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

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 combin...

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Main Authors: Jonathan Desponds, Massimo Vergassola, Aleksandra M Walczak
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/49758
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spelling doaj-67aa5d7a3259488383481a8c23dc74b62021-05-05T21:21:33ZengeLife Sciences Publications LtdeLife2050-084X2020-07-01910.7554/eLife.49758A mechanism for hunchback promoters to readout morphogenetic positional information in less than a minuteJonathan Desponds0https://orcid.org/0000-0001-7112-3217Massimo Vergassola1https://orcid.org/0000-0002-7212-8244Aleksandra M Walczak2https://orcid.org/0000-0002-2686-5702Physics Department, University of California, San Diego, La Jolla, United StatesPhysics Department, University of California, San Diego, La Jolla, United StatesLaboratoire de Physique, Ecole Normale Supérieure, PSL Research University, CNRS, Sorbonne Université, Paris, FranceCell 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.https://elifesciences.org/articles/49758regulationbiological decisionsspeed-accuracymorphogenesiscell fateDrosophila
collection DOAJ
language English
format Article
sources DOAJ
author Jonathan Desponds
Massimo Vergassola
Aleksandra M Walczak
spellingShingle Jonathan Desponds
Massimo Vergassola
Aleksandra M Walczak
A mechanism for hunchback promoters to readout morphogenetic positional information in less than a minute
eLife
regulation
biological decisions
speed-accuracy
morphogenesis
cell fate
Drosophila
author_facet Jonathan Desponds
Massimo Vergassola
Aleksandra M Walczak
author_sort Jonathan Desponds
title A mechanism for hunchback promoters to readout morphogenetic positional information in less than a minute
title_short A mechanism for hunchback promoters to readout morphogenetic positional information in less than a minute
title_full A mechanism for hunchback promoters to readout morphogenetic positional information in less than a minute
title_fullStr A mechanism for hunchback promoters to readout morphogenetic positional information in less than a minute
title_full_unstemmed A mechanism for hunchback promoters to readout morphogenetic positional information in less than a minute
title_sort mechanism for hunchback promoters to readout morphogenetic positional information in less than a minute
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-07-01
description 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.
topic regulation
biological decisions
speed-accuracy
morphogenesis
cell fate
Drosophila
url https://elifesciences.org/articles/49758
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