TY - JOUR

T1 - The noisy basis of morphogenesis

T2 - Mechanisms and mechanics of cell sheet folding inferred from developmental variability.

AU - Haas, Pierre

AU - Höhn, Stephanie SMH

AU - Honerkamp-Smith, Aurelia R

AU - Kirkegaard, Julius

AU - Goldstein, Raymond

PY - 2018/9/8

Y1 - 2018/9/8

N2 - 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 morphogenesis based on its variability.

AB - 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 morphogenesis based on its variability.

U2 - 10.17863/cam.27137

DO - 10.17863/cam.27137

M3 - Journal article

JO - PLoS Biology

JF - PLoS Biology

SN - 1544-9173

M1 - e2005536

ER -