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Quantitative Modeling of a Transcriptional Grammar: Short‐Range Repression in Drosophila

Developmental gene regulation is characterized by complex networks of transcription factors and enhancers, but analysis of cis regulatory information on a genomic level by direct experimentation remains a challenge. Quantitative modeling offers an alternative path to develop a global understanding of the transcriptional regulatory code. Recent studies have focused on endogenous regulatory sequences; however distinct enhancers differ in many features, making it difficult to generalize to other cis‐regulatory elements. To isolate the effects of factor spacing, stoichiometry, and arrangement, we applied a systematic, quantitative approach to 27 simpler regulatory elements that were analyzed in the context of the Drosophila blastoderm embryo. Using a database of almost 1000 images, we present here the first quantitative analysis of short‐range transcriptional repressors, which play central roles in metazoan development. Our fractional occupancy‐ based modeling uncovered unexpected features of these proteins' activity that allow accurate predictions of regulation by the Giant, Knirps, Krüppel and Snail repressors, including modeling of endogenous enhancer sequences. This study provides essential elements of a transcriptional grammar that will allow extensive analysis of genomic information in Drosophila melanogaster and related organisms.