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Background <p>Sexual growth dimorphism is a unique trait of the Chinese tongue sole (<i>Cynoglossus semilaevis</i>) where female fish grow much faster and bigger than their male counterparts. In tongue sole, the transcription factor <i>dmrt1</i> is essential for testis formation and germ cell maintenance, but its disruption not only causes sterility but also leads to enhanced somatic growth in males.</p> Results <p>To study how <i>dmrt1</i> links reproduction and growth, homozygous <i>dmrt1</i>-knockout males were treated with LNP-<i>dmrt1</i>, which carries <i>dmrt1</i> mRNA inside. After several weeks of repeated injections, histological examination revealed some recovery of spermatogenesis, while some seminiferous tubules contained developing sperms. The transcriptome across the brain, blood, and gonad showed that the <i>dmrt1</i> knock out changed steroidogenesis, meiosis, and hormone signaling, but LNP-<i>dmrt1</i> treatment turned on many pathways involved in extracellular matrix interaction and steroid biosynthesis. Using circRNA, miRNA, and mRNA expression data together we built a ceRNA network, showing a couple of main controllers linked to cell cycle and neural signaling.</p> Conclusions <p>Our results show that although LNP-mediated dmrt1 mRNA delivery was able to partially rebuild testicular structure and reactivate some key pathways related to steroid synthesis and tissue organization, full recovery of normal spermatogenesis was not achieved. The involvement of circRNA–miRNA–mRNA regulatory networks further suggesting that post-transcriptional regulation may be involved in the limited rescue effect, rather than dmrt1 acting alone. These findings deepen our understanding of how reproductive capacity and growth are coordinated in sexually dimorphic fish and provide a potential foundation for developing more effective strategies to improve fertility and breeding efficiency in tongue sole aquaculture.</p>

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Multi-omic dissection of dmrt1-dependent regulatory networks reveals brain–blood-gonad crosstalk and ceRNA-mediated reprogramming during fertility restoration in Cynoglossus semilaevis

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2026年3月19日

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  • Yuanri Hu,
  • Lanqing Ding,
  • Xu Yan,
  • Chaoyang Su,
  • Fangzhou Cheng,
  • He Jiang,
  • Xiaoyu Zhang,
  • Zhongkai Cui

摘要

Background

Sexual growth dimorphism is a unique trait of the Chinese tongue sole (Cynoglossus semilaevis) where female fish grow much faster and bigger than their male counterparts. In tongue sole, the transcription factor dmrt1 is essential for testis formation and germ cell maintenance, but its disruption not only causes sterility but also leads to enhanced somatic growth in males.

Results

To study how dmrt1 links reproduction and growth, homozygous dmrt1-knockout males were treated with LNP-dmrt1, which carries dmrt1 mRNA inside. After several weeks of repeated injections, histological examination revealed some recovery of spermatogenesis, while some seminiferous tubules contained developing sperms. The transcriptome across the brain, blood, and gonad showed that the dmrt1 knock out changed steroidogenesis, meiosis, and hormone signaling, but LNP-dmrt1 treatment turned on many pathways involved in extracellular matrix interaction and steroid biosynthesis. Using circRNA, miRNA, and mRNA expression data together we built a ceRNA network, showing a couple of main controllers linked to cell cycle and neural signaling.

Conclusions

Our results show that although LNP-mediated dmrt1 mRNA delivery was able to partially rebuild testicular structure and reactivate some key pathways related to steroid synthesis and tissue organization, full recovery of normal spermatogenesis was not achieved. The involvement of circRNA–miRNA–mRNA regulatory networks further suggesting that post-transcriptional regulation may be involved in the limited rescue effect, rather than dmrt1 acting alone. These findings deepen our understanding of how reproductive capacity and growth are coordinated in sexually dimorphic fish and provide a potential foundation for developing more effective strategies to improve fertility and breeding efficiency in tongue sole aquaculture.