Zinc Dynamics During <i>Drosophila</i> Oocyte Maturation and Egg Activation

Abstract

Temporal fluctuations in zinc concentration are emerging as essential signaling events in the regulation of meiosis during oogenesis and early embryogenesis. For example, accumulation and release of zinc in mammalian gametes are required for oocyte maturation and egg activation, respectively. Here, we report that significant zinc fluctuations occur in Drosophila melanogaster oocytes and activated eggs, and that zinc is required for female fertility. Using synchrotron-based X-ray fluorescence microscopy (XFM), we mapped the subcellular localization of essential transition metals during fly oogenesis and egg activation. Quantitative analysis of the XFM data reveals that zinc is the most abundant transition metal in oocytes and that its levels increase during oocyte maturation. This increase is accompanied by appearance of zinc-enriched intracellular granules in the oocyte. The zinc transporter Znt35C is required for maintenance of these zinc-enriched granules in mature oocytes. During egg activation, the process that follows oocyte maturation and mediates the transition of the egg to an embryo, oocyte zinc levels decrease significantly, accompanied by a decrease in the number of zinc-enriched granules. This essential pattern of zinc dynamics in Drosophila oocytes follows a similar trajectory to that in mammals, rising during oogenesis and decreasing during egg activation. This further extends the parallels in female gamete processes between Drosophila and mammals, suggesting that the former may provide an important genetically tractable model for studying the role of zinc in female reproduction.