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Background <p>The evolutionary conservation of lipid storage mechanisms across metazoans is well illustrated by vertebrate white adipose tissue (WAT) and its functional counterpart, the amphibian fat body. While serving as the principal lipid reservoir, the amphibian fat body is connected to the gonads and demonstrates unique endocrine-reproductive integration, particularly through its bidirectional regulation of gonadal function and energy metabolism. However, our understanding of this organ’s cellular heterogeneity and sex-specific functional adaptations is still limited.</p> Results <p>In this study, we investigated the molecular mechanisms underlying the adipose tissue specialization in <i>Bufo gargarizans</i>, revealing sex- and depot-specific adaptations between visceral fat bodies and subcutaneous adipose tissue. Through comparative transcriptomics, we identified 1,201 visceral and 1,225 subcutaneous sex-biased differentially expressed genes (DEGs), with functional enrichment in calcium signaling pathway, MAPK signaling pathway, and vascular smooth muscle contraction. Subcutaneous depots exhibited calcium flux-driven lipogenesis regulation, where <i>CACNA1G</i> and <i>NCX1</i> orchestrated adipocytes differentiation via <i>PHKG1</i>-mediated phosphorylation and <i>NFATc1</i> nuclear translocation. In visceral fat bodies, sexually dimorphic metabolic strategies were prominent, females prioritized lipid storage through TCA cycle augmentation, while males upregulated Mucin-type O-glycan biosynthesis, suggesting a protective role against testicular oxidative stress. Regulatory divergence in subcutaneous adipose tissue extended to vascular dynamics, males enhanced <i>KLF2</i>-dependent angiogenesis via the Apelin pathway, whereas females activated <i>MYLK3</i>-mediated vascular permeability through tight junction remodeling.</p> Conclusions <p>Our study revealed the central role of calcium signaling in adipose tissue diversification in <i>B. gargarizans</i>, linking tissue-biased gene networks to evolutionary adaptations. We found subcutaneous fat depots prioritized calcium-mediated adipogenesis, while visceral fat diverged into female lipid storage versus male gonadal protection via Mucin O-glycans. Our work redefines amphibian adipose systems as vertebrate lipid metabolism models, uncovers evolutionarily conserved modules in vascular regulation and stress-induced glycosylation, and elucidates mechanisms bridging adaptive energy allocation in amphibians.</p>

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Transcriptomic profiling reveals tissue-specific and sex-dimorphic lipid storage in Bufo gargarizans

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2025年11月11日

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  • Yimin Zhang,
  • Xinyue Yang,
  • Tonghang Wang,
  • Ruinan Zhao,
  • Yanjun Zhu,
  • Yinmeng Hou,
  • Zhuo Chen,
  • Xiaohong Chen

摘要

Background

The evolutionary conservation of lipid storage mechanisms across metazoans is well illustrated by vertebrate white adipose tissue (WAT) and its functional counterpart, the amphibian fat body. While serving as the principal lipid reservoir, the amphibian fat body is connected to the gonads and demonstrates unique endocrine-reproductive integration, particularly through its bidirectional regulation of gonadal function and energy metabolism. However, our understanding of this organ’s cellular heterogeneity and sex-specific functional adaptations is still limited.

Results

In this study, we investigated the molecular mechanisms underlying the adipose tissue specialization in Bufo gargarizans, revealing sex- and depot-specific adaptations between visceral fat bodies and subcutaneous adipose tissue. Through comparative transcriptomics, we identified 1,201 visceral and 1,225 subcutaneous sex-biased differentially expressed genes (DEGs), with functional enrichment in calcium signaling pathway, MAPK signaling pathway, and vascular smooth muscle contraction. Subcutaneous depots exhibited calcium flux-driven lipogenesis regulation, where CACNA1G and NCX1 orchestrated adipocytes differentiation via PHKG1-mediated phosphorylation and NFATc1 nuclear translocation. In visceral fat bodies, sexually dimorphic metabolic strategies were prominent, females prioritized lipid storage through TCA cycle augmentation, while males upregulated Mucin-type O-glycan biosynthesis, suggesting a protective role against testicular oxidative stress. Regulatory divergence in subcutaneous adipose tissue extended to vascular dynamics, males enhanced KLF2-dependent angiogenesis via the Apelin pathway, whereas females activated MYLK3-mediated vascular permeability through tight junction remodeling.

Conclusions

Our study revealed the central role of calcium signaling in adipose tissue diversification in B. gargarizans, linking tissue-biased gene networks to evolutionary adaptations. We found subcutaneous fat depots prioritized calcium-mediated adipogenesis, while visceral fat diverged into female lipid storage versus male gonadal protection via Mucin O-glycans. Our work redefines amphibian adipose systems as vertebrate lipid metabolism models, uncovers evolutionarily conserved modules in vascular regulation and stress-induced glycosylation, and elucidates mechanisms bridging adaptive energy allocation in amphibians.