Diffusion vs direct transport in the precision of morphogen readout

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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.

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

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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.

"This ORCID iD identifies the author of this article:" 0000-0002-8701-192X
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.

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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.