The pineal gland has evolved from a photoreceptive organ in fish to a neuroendocrine organ in mammals. This study integrated multiple daytime single-cell RNA-seq datasets from the pineal glands of zebrafish, rats, and monkeys, providing a detailed examination of the evolutionary transition at single-cell resolution. We identified key factors responsible for the anatomical and functional transformation of the pineal gland. We retrieved and integrated daytime single-cell transcriptomic datasets from the pineal glands of zebrafish, rats, and monkeys, resulting in a total of 22 431 cells after rigorous quality filtering. Comparative analysis was then conducted to elucidate the evolution of pineal cells, their photosensitivity, their role in melatonin production, and the signaling processes within the glands of these species. Our analysis identified distinct cellular compositions of the pineal gland in zebrafish, rats, and monkeys. Zebrafish photoreceptors exhibited comprehensive phototransduction gene expression, while specific genes, including transducin (Gngt1, Gnb3, and Gngt2) and phosducin (Pdc), were consistently present in mammalian pinealocytes. We found transcriptional similarities between the pineal gland and retina, underscoring shared evolutionary and functional pathways. Zebrafish displayed unique light-responsive circadian gene activity compared to rats and monkeys. Key ligand-receptor interactions were identified, especially involving MDK and PTN, influencing melatonin synthesis across species. Furthermore, we observed species-specific GPCR (G protein-coupled receptors) expressions related to melatonin synthesis and their alignment with retinal expressions. Our findings also highlighted specific transcription factors (TFs) and regulatory networks associated with pineal gland evolution and function. Our study provides a detailed analysis of the pineal gland's evolution from fish to mammals. We identified key transcriptional changes and controls that highlight the gland's functional diversity. Notably, we found significant ligand-receptor interactions influencing melatonin synthesis and demonstrated parallels between pineal and retinal expressions. These insights enhance our understanding of the pineal gland's role in phototransduction, melatonin production, and circadian rhythms in vertebrates.

中文翻译：

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脊椎动物松果体的跨物种单细胞景观

松果体已从鱼类的感光器官进化为哺乳动物的神经内分泌器官。这项研究整合了斑马鱼、大鼠和猴子松果体的多个白天单细胞 RNA-seq 数据集，以单细胞分辨率详细检查了进化转变。我们确定了导致松果体解剖和功能转变的关键因素。我们检索并整合了斑马鱼、大鼠和猴子松果体的白天单细胞转录组数据集，经过严格的质量过滤后总共得到了 22 431 个细胞。然后进行比较分析，以阐明松果体细胞的进化、它们的光敏性、它们在褪黑激素产生中的作用，以及这些物种腺体内的信号传导过程。我们的分析确定了斑马鱼、大鼠和猴子松果体的不同细胞组成。斑马鱼光感受器表现出全面的光转导基因表达，而包括转导蛋白（Gngt1、Gnb3和Gngt2）和光导蛋白（Pdc）在内的特定基因始终存在于哺乳动物松果体细胞中。我们发现松果体和视网膜之间的转录相似性，强调了共同的进化和功能途径。与大鼠和猴子相比，斑马鱼表现出独特的光响应昼夜节律基因活性。确定了关键的配体-受体相互作用，特别是涉及MDK和PTN 的相互作用，影响跨物种褪黑激素的合成。此外，我们观察到与褪黑激素合成相关的物种特异性 GPCR（G 蛋白偶联受体）表达及其与视网膜表达的一致性。我们的研究结果还强调了与松果体进化和功能相关的特定转录因子（TF）和调节网络。我们的研究详细分析了松果体从鱼类到哺乳动物的进化过程。我们确定了突出腺体功能多样性的关键转录变化和控制。值得注意的是，我们发现显着的配体-受体相互作用影响褪黑激素的合成，并证明了松果体和视网膜表达之间的相似性。这些见解增强了我们对松果体在脊椎动物光转导、褪黑激素产生和昼夜节律中的作用的理解。