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

Elife. 2020 Jul 29:9:e49758. doi: 10.7554/eLife.49758.

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.

Keywords: D. melanogaster; Drosophila; biological decisions; cell fate; morphogenesis; physics of living systems; regulation; speed-accuracy.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / embryology*
  • Embryo, Nonmammalian / embryology*
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Models, Genetic
  • Promoter Regions, Genetic / genetics
  • Trans-Activators / genetics
  • Trans-Activators / metabolism
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism

Substances

  • DNA-Binding Proteins
  • Drosophila Proteins
  • Homeodomain Proteins
  • Trans-Activators
  • Transcription Factors
  • bcd protein, Drosophila
  • hb protein, Drosophila