Transcriptome Profiling Insights the Feature of Sex Reversal Induced by High Temperature in Tongue Sole Cynoglossus semilaevis

Sex reversal induced by temperature change is a common feature in fish. Usually, the sex ratio shift occurs when temperature deviates too much from normal during embryogenesis or sex differentiation stages. Despite decades of work, the mechanism of how temperature functions during early development...

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Main Authors: Jinxiang Liu, Xiaobing Liu, Chaofan Jin, Xinxin Du, Yan He, Quanqi Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-05-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fgene.2019.00522/full
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spelling doaj-88f247cd1db4451ba1ef4cf97c5462a12020-11-25T01:37:17ZengFrontiers Media S.A.Frontiers in Genetics1664-80212019-05-011010.3389/fgene.2019.00522437067Transcriptome Profiling Insights the Feature of Sex Reversal Induced by High Temperature in Tongue Sole Cynoglossus semilaevisJinxiang Liu0Jinxiang Liu1Xiaobing Liu2Chaofan Jin3Xinxin Du4Yan He5Yan He6Quanqi Zhang7Quanqi Zhang8Key Laboratory of Marine Genetics and Breeding, Ministry of Education, Ocean University of China, Qingdao, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaKey Laboratory of Marine Genetics and Breeding, Ministry of Education, Ocean University of China, Qingdao, ChinaKey Laboratory of Marine Genetics and Breeding, Ministry of Education, Ocean University of China, Qingdao, ChinaKey Laboratory of Marine Genetics and Breeding, Ministry of Education, Ocean University of China, Qingdao, ChinaKey Laboratory of Marine Genetics and Breeding, Ministry of Education, Ocean University of China, Qingdao, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaKey Laboratory of Marine Genetics and Breeding, Ministry of Education, Ocean University of China, Qingdao, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaSex reversal induced by temperature change is a common feature in fish. Usually, the sex ratio shift occurs when temperature deviates too much from normal during embryogenesis or sex differentiation stages. Despite decades of work, the mechanism of how temperature functions during early development and sex reversal remains mysterious. In this study, we used Chinese tongue sole as a model to identify features from gonad transcriptomic and epigenetic mechanisms involved in temperature induced masculinization. Some of genetic females reversed to pseudomales after high temperature treatment which caused the sex ratio imbalance. RNA-seq data showed that the expression profiles of females and males were significantly different, and set of genes showed sexually dimorphic expression. The general transcriptomic feature of pesudomales was similar with males, but the genes involved in spermatogenesis and energy metabolism were differentially expressed. In gonads, the methylation level of cyp19a1a promoter was higher in females than in males and pseudomales. Furthermore, high-temperature treatment increased the cyp19a1a promoter methylation levels of females. We observed a significant negative correlation between methylation levels and expression of cyp19ala. In vitro study showed that CpG within the cAMP response element (CRE) of the cyp19a1a promoter was hypermethylated, and DNA methylation decreased the basal and forskolin-induced activities of cyp19a1a promoter. These results suggested that epigenetic change, i.e., DNA methylation, which regulate the expression of cyp19a1a might be the mechanism for the temperature induced masculinization in tongue sole. It may be a common mechanism in teleost that can be induced sex reversal by temperature.https://www.frontiersin.org/article/10.3389/fgene.2019.00522/fullhigh-temperature treatmentRNA-seqcyp19a1aDNA methylationCynoglossus semilaevis
collection DOAJ
language English
format Article
sources DOAJ
author Jinxiang Liu
Jinxiang Liu
Xiaobing Liu
Chaofan Jin
Xinxin Du
Yan He
Yan He
Quanqi Zhang
Quanqi Zhang
spellingShingle Jinxiang Liu
Jinxiang Liu
Xiaobing Liu
Chaofan Jin
Xinxin Du
Yan He
Yan He
Quanqi Zhang
Quanqi Zhang
Transcriptome Profiling Insights the Feature of Sex Reversal Induced by High Temperature in Tongue Sole Cynoglossus semilaevis
Frontiers in Genetics
high-temperature treatment
RNA-seq
cyp19a1a
DNA methylation
Cynoglossus semilaevis
author_facet Jinxiang Liu
Jinxiang Liu
Xiaobing Liu
Chaofan Jin
Xinxin Du
Yan He
Yan He
Quanqi Zhang
Quanqi Zhang
author_sort Jinxiang Liu
title Transcriptome Profiling Insights the Feature of Sex Reversal Induced by High Temperature in Tongue Sole Cynoglossus semilaevis
title_short Transcriptome Profiling Insights the Feature of Sex Reversal Induced by High Temperature in Tongue Sole Cynoglossus semilaevis
title_full Transcriptome Profiling Insights the Feature of Sex Reversal Induced by High Temperature in Tongue Sole Cynoglossus semilaevis
title_fullStr Transcriptome Profiling Insights the Feature of Sex Reversal Induced by High Temperature in Tongue Sole Cynoglossus semilaevis
title_full_unstemmed Transcriptome Profiling Insights the Feature of Sex Reversal Induced by High Temperature in Tongue Sole Cynoglossus semilaevis
title_sort transcriptome profiling insights the feature of sex reversal induced by high temperature in tongue sole cynoglossus semilaevis
publisher Frontiers Media S.A.
series Frontiers in Genetics
issn 1664-8021
publishDate 2019-05-01
description Sex reversal induced by temperature change is a common feature in fish. Usually, the sex ratio shift occurs when temperature deviates too much from normal during embryogenesis or sex differentiation stages. Despite decades of work, the mechanism of how temperature functions during early development and sex reversal remains mysterious. In this study, we used Chinese tongue sole as a model to identify features from gonad transcriptomic and epigenetic mechanisms involved in temperature induced masculinization. Some of genetic females reversed to pseudomales after high temperature treatment which caused the sex ratio imbalance. RNA-seq data showed that the expression profiles of females and males were significantly different, and set of genes showed sexually dimorphic expression. The general transcriptomic feature of pesudomales was similar with males, but the genes involved in spermatogenesis and energy metabolism were differentially expressed. In gonads, the methylation level of cyp19a1a promoter was higher in females than in males and pseudomales. Furthermore, high-temperature treatment increased the cyp19a1a promoter methylation levels of females. We observed a significant negative correlation between methylation levels and expression of cyp19ala. In vitro study showed that CpG within the cAMP response element (CRE) of the cyp19a1a promoter was hypermethylated, and DNA methylation decreased the basal and forskolin-induced activities of cyp19a1a promoter. These results suggested that epigenetic change, i.e., DNA methylation, which regulate the expression of cyp19a1a might be the mechanism for the temperature induced masculinization in tongue sole. It may be a common mechanism in teleost that can be induced sex reversal by temperature.
topic high-temperature treatment
RNA-seq
cyp19a1a
DNA methylation
Cynoglossus semilaevis
url https://www.frontiersin.org/article/10.3389/fgene.2019.00522/full
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