Anuran metamorphosis, which is driven by thyroid hormone (TH)-mediated processes, orchestrates intricate morphological and functional transformations for the transition from aquatic tadpoles to terrestrial life, providing a valuable model for studying organ functionalization, remodeling, and regression. Larva-specific organ regression is one of the most striking phenomena observed during the anuran metamorphic climax. While previous studies extensively analyzed the regression mechanisms of the tail, the molecular processes governing gill resorption remain elusive. We employed Microhyla fissipes as a model, and utilized a comprehensive approach involving histological analysis, transmission electron microscopy, and transcriptomics to unravel gill development and resorption. The pro-metamorphic stages revealed highly developed gill structures, emphasizing their crucial role as the primary respiratory organ for tadpoles. The transcriptomic analysis highlighted the upregulation of genes associated with enhanced respiratory efficiency, such as hemoglobin and mucins. However, as metamorphosis progressed, gill filaments underwent shrinkage, decreases in blood vessel density, and structural changes that signified a decline in respiratory function. The molecular mechanisms driving gill resorption involved the TH pathway—in particular, the upregulation of thyroid hormone receptor (TR) β, genes associated with the tumor necrosis factor pathway and matrix metalloproteinases. Two distinct pathways orchestrate gill resorption, involving apoptosis directly induced by TH and cell death through the degradation of the extracellular matrix. In addition, metabolic reorganization during metamorphosis is a complex process, with tadpoles adapting their feeding behavior and mobilizing energy storage organs. The gills, which were previously overlooked, have been unveiled as potential energy storage organs that undergo metabolic reorganization. The transcriptomic analysis revealed dynamic changes in metabolism-related genes, indicating decreased protein synthesis and energy production and enhanced substrate transport and metabolism during metamorphic climax. This study sheds light on the structural, molecular, and metabolic dynamics during gill development and resorption in M. fissipes. The findings deepen our understanding of the intricate mechanisms governing organ regression and underscore the pivotal role of the gills in facilitating the transition from aquatic to terrestrial habitats.

中文翻译：

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青蛙鳃吸收带来什么：功能丧失、细胞死亡和代谢重组


无尾动物的变态是由甲状腺激素（TH）介导的过程驱动的，它为从水生蝌蚪到陆生生命的过渡精心策划了复杂的形态和功能转变，为研究器官功能化、重塑和退化提供了一个有价值的模型。幼虫特异性器官退化是无尾动物变态高潮期间观察到的最引人注目的现象之一。虽然之前的研究广泛分析了尾部的回归机制，但控制鳃吸收的分子过程仍然难以捉摸。我们以裂纹微纹藻为模型，并利用组织学分析、透射电子显微镜和转录组学等综合方法来揭示鳃的发育和吸收。前变态阶段显示出高度发达的鳃结构，强调了它们作为蝌蚪主要呼吸器官的关键作用。转录组分析强调了与呼吸效率增强相关的基因的上调，例如血红蛋白和粘蛋白。然而，随着变态的进展，鳃丝发生收缩、血管密度降低和结构变化，这意味着呼吸功能下降。驱动鳃吸收的分子机制涉及 TH 途径，特别是甲状腺激素受体 (TR) β、与肿瘤坏死因子途径和基质金属蛋白酶相关的基因的上调。两条不同的途径协调鳃吸收，涉及 TH 直接诱导的细胞凋亡和通过细胞外基质降解引起的细胞死亡。 此外，变态过程中的代谢重组是一个复杂的过程，蝌蚪会适应其摄食行为并调动能量储存器官。以前被忽视的鳃现在被发现是进行代谢重组的潜在能量储存器官。转录组分析揭示了代谢相关基因的动态变化，表明变质高峰期间蛋白质合成和能量产生减少，底物转运和代谢增强。这项研究揭示了裂口裂殖鱼鳃发育和吸收过程中的结构、分子和代谢动力学。这些发现加深了我们对控制器官退化的复杂机制的理解，并强调了鳃在促进从水生栖息地过渡到陆地栖息地方面的关键作用。