Histological observations and transcriptome analyses reveal the dynamic changes in the gonads of the blotched snakehead (Channa maculata) during sex differentiation and gametogenesis.

IF 4.9 2区 医学 Q1 ENDOCRINOLOGY & METABOLISM Biology of Sex Differences Pub Date : 2024-09-07 DOI:10.1186/s13293-024-00643-x
Xiaotian Zhang, Yuxia Wu, Yang Zhang, Jin Zhang, Pengfei Chu, Kunci Chen, Haiyang Liu, Qing Luo, Shuzhan Fei, Jian Zhao, Mi Ou
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Abstract

Background: Blotched snakehead (Channa maculata) displays significant sexual dimorphism, with males exhibiting faster growth rates and larger body sizes compared to females. The cultivation of the all-male population of snakeheads holds substantial economic and ecological value. Nonetheless, the intricate processes governing the development of bipotential gonads into either testis or ovary in C. maculata remain inadequately elucidated. Therefore, it is necessary to determine the critical time window of sex differentiation in C. maculata, providing a theoretical basis for sex control in production practices.

Methods: The body length and weight of male and female C. maculata were measured at different developmental stages to reveal when sexual dimorphism in growth initially appears. Histological observations and spatiotemporal comparative transcriptome analyses were performed on ovaries and testes across various developmental stages to determine the crucial time windows for sex differentiation in each sex and the sex-related genes. Additionally, qPCR and MG2C were utilized to validate and locate sex-related genes, and levels of E2 and T were quantified to understand sex steroid synthesis.

Results: Sexual dimorphism in growth became evident starting from 90 dpf. Histological observations revealed that morphological sex differentiation in females and males occurred between 20 and 25 dpf or earlier and 30-35 dpf or earlier, respectively, corresponding to the appearance of the ovarian cavity or efferent duct anlage. Transcriptome analyses revealed divergent gene expression patterns in testes and ovaries after 30 dpf. The periods of 40-60 dpf and 60-90 dpf marked the initiation of molecular sex differentiation in females and males, respectively. Male-biased genes (Sox11a, Dmrt1, Amh, Amhr2, Gsdf, Ar, Cyp17a2) likely play crucial roles in male sex differentiation and spermatogenesis, while female-biased genes (Foxl2, Cyp19a1a, Bmp15, Figla, Er) could be pivotal in ovarian differentiation and development. Numerous biological pathways linked to sex differentiation and gametogenesis were also identified. Additionally, E2 and T exhibited sexual dimorphism during sex differentiation and gonadal development. Based on these results, it is hypothesized that in C. maculata, the potential male sex differentiation pathway, Sox11a-Dmrt1-Sox9b, activates downstream sex-related genes (Amh, Amhr2, Gsdf, Ar, Cyp17a2) for testicular development, while the antagonistic pathway, Foxl2/Cyp19a1a, activates downstream sex-related genes (Bmp15, Figla, Er) for ovarian development.

Conclusions: This study provides a comprehensive overview of gonadal dynamic changes during sex differentiation and gametogenesis in C. maculata, establishing a scientific foundation for sex control in this species.

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组织学观察和转录组分析揭示了斑点乌鳢性腺在性别分化和配子发生过程中的动态变化。
背景:斑点乌鳢(Channa maculata)表现出明显的性二型,雄性比雌性生长速度更快、体型更大。培育全雄性乌鳢种群具有重要的经济和生态价值。然而,有关乌鳢双性腺发育成睾丸或卵巢的复杂过程仍未得到充分阐明。因此,有必要确定巨蜥性别分化的关键时间窗口,为生产实践中的性别控制提供理论依据:方法:在不同的发育阶段测量雌雄大菱鲆的体长和体重,以揭示生长中的性别二形性最初出现的时间。对不同发育阶段的卵巢和睾丸进行组织学观察和时空比较转录组分析,以确定每种性别性别分化的关键时间窗口和性别相关基因。此外,还利用 qPCR 和 MG2C 验证和定位性别相关基因,并量化 E2 和 T 的水平,以了解性类固醇的合成:结果:从90 dpf开始,生长的性别二态性开始明显。组织学观察显示,雌性和雄性的形态性别分化分别发生在20-25 dpf或更早和30-35 dpf或更早,与卵巢腔或传出导管肛门的出现相对应。转录组分析显示,睾丸和卵巢的基因表达模式在30 dpf之后出现了差异。40-60 dpf和60-90 dpf时期分别标志着雌性和雄性分子性别分化的开始。偏雄性的基因(Sox11a、Dmrt1、Amh、Amhr2、Gsdf、Ar、Cyp17a2)可能在雄性性别分化和精子发生中起着关键作用,而偏雌性的基因(Foxl2、Cyp19a1a、Bmp15、Figla、Er)可能在卵巢分化和发育中起着关键作用。还发现了许多与性别分化和配子发生相关的生物通路。此外,E2和T在性分化和性腺发育过程中表现出性二态性。基于这些结果,我们推测,在C.maculata中,潜在的雄性性分化途径Sox11a-Dmrt1-Sox9b会激活睾丸发育的下游性相关基因(Amh、Amhr2、Gsdf、Ar、Cyp17a2),而拮抗途径Foxl2/Cyp19a1a则会激活卵巢发育的下游性相关基因(Bmp15、Figla、Er):本研究全面概述了巨蜥性分化和配子发生过程中性腺的动态变化,为该物种的性别控制奠定了科学基础。
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来源期刊
Biology of Sex Differences
Biology of Sex Differences ENDOCRINOLOGY & METABOLISM-GENETICS & HEREDITY
CiteScore
12.10
自引率
1.30%
发文量
69
审稿时长
14 weeks
期刊介绍: Biology of Sex Differences is a unique scientific journal focusing on sex differences in physiology, behavior, and disease from molecular to phenotypic levels, incorporating both basic and clinical research. The journal aims to enhance understanding of basic principles and facilitate the development of therapeutic and diagnostic tools specific to sex differences. As an open-access journal, it is the official publication of the Organization for the Study of Sex Differences and co-published by the Society for Women's Health Research. Topical areas include, but are not limited to sex differences in: genomics; the microbiome; epigenetics; molecular and cell biology; tissue biology; physiology; interaction of tissue systems, in any system including adipose, behavioral, cardiovascular, immune, muscular, neural, renal, and skeletal; clinical studies bearing on sex differences in disease or response to therapy.
期刊最新文献
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