Abstract
The simultaneous expression of the hunchback gene in the numerous nuclei of the developing fly embryo gives us a unique opportunity to study how transcription is regulated in living organisms. A recently developed MS2-MCP technique for imaging nascent messenger RNA in living Drosophila embryos allows us to quantify the dynamics of the developmental transcription process. The initial measurement of the morphogens by the hunchback promoter takes place during very short cell cycles, not only giving each nucleus little time for a precise readout, but also resulting in short time traces of transcription. Additionally, the relationship between the measured signal and the promoter state depends on the molecular design of the reporting probe. We develop an analysis approach based on tailor made autocorrelation functions that overcomes the short trace problems and quantifies the dynamics of transcription initiation. Based on live imaging data, we identify signatures of bursty transcription initiation from the hunchback promoter. We show that the precision of the expression of the hunchback gene to measure its position along the anterior-posterior axis is low both at the boundary and in the anterior even at cycle 13, suggesting additional post-transcriptional averaging mechanisms to provide the precision observed in fixed embryos.
Highlights
During development the different identities of cells are determined by sequentially expressing particular subsets of genes in different parts of the embryo
The fly embryo provides a natural laboratory to study the dynamics of transcription and its implications for the developing organism
Using live imaging experiments we investigate the nature of transcription regulation of the hunchback gene—the first to read out the maternal Bicoid gradient
Summary
During development the different identities of cells are determined by sequentially expressing particular subsets of genes in different parts of the embryo. Despite many downstream points where possible mistakes can be corrected [1, 3, 4], the initial mRNA readout of the maternal Bicoid gradient by the hunchback gene is remarkably accurate and reproducible between embryos [5, 6]: it is highly expressed in the anterior part of the embryo, quickly decreasing in the middle and not expressed in the posterior part This precision is even more surprising given the very short duration of the cell cycles (6–15 minutes) during which the initial Bicoid readout takes place and the intrinsic molecular noise in transcription regulation [7,8,9]
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