The Role of the Heat Shock Cognate Protein 70 Genes in Sex Determination and Differentiation of Chinese Tongue Sole (<i>Cynoglossus semilaevis</i>)

Fish sex determination can be affected by environmental temperature. This process relies on temperature-sensitive proteins such as heat shock proteins (HSPs). Our previous work found that heat shock cognate proteins (HSCs) may participate in high-temperature associated sex reversal of Chinese tongue...

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Main Authors: Qian Liu, Yue Wang, Leilei Tan, Wenxiu Ma, Xiaona Zhao, Changwei Shao, Qian Wang
Format: Article
Language:English
Published: MDPI AG 2023-02-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/4/3761
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author Qian Liu
Yue Wang
Leilei Tan
Wenxiu Ma
Xiaona Zhao
Changwei Shao
Qian Wang
author_facet Qian Liu
Yue Wang
Leilei Tan
Wenxiu Ma
Xiaona Zhao
Changwei Shao
Qian Wang
author_sort Qian Liu
collection DOAJ
description Fish sex determination can be affected by environmental temperature. This process relies on temperature-sensitive proteins such as heat shock proteins (HSPs). Our previous work found that heat shock cognate proteins (HSCs) may participate in high-temperature associated sex reversal of Chinese tongue sole (<i>Cynoglossus semilaevis</i>). However, the role of <i>hsc</i> genes in responding to high temperature and affecting sex determination/differentiation remains unclear. Here, by using <i>C. semilaevis</i> as model, we identified <i>hsc70</i> and <i>hsc70-like</i>. <i>hsc70</i> was abundant in the gonads with a testicular-higher expression at all gonadal development stages except for 6 months post fertilization (mpf). Intriguingly, <i>hsc70-like</i> showed higher expression in testes from 6 mpf on. Both long-term heat treatment during the temperature-sensitive sex-determining period and short-term heat stress at the end of this period caused different expression of <i>hsc70</i>/<i>hsc70-like</i> between sexes. The dual-luciferase assay results also suggested that these genes can respond to high temperature rapidly <i>in vitro</i>. Heat treatment of <i>C. semilaevis</i> testis cells overexpressed with <i>hsc70</i>/<i>hsc70-like</i> could affect the expression of sex-related genes <i>sox9a</i> and <i>cyp19a1a</i>. Our results indicated that <i>hsc70</i> and <i>hsc70-like</i> were key regulators linking external high-temperature signals with sex differentiation <i>in vivo</i> and provide a new idea for understanding the mechanism by which high temperature affects sex determination/differentiation in teleosts.
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spelling doaj.art-1ab7ebd9f6e54a6a9f2acea82e8e74f42023-11-16T21:04:36ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-02-01244376110.3390/ijms24043761The Role of the Heat Shock Cognate Protein 70 Genes in Sex Determination and Differentiation of Chinese Tongue Sole (<i>Cynoglossus semilaevis</i>)Qian Liu0Yue Wang1Leilei Tan2Wenxiu Ma3Xiaona Zhao4Changwei Shao5Qian Wang6College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, ChinaNational Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Re-search Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaNational Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Re-search Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaNational Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Re-search Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaNational Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Re-search Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaNational Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Re-search Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaNational Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Re-search Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, ChinaFish sex determination can be affected by environmental temperature. This process relies on temperature-sensitive proteins such as heat shock proteins (HSPs). Our previous work found that heat shock cognate proteins (HSCs) may participate in high-temperature associated sex reversal of Chinese tongue sole (<i>Cynoglossus semilaevis</i>). However, the role of <i>hsc</i> genes in responding to high temperature and affecting sex determination/differentiation remains unclear. Here, by using <i>C. semilaevis</i> as model, we identified <i>hsc70</i> and <i>hsc70-like</i>. <i>hsc70</i> was abundant in the gonads with a testicular-higher expression at all gonadal development stages except for 6 months post fertilization (mpf). Intriguingly, <i>hsc70-like</i> showed higher expression in testes from 6 mpf on. Both long-term heat treatment during the temperature-sensitive sex-determining period and short-term heat stress at the end of this period caused different expression of <i>hsc70</i>/<i>hsc70-like</i> between sexes. The dual-luciferase assay results also suggested that these genes can respond to high temperature rapidly <i>in vitro</i>. Heat treatment of <i>C. semilaevis</i> testis cells overexpressed with <i>hsc70</i>/<i>hsc70-like</i> could affect the expression of sex-related genes <i>sox9a</i> and <i>cyp19a1a</i>. Our results indicated that <i>hsc70</i> and <i>hsc70-like</i> were key regulators linking external high-temperature signals with sex differentiation <i>in vivo</i> and provide a new idea for understanding the mechanism by which high temperature affects sex determination/differentiation in teleosts.https://www.mdpi.com/1422-0067/24/4/3761<i>hsc70</i> geneshigh temperaturesex determination and differentiation<i>Cynoglossus semilaevis</i>
spellingShingle Qian Liu
Yue Wang
Leilei Tan
Wenxiu Ma
Xiaona Zhao
Changwei Shao
Qian Wang
The Role of the Heat Shock Cognate Protein 70 Genes in Sex Determination and Differentiation of Chinese Tongue Sole (<i>Cynoglossus semilaevis</i>)
International Journal of Molecular Sciences
<i>hsc70</i> genes
high temperature
sex determination and differentiation
<i>Cynoglossus semilaevis</i>
title The Role of the Heat Shock Cognate Protein 70 Genes in Sex Determination and Differentiation of Chinese Tongue Sole (<i>Cynoglossus semilaevis</i>)
title_full The Role of the Heat Shock Cognate Protein 70 Genes in Sex Determination and Differentiation of Chinese Tongue Sole (<i>Cynoglossus semilaevis</i>)
title_fullStr The Role of the Heat Shock Cognate Protein 70 Genes in Sex Determination and Differentiation of Chinese Tongue Sole (<i>Cynoglossus semilaevis</i>)
title_full_unstemmed The Role of the Heat Shock Cognate Protein 70 Genes in Sex Determination and Differentiation of Chinese Tongue Sole (<i>Cynoglossus semilaevis</i>)
title_short The Role of the Heat Shock Cognate Protein 70 Genes in Sex Determination and Differentiation of Chinese Tongue Sole (<i>Cynoglossus semilaevis</i>)
title_sort role of the heat shock cognate protein 70 genes in sex determination and differentiation of chinese tongue sole i cynoglossus semilaevis i
topic <i>hsc70</i> genes
high temperature
sex determination and differentiation
<i>Cynoglossus semilaevis</i>
url https://www.mdpi.com/1422-0067/24/4/3761
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