Systematic Imaging Reveals Features of Localized mRNAs and Their Changing Subcellular Destinations in Development

mRNA localization is critical for eukaryotic cells and affects numerous transcripts, yet how cells regulate distribution of many mRNAs to their subcellular destinations is still unknown. We combined transcriptomics and systematic imaging to determine tissue-specific expression and subcellular distribution of 5862 mRNAs during Drosophila oogenesis. mRNA localization is widespread in the ovary, depends on the microtubule cytoskeleton and the mRNAs enriched at the posterior cortex share common localization machinery. Localized mRNAs, in particular the posterior class, have distinct gene features and differ in expression level, 3UTR length and sequence conservation from unlocalized mRNAs. Using cross-tissue comparison we revealed that the localization status of mRNAs differs between epithelial, germline and embryonic cell types and also changes within one cell, the oocyte, over time. This dataset enables the transition from deep mechanistic dissection of singular mRNA localization events towards global understanding of how mRNAs transcribed in the nucleus distribute in cells.