Excess dNTPs Trigger Oscillatory Surface Flow in the Early Drosophila Embryo

Abstract

During the first 2 hours of Drosophila development, precisely orchestrated nuclear cleavages, cytoskeletal rearrangements, and directed membrane growth lead to the formation of an epithelial sheet around the yolk. The newly formed epithelium remains relatively quiescent during the next hour as it is patterned by maternal inductive signals and zygotic gene products. We discovered that this mechanically quiet period is disrupted in embryos with high levels of dNTPs, which have been recently shown to cause abnormally fast nuclear cleavages and interfere with zygotic transcription. High levels of dNTPs are associated with robust onset of oscillatory two-dimensional flows during the third hour of development. Tissue cartography, particle image velocimetry, and dimensionality reduction techniques reveal that these oscillatory flows are low dimensional and are characterized by the presence of spiral vortices. We speculate that these aberrant flows emerge through an instability triggered by deregulated mechanical coupling between the nascent epithelium and three-dimensional yolk. These results highlight an unexplored connection between a core metabolic process and large-scale mechanics in a rapidly developing embryo.