Elevated temperature fatally disrupts nuclear divisions in the earlyDrosophilaembryo

Abstract

AbstractTemperature fluctuations can challenge animal survival, especially in embryos of animals that can’t actively regulate their body temperature. Previous work in insects suggests that spatial gradients and temporal variations in temperature can affect embryonic development in a region-specific manner. Yet, it is unclear if elevated temperature produces developmental defects, and if so, how the disruption may manifest. Here we use early embryonic development of the fruit flyDrosophila melanogasteras a model to address consequences of elevated temperature on fly embryonic development.We identified the syncytial blastoderm stage as a critical time window, being particularly sensitive to elevated temperature. The syncytial blastoderm stage involves 4 rounds of meta-synchronous nuclear divisions at the embryo cortex, followed by cellularization to form the cellular blastoderm. Live imaging these processes at elevated temperature revealed an increase in mitotic failures and a loss of cortical nuclei, both, during syncytial- and cellular-blastoderm stage. Additionally, embryos developing at elevated temperature show a local crowding of nuclei and an increase in asynchrony between the nuclear cycles in the middle vs. anterior/posterior poles. Interestingly, nuclear crowding and nuclear cycle asynchrony cooperatively amplify the frequency of mitotic failures, leading to holes in the blastoderm epithelium. Strikingly, the same treatment also increased embryonic lethality. We propose that the loss of nuclei results in a loss of patterning information and the abrogation of proper embryonic development. We identified genes that regulate mitosis, especially the ones mediating the interaction between microtubules and F-actin, and functionally tested their capacity to rescue the embryonic lethality.Our results expose a vulnerability at elevated temperatures in the interaction between cortical actin and microtubules, which leads to mitotic failures, and can be potentially rescued by modulating the expression of just a few factors. We propose that the expression levels of the corresponding genes could be used as indicators to predict fitness effects on insect populations that are exposed to increasing temperature variations.