Temperature variation drives coordinated scaling of temporal and dynamic features of transcription in embryonic development

Abstract

Temperature affects the timing of development in most poikilothermic organisms that cannot regulate their internal body temperature. In the fruit fly, Drosophila melanogaster, similar quantitative trends characterize changes in the timing of morphological events in embryogenesis from cellularization to hatching across a 10{degrees}C temperature range, such that the relative duration of each of these stages is temperature-independent. However, the extent to which the timing of the individual molecular and cellular processes underlying these morphological events recapitulates this relationship with temperature is largely unknown. Here, we characterized how the spatiotemporal dynamics of the process of transcription, which are so fundamental to cell fate commitment, scale with temperature in single cells of living fly embryos. Using the hunchback gene as a case study, we discovered that the duration of the cell cycle and the temporal and dynamic features of hunchback transcription scaled in a coordinated fashion such that the relative rates of all observed processes were temperature independent and, perhaps most surprisingly, such that the total amount of mRNA produced by the gene is unaltered by temperature changes. Our approach provides a crucial tool for understanding both developmental robustness in the face of environmental variation and for applying biochemical approaches in living Drosophila embryos.