The noisy basis of morphogenesis: Mechanisms and mechanics of cell sheet folding inferred from developmental variability

PLoS Biology
Pierre A HaasRaymond E Goldstein

Abstract

Variability is emerging as an integral part of development. It is therefore imperative to ask how to access the information contained in this variability. Yet most studies of development average their observations and, discarding the variability, seek to derive models, biological or physical, that explain these average observations. Here, we analyse this variability in a study of cell sheet folding in the green alga Volvox, whose spherical embryos turn themselves inside out in a process sharing invagination, expansion, involution, and peeling of a cell sheet with animal models of morphogenesis. We generalise our earlier, qualitative model of the initial stages of inversion by combining ideas from morphoelasticity and shell theory. Together with three-dimensional visualisations of inversion using light sheet microscopy, this yields a detailed, quantitative model of the entire inversion process. With this model, we show how the variability of inversion reveals that two separate, temporally uncoupled processes drive the initial invagination and subsequent expansion of the cell sheet. This implies a prototypical transition towards higher developmental complexity in the volvocine algae and provides proof of principle of analysing mo...Continue Reading

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Citations

Apr 3, 2019·Physical Review. E·Pierre A Haas, Raymond E Goldstein
Dec 7, 2018·Physical Review. E·Pierre A Haas, Raymond E Goldstein
Feb 19, 2020·Development·Adrien Hallou, Thibaut Brunet
Mar 20, 2021·Physical Review. E·Pierre A Haas, Raymond E Goldstein

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Methods Mentioned

BETA
light sheet microscopy

Software Mentioned

Python
globator
Matlab
OpenSPIM
Volvox
bvp4c
InvA
Fiji
fminsearch
SPIM

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