Piccinini Giovanni, Valdrè Umberto, Milani Liliana
Department of Biological, Geological, and Environmental Sciences, University of Bologna, Bologna, Italy.
Genome Biol Evol. 2025 May 30;17(6). doi: 10.1093/gbe/evaf051.
Early metazoan evolution was characterized by the expansion of multiple gene families, such as the Tudor family, involved in novel multicellularity-related functions. In eukaryotes, Tudor genes (i.e. genes including at least one Tudor domain) are numerous, heterogeneous, and mostly associated with gene expression regulation. However, they underwent an animal-specific expansion, with novel elements almost exclusively involved in retrotransposon regulation through Piwi-interacting RNAs, as spatiotemporal regulators of the key-element Piwi, another previously considered animal-specific gene. Here, we used online-available proteomes covering 25 major taxonomic groups to characterize the Tudor gene family at a holozoan-wide level, confirming the apomorphic metazoan expansion of Piwi-interacting RNA-related Tudor genes. However, we also annotated elements of the Piwi-interacting RNA pathway (Tudor and Piwi genes) in Ichthyosporea species, suggesting that elements of the Piwi-interacting RNA pathway were already present in the holozoan common ancestors. We observed an outstanding variability (34-fold) of Tudor gene number between and within metazoan phyla that could be associated with convergent genomic and phenotypic evolutions: expansions were usually sided by whole-genome duplications and/or life history traits such as parthenogenesis; reductions were mostly associated to overall phenotypic and genomic simplifications, like in almost all considered endoparasites. Lastly, we phylogenetically tested, and mostly (but not completely) confirmed, a previously proposed model for the evolution of the Tudor domain secondary structures.
早期后生动物的进化特征是多个基因家族的扩张，比如参与新型多细胞相关功能的Tudor家族。在真核生物中，Tudor基因（即包含至少一个Tudor结构域的基因）数量众多、种类各异，且大多与基因表达调控相关。然而，它们经历了一次动物特有的扩张，新出现的元件几乎都通过与Piwi相互作用的RNA参与逆转座子调控，作为关键元件Piwi的时空调节因子，Piwi是另一个之前被认为是动物特有的基因。在这里，我们使用涵盖25个主要分类群的在线蛋白质组，在全后生动物水平上对Tudor基因家族进行了表征，证实了与Piwi相互作用的RNA相关Tudor基因的后生动物特有的扩张。然而，我们也在丝足虫物种中注释了与Piwi相互作用的RNA途径的元件（Tudor和Piwi基因），这表明与Piwi相互作用的RNA途径的元件在全后生动物的共同祖先中就已经存在。我们观察到后生动物门之间和门内Tudor基因数量存在显著差异（34倍），这可能与趋同的基因组和表型进化有关：基因扩张通常伴随着全基因组复制和/或孤雌生殖等生活史特征；基因数量减少大多与整体表型和基因组简化有关，比如几乎所有被研究的内寄生虫。最后，我们通过系统发育分析测试并大多（但并非完全）证实了之前提出的Tudor结构域二级结构进化模型。
