School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London, E1 4NS, UK.
Marine Eco-Evo-Devo Unit, Okinawa Institute for Science and Technology (OIST), 1919-1 Tancha, Onna-son, Okinawa, 904-0495, Japan.
BMC Biol. 2021 Feb 5;19(1):22. doi: 10.1186/s12915-021-00948-y.
Insects and other arthropods utilise external sensory structures for mechanosensory, olfactory, and gustatory reception. These sense organs have characteristic shapes related to their function, and in many cases are distributed in a fixed pattern so that they are identifiable individually. In Drosophila melanogaster, the identity of sense organs is regulated by specific combinations of transcription factors. In other arthropods, however, sense organ subtypes cannot be linked to the same code of gene expression. This raises the questions of how sense organ diversity has evolved and whether the principles underlying subtype identity in D. melanogaster are representative of other insects. Here, we provide evidence that such principles cannot be generalised, and suggest that sensory organ diversification followed the recruitment of sensory genes to distinct sensory organ specification mechanism. RESULTS: We analysed sense organ development in a nondipteran insect, the flour beetle Tribolium castaneum, by gene expression and RNA interference studies. We show that in contrast to D. melanogaster, T. castaneum sense organs cannot be categorised based on the expression or their requirement for individual or combinations of conserved sense organ transcription factors such as cut and pox neuro, or members of the Achaete-Scute (Tc ASH, Tc asense), Atonal (Tc atonal, Tc cato, Tc amos), and neurogenin families (Tc tap). Rather, our observations support an evolutionary scenario whereby these sensory genes are required for the specification of sense organ precursors and the development and differentiation of sensory cell types in diverse external sensilla which do not fall into specific morphological and functional classes. CONCLUSIONS: Based on our findings and past research, we present an evolutionary scenario suggesting that sense organ subtype identity has evolved by recruitment of a flexible sensory gene network to the different sense organ specification processes. A dominant role of these genes in subtype identity has evolved as a secondary effect of the function of these genes in individual or subsets of sense organs, probably modulated by positional cues.
昆虫和其他节肢动物利用外部感觉结构进行机械感觉、嗅觉和味觉接收。这些感觉器官具有与其功能相关的特征形状,并且在许多情况下以固定的模式分布,因此可以单独识别。在黑腹果蝇中,感觉器官的身份由特定的转录因子组合调节。然而,在其他节肢动物中,感觉器官亚型不能与相同的基因表达代码相关联。这就提出了感觉器官多样性是如何进化的以及在黑腹果蝇中决定感觉器官亚型身份的原则是否代表其他昆虫的问题。在这里,我们提供的证据表明,这些原则不能被普遍化,并且表明感觉器官多样化是通过将感觉基因招募到不同的感觉器官特异性机制中而发生的。结果:我们通过基因表达和 RNA 干扰研究分析了非双翅目昆虫,即面粉甲虫 Tribolium castaneum 的感觉器官发育。我们表明,与黑腹果蝇相反,T. castaneum 感觉器官不能基于单个或组合的保守感觉器官转录因子(如 cut 和 pox neuro 或 Achaete-Scute(Tc ASH、Tc asense)、Atonal(Tc atonal、Tc cato、Tc amos)和 neurogenin 家族(Tc tap)的表达或它们的要求进行分类。相反,我们的观察结果支持这样一种进化情景,即这些感觉基因是外部感觉毛中感觉器官前体的特异性、感觉细胞类型的发育和分化所必需的,而这些感觉毛不属于特定的形态和功能类。结论:基于我们的发现和过去的研究,我们提出了一种进化情景,表明感觉器官亚型身份是通过将灵活的感觉基因网络招募到不同的感觉器官特异性过程中而进化的。这些基因在亚型身份中的主导作用是这些基因在单个或一组感觉器官中的功能的次要影响,可能由位置线索调节。