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The ontogenic gonadal transcriptomes provide insights into sex change in the ricefield eel Monopterus albus

BACKGROUND: The ricefield eel is a freshwater protogynous hermaphrodite fish and has become an important aquaculture species in China. The sex change of ricefield eel is impeding its aquaculture practice, particularly the large-scale artificial breeding. Many studies including transcriptomes of mixe...

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Autores principales: Fan, Miao, Yang, Wei, Zhang, Weimin, Zhang, Lihong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10127409/
https://www.ncbi.nlm.nih.gov/pubmed/37170354
http://dx.doi.org/10.1186/s40850-022-00155-4
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author Fan, Miao
Yang, Wei
Zhang, Weimin
Zhang, Lihong
author_facet Fan, Miao
Yang, Wei
Zhang, Weimin
Zhang, Lihong
author_sort Fan, Miao
collection PubMed
description BACKGROUND: The ricefield eel is a freshwater protogynous hermaphrodite fish and has become an important aquaculture species in China. The sex change of ricefield eel is impeding its aquaculture practice, particularly the large-scale artificial breeding. Many studies including transcriptomes of mixed gonadal samples from different individuals have been aimed to elucidate mechanisms underlying the sex change. However, the key physiological factors involved in the initiation of sex change remain to be identified.  RESULTS: The present study performed transcriptomic analysis on gonadal samples of different sexual stages obtained through biopsy from the same fish undergoing sex change. A total of 539,764,816 high-quality reads were generated from twelve cDNA libraries of gonadal tissues at female (F), early intersexual (EI), mid-intersexual (MI), and late intersexual (LI) stages of three individual sex-changing fish. Pairwise comparisons between EI and F, MI and EI, and LI and MI identified 886, 319, and 10,767 differentially expressed genes (DEGs), respectively. Realtime quantitative PCR analysis of 12 representative DEGs showed similar expression profiles to those inferred from transcriptome data, suggesting the reliability of RNA-seq data for gene expression analysis. The expression of apoeb, csl2, and enpp2 was dramatically increased and peaked at EI while that of cyp19a1a, wnt4a, fgf16, and foxl2a significantly downregulated from F to EI and remained at very low levels during subsequent development until LI, which suggests that apoeb, csl2, enpp2, cyp19a1a, wnt4a, fgf16, and foxl2a may be closely associated with the initiation of sex change of ricefield eels. CONCLUSIONS: Collectively, results of the present study confirmed that the down-regulation of female-related genes, such as cyp19a1a, wnt4a, fgf16, and foxl2a, is important for the sex change of ricefield eels. More importantly, some novel genes, including apoeb, csl2, and enpp2, were shown to be expressed with peak values at EI, which are potentially involved in the initiation of sex change. The present transcriptomic data may provide an important research resource for further unraveling the mechanisms underlying the sex change and testicular development in ricefield eels as well as other teleosts. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40850-022-00155-4.
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spelling pubmed-101274092023-04-26 The ontogenic gonadal transcriptomes provide insights into sex change in the ricefield eel Monopterus albus Fan, Miao Yang, Wei Zhang, Weimin Zhang, Lihong BMC Zool Research BACKGROUND: The ricefield eel is a freshwater protogynous hermaphrodite fish and has become an important aquaculture species in China. The sex change of ricefield eel is impeding its aquaculture practice, particularly the large-scale artificial breeding. Many studies including transcriptomes of mixed gonadal samples from different individuals have been aimed to elucidate mechanisms underlying the sex change. However, the key physiological factors involved in the initiation of sex change remain to be identified.  RESULTS: The present study performed transcriptomic analysis on gonadal samples of different sexual stages obtained through biopsy from the same fish undergoing sex change. A total of 539,764,816 high-quality reads were generated from twelve cDNA libraries of gonadal tissues at female (F), early intersexual (EI), mid-intersexual (MI), and late intersexual (LI) stages of three individual sex-changing fish. Pairwise comparisons between EI and F, MI and EI, and LI and MI identified 886, 319, and 10,767 differentially expressed genes (DEGs), respectively. Realtime quantitative PCR analysis of 12 representative DEGs showed similar expression profiles to those inferred from transcriptome data, suggesting the reliability of RNA-seq data for gene expression analysis. The expression of apoeb, csl2, and enpp2 was dramatically increased and peaked at EI while that of cyp19a1a, wnt4a, fgf16, and foxl2a significantly downregulated from F to EI and remained at very low levels during subsequent development until LI, which suggests that apoeb, csl2, enpp2, cyp19a1a, wnt4a, fgf16, and foxl2a may be closely associated with the initiation of sex change of ricefield eels. CONCLUSIONS: Collectively, results of the present study confirmed that the down-regulation of female-related genes, such as cyp19a1a, wnt4a, fgf16, and foxl2a, is important for the sex change of ricefield eels. More importantly, some novel genes, including apoeb, csl2, and enpp2, were shown to be expressed with peak values at EI, which are potentially involved in the initiation of sex change. The present transcriptomic data may provide an important research resource for further unraveling the mechanisms underlying the sex change and testicular development in ricefield eels as well as other teleosts. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40850-022-00155-4. BioMed Central 2022-11-23 /pmc/articles/PMC10127409/ /pubmed/37170354 http://dx.doi.org/10.1186/s40850-022-00155-4 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Fan, Miao
Yang, Wei
Zhang, Weimin
Zhang, Lihong
The ontogenic gonadal transcriptomes provide insights into sex change in the ricefield eel Monopterus albus
title The ontogenic gonadal transcriptomes provide insights into sex change in the ricefield eel Monopterus albus
title_full The ontogenic gonadal transcriptomes provide insights into sex change in the ricefield eel Monopterus albus
title_fullStr The ontogenic gonadal transcriptomes provide insights into sex change in the ricefield eel Monopterus albus
title_full_unstemmed The ontogenic gonadal transcriptomes provide insights into sex change in the ricefield eel Monopterus albus
title_short The ontogenic gonadal transcriptomes provide insights into sex change in the ricefield eel Monopterus albus
title_sort ontogenic gonadal transcriptomes provide insights into sex change in the ricefield eel monopterus albus
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10127409/
https://www.ncbi.nlm.nih.gov/pubmed/37170354
http://dx.doi.org/10.1186/s40850-022-00155-4
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