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 morphogenesis based on its variability.
Highlights
We show how to access the information hidden in the variability in an analysis of the variability of cell sheet folding in the green alga Volvox globator
Through a combination of light sheet microscopy and mathematical modelling, we show how the inversion process, by which the spherical embryos of Volvox turn themselves inside out, results from two separate mechanisms of bending and stretching
The natural question of how to use this variability to infer developmental mechanisms appears to lie in uncharted waters,. This is the question that we explore in this paper to provide proof of principle of analysing cell sheet folding based on its variability
Summary
Acquisition of experimental dataWild-type strain V. globator Linne (SAG 199.80) was obtained from the Culture Collection of Algae at the University of Gottingen, Germany [85], and cultured as previously described [86] with a cycle of 16 h light at 24 ̊C and 8 h dark at 22 ̊C.SPIM. To decrease the loss of data due to shadowing, a second illumination arm was added to the setup (Fig 14). Illumination from both sides improved the image quality and enabled reslicing of the z-stacks when embryos began to spin during anterior inversion. V. globator parent spheroids were mounted in a column of low-melting-point agarose and suspended in fluid medium in the sample chamber. To visualise the cell sheet deformations of inverting V. globator embryos, chlorophyll autofluorescence was excited at λ = 561 nm and detected at λ > 570 nm. We acquired time-lapse data of 13 different parent spheroids, each containing 4–7 embryos
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