Diffusion vs direct transport in the precision of morphogen readout

  1. Sean Fancher  Is a corresponding author
  2. Andrew Mugler  Is a corresponding author
  1. University of Pennsylvania, United States
  2. Purdue University, United States

Abstract

Morphogen profiles allow cells to determine their position within a developing organism, but not all morphogen profiles form by the same mechanism. Here we derive fundamental limits to the precision of morphogen concentration sensing for two canonical mechanisms: the diffusion of morphogen through extracellular space and the direct transport of morphogen from source cell to target cell, e.g., via cytonemes. We find that direct transport establishes a morphogen profile without adding noise in the process. Despite this advantage, we find that for sufficiently large values of profile length, the diffusion mechanism is many times more precise due to a higher refresh rate of morphogen molecules. We predict a profile lengthscale below which direct transport is more precise, and above which diffusion is more precise. This prediction is supported by data from a wide variety of morphogens in developing Drosophila and zebrafish.

Data availability

All data used in this study is simulated via computational methods outlined in the manuscript and appendices.

Article and author information

Author details

  1. Sean Fancher

    Department of Physics and Astronomy, University of Pennsylvania, Philadelphia, United States
    For correspondence
    sfancher@sas.upenn.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8701-192X
  2. Andrew Mugler

    Department of Physics and Astronomy, Purdue University, West Lafayette, United States
    For correspondence
    Amugler@purdue.edu
    Competing interests
    The authors declare that no competing interests exist.

Funding

Simons Foundation (376198)

  • Sean Fancher
  • Andrew Mugler

Simons Foundation (568888)

  • Sean Fancher

National Science Foundation (PHY-1945018)

  • Andrew Mugler

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

Reviewing Editor

  1. Raymond E Goldstein, University of Cambridge, United Kingdom

Publication history

  1. Received: May 15, 2020
  2. Accepted: October 13, 2020
  3. Accepted Manuscript published: October 14, 2020 (version 1)
  4. Version of Record published: November 4, 2020 (version 2)
  5. Version of Record updated: November 6, 2020 (version 3)

Copyright

© 2020, Fancher & Mugler

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.

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  1. Sean Fancher
  2. Andrew Mugler
(2020)
Diffusion vs direct transport in the precision of morphogen readout
eLife 9:e58981.
https://doi.org/10.7554/eLife.58981

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