Diverse spatial expression patterns emerge from common transcription bursting kinetics

Abstract

In early development, regulation of transcription results in precisely positioned and highly reproducible expression patterns that specify cellular identities. How transcription, a fundamentally noisy molecular process, is regulated to achieve reliable embryonic patterning remains unclear. In particular, it is unknown how gene-specific regulation mechanisms affect kinetic rates of transcription, and whether there are common, global features that govern these rates across a genetic network. Here, we measure nascent transcriptional activity in the gap gene network of early Drosophila embryos and characterize the variability in absolute activity levels across expression boundaries. We demonstrate that boundary formation follows a common transcriptional principle: a single control parameter determines the distribution of transcriptional activity, regardless of gene identity, boundary position, or enhancer-promoter architecture. By employing a minimalist model of transcription, we infer kinetic rates of transcriptional bursting for these patterning genes; we find that the key regulatory parameter is the fraction of time a gene is in an actively transcribing state, while the rate of Pol II loading appears globally conserved. These results point to a universal simplicity underlying the apparently complex transcriptional processes responsible for early embryonic patterning and indicate a path to general rules in transcriptional regulation.