The Function of Heat Shock Transcription Factors in Sex Differentiation in <i>Cynoglossus semilaevis</i>

Chinese tongue sole (<i>Cynoglossus semilaevis</i>) is an important marine fish in China. It has sexual dimorphism. The weight and growth rate of female fish are much greater than those of male fish. However, high temperatures can induce sex reversal in genetic female fish (ZW) to phenot...

Full description

Saved in:
Bibliographic Details
Main Authors: Zhijie Li, Xuexue Sun, Haipeng Yan, Lijun Wang, Xihong Li, Na Wang, Min Wei, Wenteng Xu
Format: Article
Language:English
Published: MDPI AG 2025-05-01
Series:Animals
Subjects:
Online Access:https://www.mdpi.com/2076-2615/15/10/1443
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849327727959605248
author Zhijie Li
Xuexue Sun
Haipeng Yan
Lijun Wang
Xihong Li
Na Wang
Min Wei
Wenteng Xu
author_facet Zhijie Li
Xuexue Sun
Haipeng Yan
Lijun Wang
Xihong Li
Na Wang
Min Wei
Wenteng Xu
author_sort Zhijie Li
collection DOAJ
description Chinese tongue sole (<i>Cynoglossus semilaevis</i>) is an important marine fish in China. It has sexual dimorphism. The weight and growth rate of female fish are much greater than those of male fish. However, high temperatures can induce sex reversal in genetic female fish (ZW) to phenotypic male fish; thus, identifying the genetic elements involved in temperature perception will provide the molecular basis for sex control. The heat shock transcription factor (<i>hsf</i>) is known as an important component of temperature sensing and mediates the heat shock response in fish such as <i>Danio rerio</i>; however, its function in <i>C. semilaevis</i> is unclear. In this study, five <i>hsf</i> genes (<i>hsf1</i>, <i>hsf2</i>, <i>hsf4</i>, <i>hsf5a</i>, and <i>hsf5b</i>) were identified in tongue sole and found to be expressed in the gonads at different developmental stages, peaking from 7M to 1Y. Gonadal in situ hybridization revealed that <i>hsf</i> gene signals were mainly localized in germ cells, e.g., sperm in the testis and all-stage oocytes in the ovary. Upon high-temperature stimulation, the expression of the <i>hsf</i> gene in the gonads increased gradually with increasing stimulation time, but different <i>hsf</i> genes presented different response patterns. After the RNA interference of <i>hsf</i> in the testis and ovarian cell lines, a series of sex-related genes, such as <i>foxl2</i> and <i>dmrt1</i>, significantly changed. In vivo RNA interference had an effect on the female gonads and mainly affected <i>neurl3</i> expression. On the basis of these data, we speculate that <i>hsf</i> responds to temperature stimulation and plays an important role in sex differentiation. This study helps elucidate the relationship between temperature sensing and sex differentiation in <i>C. semilaevis</i>.
format Article
id doaj-art-66fe1c46abab4d5aa141336d5e1b66c8
institution Kabale University
issn 2076-2615
language English
publishDate 2025-05-01
publisher MDPI AG
record_format Article
series Animals
spelling doaj-art-66fe1c46abab4d5aa141336d5e1b66c82025-08-20T03:47:48ZengMDPI AGAnimals2076-26152025-05-011510144310.3390/ani15101443The Function of Heat Shock Transcription Factors in Sex Differentiation in <i>Cynoglossus semilaevis</i>Zhijie Li0Xuexue Sun1Haipeng Yan2Lijun Wang3Xihong Li4Na Wang5Min Wei6Wenteng Xu7School of Marine Science and Fisheries, Jiangsu Ocean University, Lianyungang 222005, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaSchool of Marine Science and Fisheries, Jiangsu Ocean University, Lianyungang 222005, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaChinese tongue sole (<i>Cynoglossus semilaevis</i>) is an important marine fish in China. It has sexual dimorphism. The weight and growth rate of female fish are much greater than those of male fish. However, high temperatures can induce sex reversal in genetic female fish (ZW) to phenotypic male fish; thus, identifying the genetic elements involved in temperature perception will provide the molecular basis for sex control. The heat shock transcription factor (<i>hsf</i>) is known as an important component of temperature sensing and mediates the heat shock response in fish such as <i>Danio rerio</i>; however, its function in <i>C. semilaevis</i> is unclear. In this study, five <i>hsf</i> genes (<i>hsf1</i>, <i>hsf2</i>, <i>hsf4</i>, <i>hsf5a</i>, and <i>hsf5b</i>) were identified in tongue sole and found to be expressed in the gonads at different developmental stages, peaking from 7M to 1Y. Gonadal in situ hybridization revealed that <i>hsf</i> gene signals were mainly localized in germ cells, e.g., sperm in the testis and all-stage oocytes in the ovary. Upon high-temperature stimulation, the expression of the <i>hsf</i> gene in the gonads increased gradually with increasing stimulation time, but different <i>hsf</i> genes presented different response patterns. After the RNA interference of <i>hsf</i> in the testis and ovarian cell lines, a series of sex-related genes, such as <i>foxl2</i> and <i>dmrt1</i>, significantly changed. In vivo RNA interference had an effect on the female gonads and mainly affected <i>neurl3</i> expression. On the basis of these data, we speculate that <i>hsf</i> responds to temperature stimulation and plays an important role in sex differentiation. This study helps elucidate the relationship between temperature sensing and sex differentiation in <i>C. semilaevis</i>.https://www.mdpi.com/2076-2615/15/10/1443Chinese tongue sole<i>hsf</i>sex differentiationexpression patternsiRNA knockdown
spellingShingle Zhijie Li
Xuexue Sun
Haipeng Yan
Lijun Wang
Xihong Li
Na Wang
Min Wei
Wenteng Xu
The Function of Heat Shock Transcription Factors in Sex Differentiation in <i>Cynoglossus semilaevis</i>
Animals
Chinese tongue sole
<i>hsf</i>
sex differentiation
expression pattern
siRNA knockdown
title The Function of Heat Shock Transcription Factors in Sex Differentiation in <i>Cynoglossus semilaevis</i>
title_full The Function of Heat Shock Transcription Factors in Sex Differentiation in <i>Cynoglossus semilaevis</i>
title_fullStr The Function of Heat Shock Transcription Factors in Sex Differentiation in <i>Cynoglossus semilaevis</i>
title_full_unstemmed The Function of Heat Shock Transcription Factors in Sex Differentiation in <i>Cynoglossus semilaevis</i>
title_short The Function of Heat Shock Transcription Factors in Sex Differentiation in <i>Cynoglossus semilaevis</i>
title_sort function of heat shock transcription factors in sex differentiation in i cynoglossus semilaevis i
topic Chinese tongue sole
<i>hsf</i>
sex differentiation
expression pattern
siRNA knockdown
url https://www.mdpi.com/2076-2615/15/10/1443
work_keys_str_mv AT zhijieli thefunctionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT xuexuesun thefunctionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT haipengyan thefunctionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT lijunwang thefunctionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT xihongli thefunctionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT nawang thefunctionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT minwei thefunctionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT wentengxu thefunctionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT zhijieli functionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT xuexuesun functionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT haipengyan functionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT lijunwang functionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT xihongli functionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT nawang functionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT minwei functionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi
AT wentengxu functionofheatshocktranscriptionfactorsinsexdifferentiationinicynoglossussemilaevisi