A mechanism for hunchback promoters to readout morphogenetic positional information in less than a minute

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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.

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All data analyzed during this study were previously published in the literature and references are included in the paper

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Jonathan Desponds

Physics Department, University of California San Diego, La Jolla, United States

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-7112-3217
Massimo Vergassola

Physics Department, University of California San Diego, La Jolla, United States

For correspondence
massimo@physics.ucsd.edu

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-7212-8244
Aleksandra M Walczak

Laboratoire de Physique Theorique, École Normale Supérieure, Paris, France

Competing interests
Aleksandra M Walczak, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0002-2686-5702

Funding

National Science Foundation (PoLS Grant 1411313)

Massimo Vergassola

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.