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<p>Although the eyestalk-androgenic gland-testis axis (ES-AG-TS axis) has been acknowledged as the core neuro-endocrine regulatory system for sex differentiation and gonad development in decapod crustaceans, the molecular regulatory networks underlying the ES-AG-TS axis remains unclear. In this study, we performed multi-tissue comparative transcriptomic analysis at different testis developmental stages of the giant freshwater prawn <i>Macrobrachium rosenbergii</i>. 116,892 unigenes were obtained from 27 sequencing libraries. Differential gene expression (DEG) analysis identified 7,126 to 27,532 DEGs across the eyestalk ganglia, androgenic gland and testis tissues at different stages. Functional enrichment analysis revealed that in the eyestalk ganglia, gonad inhibitory genes such as <i>GIH</i> were significantly down-regulated, while glucose metabolism-related pathways were markedly activated. The androgenic gland exhibited distinct regulation characteristics, with steroid hormone biosynthesis pathways showing progressive activation at later stages. In the testis tissue, metabolic patterns shifted from predominant oxidation-reduction process to protein phosphorylation. Further inter-tissue comparisons identified 19,652 and 37,075 DEGs in the comparisons of ES-vs-AG and AG-vs-TS, respectively. Based on the results of DEG analysis and functional enrichment, we propose that the calcium signaling-WNT/β-catenin pathway regulates male differentiation through the<i> Sox9</i>-<i>Dmrt</i>-<i>IAG</i> cascade, while the p53-MMPs-TNFα axis mediates testis development. In summary, this study demonstrates that eyestalk ablation triggers reprogramming of glucose metabolism in the eyestalk ganglia, activates the androgenic gland steroid synthesis pathway, and facilitates the timing transition of testis metabolism. These findings enhance our understanding of the ES-AG-TS regulatory axis and provide novel potential targets for sex manipulation in crustacean aquaculture.</p>

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Uncovering the Eyestalk-Androgenic Gland-Testis Regulatory Axis Underlying Male Sexual Development of the Giant Freshwater Prawn Macrobrachium Rosenbergii: Insights from Multi-Tissue Comparative Transcriptomics Analysis

  • 期刊论文

  • 发表日期：

    2026年1月27日

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  • Chunmei Ao,
  • Yiguo Lei,
  • Boquan Wan,
  • Wei Wang

摘要

Although the eyestalk-androgenic gland-testis axis (ES-AG-TS axis) has been acknowledged as the core neuro-endocrine regulatory system for sex differentiation and gonad development in decapod crustaceans, the molecular regulatory networks underlying the ES-AG-TS axis remains unclear. In this study, we performed multi-tissue comparative transcriptomic analysis at different testis developmental stages of the giant freshwater prawn Macrobrachium rosenbergii. 116,892 unigenes were obtained from 27 sequencing libraries. Differential gene expression (DEG) analysis identified 7,126 to 27,532 DEGs across the eyestalk ganglia, androgenic gland and testis tissues at different stages. Functional enrichment analysis revealed that in the eyestalk ganglia, gonad inhibitory genes such as GIH were significantly down-regulated, while glucose metabolism-related pathways were markedly activated. The androgenic gland exhibited distinct regulation characteristics, with steroid hormone biosynthesis pathways showing progressive activation at later stages. In the testis tissue, metabolic patterns shifted from predominant oxidation-reduction process to protein phosphorylation. Further inter-tissue comparisons identified 19,652 and 37,075 DEGs in the comparisons of ES-vs-AG and AG-vs-TS, respectively. Based on the results of DEG analysis and functional enrichment, we propose that the calcium signaling-WNT/β-catenin pathway regulates male differentiation through the Sox9-Dmrt-IAG cascade, while the p53-MMPs-TNFα axis mediates testis development. In summary, this study demonstrates that eyestalk ablation triggers reprogramming of glucose metabolism in the eyestalk ganglia, activates the androgenic gland steroid synthesis pathway, and facilitates the timing transition of testis metabolism. These findings enhance our understanding of the ES-AG-TS regulatory axis and provide novel potential targets for sex manipulation in crustacean aquaculture.