Subcellular spatial transcriptomics identifies three mechanistically different classes of localizing RNAs

In this study the authors identify localized RNAs in the Drosophila follicular epithelium by spatial transcriptomics and through genetic analyses determine canonical and translation-based mechanisms underlying basal and apical RNA localization. Intracellular RNA localization is a widespread and dynamic phenomenon that compartmentalizes gene expression and contributes to the functional polarization of cells. Thus far, mechanisms of RNA localization identified in Drosophila have been based on a few RNAs in different tissues, and a comprehensive mechanistic analysis of RNA localization in a single tissue is lacking. Here, by subcellular spatial transcriptomics we identify RNAs localized in the apical and basal domains of the columnar follicular epithelium (FE) and we analyze the mechanisms mediating their localization. Whereas the dynein/BicD/Egl machinery controls apical RNA localization, basally-targeted RNAs require kinesin-1 to overcome a default dynein-mediated transport. Moreover, a non-canonical, translation- and dynein-dependent mechanism mediates apical localization of a subgroup of dynein-activating adaptor-encoding RNAs (BicD, Bsg25D, hook). Altogether, our study identifies at least three mechanisms underlying RNA localization in the FE, and suggests a possible link between RNA localization and dynein/dynactin/adaptor complex formation in vivo.

Automated summary

In this study, the authors use spatial transcriptomics to identify localized RNAs in the Drosophila follicular epithelium and analyze the mechanisms underlying their localization. They find that apical RNA localization is mediated by the dynein/BicD/Egl machinery, while basally-targeted RNAs require kinesin-1. They also discover a non-canonical, translation- and dynein-dependent mechanism for the apical localization of a subgroup of dynein-activating adaptor-encoding RNAs.