Abstract
Cell fate decisions in the fly embryo are rapid: hunchback genes decide in minutes whether nuclei follow the anterior/posterior developmental blueprint by reading out positional information in the Bicoid morphogen. This developmental system is a prototype of regulatory decision processes that combine speed and accuracy. Traditional arguments based on fixed-time sampling of Bicoid concentration indicate that an accurate readout is impossible within the experimental times. This raises the general issue of how speed-accuracy tradeoffs are achieved. Here, we compare fixed-time to on-the-fly decisions, based on comparing the likelihoods of anterior/posterior locations. We found that these more efficient schemes complete reliable cell fate decisions within the short embryological timescales. We discuss the influence of promoter architectures on decision times and error rates, present concrete examples that rapidly readout the morphogen, and predictions for new experiments. Lastly, we suggest a simple mechanism for RNA production and degradation that approximates the log-likelihood function.
Highlights
From development to chemotaxis and immune response, living organisms make precise decisions based on limited information cues and intrinsically noisy molecular processes, such as the readout of ligand concentrations by specialized genes or receptors [1, 2, 3, 4, 5]
In Drosophila embryos, the first 13 cycles of DNA replication and mitosis occur without cytokinesis, resulting in a multinucleated syncytium containing about 6,000 nuclei [7]
Adding to the time constraints, mitosis resets the binding of transcription factors (TF) during the phase of synchronous divisions, suggesting that the decision about the nuclei’s position is made by using information accessible within one nuclear cycle
Summary
From development to chemotaxis and immune response, living organisms make precise decisions based on limited information cues and intrinsically noisy molecular processes, such as the readout of ligand concentrations by specialized genes or receptors [1, 2, 3, 4, 5]. The copyright holder for this preprint It is made available under hunchback promoters can readout morphogenetic positional information in less than a minute A PREPRINT spatial profiles are sharp and the variance in hunchback expression of nuclei at similar positions along the AP axis is small [11, 8]. Taken together, these observations imply that the short-time readout is accurate and has a low error. Experiments show that during the nuclear cycles 10-13 the positional information encoded by the Bicoid gradient is read out by hunchback promoters precisely and within 3 minutes
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