD and sex reversal from female to pseudomale, is an ideal model for exploring SSD mechanism at the molecular level. The present study aimed to integrate transcriptome and methylome analysis to unravel the genetic and epigenetic changes in female, male, and pseudomale C. semilaevis. The somatotropic and reproductive tissues (brain, liver, gonad, and muscle) transcriptomes were characterized by RNA-seq technology. Transcriptomic analysis unravelled numerous differentially expressed genes (DEGs) involved in cell growth and death-related pathways. The gonad and muscle methylomes were further employed for screening differentially methylated genes (DMGs). Relatively higher DNA methylation levels were observed in the male and pseudomale individuals. In detail, hypermethylation of the chromosome W was pronounced in the pseudomale group than in the female group. Furthermore, weighted gene co-expression network analysis showed that turquoise and brown modules positively and negatively correlated with the female-biased SSD, respectively. A combined analysis of the module genes and DMGs revealed the female-biased mRNA transcripts and hypomethylated levels in the upstream and downstream regions across the cell cycle-related genes. Moreover, the male and pseudomale-biased gene expression in the hippo signaling pathway were positively correlated with their hypermethylation levels in the gene body. These findings implied that the activation of the cell cycle and the inhibition of the hippo signaling pathway were implicated in C. semilaevis female-biased SSD. In addition, the dynamic expression pattern of the epigenetic regulatory factors, including dnmt1, dnmt3a, dnmt3b, and uhrf1, among the different sexes correspond with their distinct DNA methylation levels. Herein, we provide valuable clues for understanding female-biased SSD in C. semilaevis.Na WangNa WangNa WangQian YangQian YangJialin WangJialin WangRui ShiRui ShiMing LiMing LiJin GaoWenteng XuWenteng XuWenteng XuYingming YangYingming YangYingming YangYadong ChenYadong ChenYadong ChenSonglin ChenSonglin ChenSonglin ChenFrontiers Media S.A.articlecell cycleChinese tongue sole (Cynoglossus semilaevis)hippo signaling pathwaymethylomesexual size dimorphismtranscriptomeBiology (General)QH301-705.5ENFrontiers in Cell and Developmental Biology, Vol 9 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	cell cycle Chinese tongue sole (Cynoglossus semilaevis) hippo signaling pathway methylome sexual size dimorphism transcriptome Biology (General) QH301-705.5
spellingShingle	cell cycle Chinese tongue sole (Cynoglossus semilaevis) hippo signaling pathway methylome sexual size dimorphism transcriptome Biology (General) QH301-705.5 Na Wang Na Wang Na Wang Qian Yang Qian Yang Jialin Wang Jialin Wang Rui Shi Rui Shi Ming Li Ming Li Jin Gao Wenteng Xu Wenteng Xu Wenteng Xu Yingming Yang Yingming Yang Yingming Yang Yadong Chen Yadong Chen Yadong Chen Songlin Chen Songlin Chen Songlin Chen Integration of Transcriptome and Methylome Highlights the Roles of Cell Cycle and Hippo Signaling Pathway in Flatfish Sexual Size Dimorphism
description	Sexual size dimorphism (SSD) is the difference in segments or body size between sexes prevalent in various species. Understanding the genetic architecture of SSD has remained a significant challenge owing to the complexity of growth mechanisms and the sexual influences among species. The Chinese tongue sole (Cynoglossus semilaevis), which exhibits a female-biased SSD and sex reversal from female to pseudomale, is an ideal model for exploring SSD mechanism at the molecular level. The present study aimed to integrate transcriptome and methylome analysis to unravel the genetic and epigenetic changes in female, male, and pseudomale C. semilaevis. The somatotropic and reproductive tissues (brain, liver, gonad, and muscle) transcriptomes were characterized by RNA-seq technology. Transcriptomic analysis unravelled numerous differentially expressed genes (DEGs) involved in cell growth and death-related pathways. The gonad and muscle methylomes were further employed for screening differentially methylated genes (DMGs). Relatively higher DNA methylation levels were observed in the male and pseudomale individuals. In detail, hypermethylation of the chromosome W was pronounced in the pseudomale group than in the female group. Furthermore, weighted gene co-expression network analysis showed that turquoise and brown modules positively and negatively correlated with the female-biased SSD, respectively. A combined analysis of the module genes and DMGs revealed the female-biased mRNA transcripts and hypomethylated levels in the upstream and downstream regions across the cell cycle-related genes. Moreover, the male and pseudomale-biased gene expression in the hippo signaling pathway were positively correlated with their hypermethylation levels in the gene body. These findings implied that the activation of the cell cycle and the inhibition of the hippo signaling pathway were implicated in C. semilaevis female-biased SSD. In addition, the dynamic expression pattern of the epigenetic regulatory factors, including dnmt1, dnmt3a, dnmt3b, and uhrf1, among the different sexes correspond with their distinct DNA methylation levels. Herein, we provide valuable clues for understanding female-biased SSD in C. semilaevis.
format	article
author	Na Wang Na Wang Na Wang Qian Yang Qian Yang Jialin Wang Jialin Wang Rui Shi Rui Shi Ming Li Ming Li Jin Gao Wenteng Xu Wenteng Xu Wenteng Xu Yingming Yang Yingming Yang Yingming Yang Yadong Chen Yadong Chen Yadong Chen Songlin Chen Songlin Chen Songlin Chen
author_facet	Na Wang Na Wang Na Wang Qian Yang Qian Yang Jialin Wang Jialin Wang Rui Shi Rui Shi Ming Li Ming Li Jin Gao Wenteng Xu Wenteng Xu Wenteng Xu Yingming Yang Yingming Yang Yingming Yang Yadong Chen Yadong Chen Yadong Chen Songlin Chen Songlin Chen Songlin Chen
author_sort	Na Wang
title	Integration of Transcriptome and Methylome Highlights the Roles of Cell Cycle and Hippo Signaling Pathway in Flatfish Sexual Size Dimorphism
title_short	Integration of Transcriptome and Methylome Highlights the Roles of Cell Cycle and Hippo Signaling Pathway in Flatfish Sexual Size Dimorphism
title_full	Integration of Transcriptome and Methylome Highlights the Roles of Cell Cycle and Hippo Signaling Pathway in Flatfish Sexual Size Dimorphism
title_fullStr	Integration of Transcriptome and Methylome Highlights the Roles of Cell Cycle and Hippo Signaling Pathway in Flatfish Sexual Size Dimorphism
title_full_unstemmed	Integration of Transcriptome and Methylome Highlights the Roles of Cell Cycle and Hippo Signaling Pathway in Flatfish Sexual Size Dimorphism
title_sort	integration of transcriptome and methylome highlights the roles of cell cycle and hippo signaling pathway in flatfish sexual size dimorphism
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/f7a9d8625b2d4555a9edbee8154420b4
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Integration of Transcriptome and Methylome Highlights the Roles of Cell Cycle and Hippo Signaling Pathway in Flatfish Sexual Size Dimorphism

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