Back in September, I reported on an arXiv preprint by Pierre Haas, Stephanie Höhn, and colleagues*, “Mechanics and variability of cell sheet folding in the embryonic inversion of Volvox.” A revised version of that manuscript has now been published in PLoS Biology (“The noisy basis of morphogenesis: Mechanisms and mechanics of cell sheet folding inferred from developmental variability”).
Figure 3 from Haas, Höhn, et al. 2018. Inverting Volvox globator embryo visualised by selective plane illumination microscopy of chlorophyll autofluorescence. Top row: maximum-intensity projection of z-stacks. Bottom row: tracing of midsagittal cross-sections; the colour scheme indicates image intensity. Scale bar: 50 μm.
Inversion is a crucial process in the development of algae in the family Volvocaceae (which includes Colemanosphaera, Eudorina, Pandorina, Platydorina, Pleodorina, Volvox, Volvulina, and Yamagishiella), because they start off inside-out, with their flagella pointing inward. Inversion gets the flagella on the outside where they are useful for propulsion.
This is the latest in a series of papers on the physics of Volvox inversion from Ray Goldstein’s lab, and (as with all PLoS articles) it’s open access. It presents a detailed mechanical model for the so-called “type-B” inversion that Volvox globator undergoes. This process appears to have two separately regulated components, which differ between the anterior and posterior hemispheres:
Figure 13 from Hass, Höhn, et al. 2018. Cell sheet deformations during inversion and their relative timing. (a) Equatorial invagination is driven by cell wedging that imposes bending (purple arrows in panels a–c), while the posterior hemisphere contracts simultaneously (blue arrows). These combined changes move the posterior towards the anterior pole (black arrows in panels a–c). (b) Expansion of the anterior hemisphere is initiated in the anterior fold (orange arrows in panels b and c). (c) Detail as indicated in panel b. Illustration of the relative timing of local bending and expansion. Clock diagrams correspond to locations indicated on the shapes and represent the local timing of bending (purple) and expansion (orange) relative to the average shape (red line) and average time (red clock diagrams). There is a higher variability in the timing of expansion in the anterior fold compared to the invagination of the bend region. (d) Contraction on the inner side of the anterior fold (orange arrows) can pull cells over the inflection point and drive peeling of the anterior hemisphere (curved black arrows).
Understanding inversion in Volvox has implications for animal development as well:
Type-B inversion involves equatorial invagination, posterior contraction, anterior expansion, involution, and peeling of an initially spherical cell sheet (Fig 13). Numerous morphogenetic events in metazoans share these global deformations. Invagination in amphibian, echinoderm, and nematode gastrulation; in vertebrate neurulation; and Drosophila mesoderm formation involves the formation of bottle cells that resemble the wedge-shaped cells driving invagination during inversion in Volvox. [references omitted]
The authors point out that much about the mechanics of Volvox inversion remains unknown:
it remains unclear what triggers the initial cell shape changes, what determines their location, and what kind of signal drives the propagation of waves of cell shape changes. It seems likely that the cytoplasmic bridges play a role in chemical or mechanical signal transduction. It is curious that inversion starts at the equator in type-B inversion but starts at the phialopore in type-A inversion. It is not known whether there are patterning mechanisms in Volvox that predetermine the spatial distribution of specific cell shape changes. It is unlikely that morphogens known from animals are conserved in Volvox, but plant hormones have been suggested to act as morphogens in photosynthetic organisms. Alternatively, the position of the bend region could be determined by mechanical and/or chemical cues right at the start of inversion. [references omitted]
Furthermore, there is still much to be learned about the evolution of inversion:
…all genera of Volvocaceae and its sister group Goniaceae—with the exception of the single genus Astrephomene—display some form of inversion. There is a general trend among these genera for complexity of inversion to increase with cell number, enabling comparative studies of the evolution of this complexity. The simplest inversion occurs in Gonium: as cells uniformly change their shape, the initially bowl-shaped, convex embryos become concave. Increases of this complexity may appear in different guises: certain cell shape changes may arise only in part of the cell sheet, as in Pleodorina, or cell shape changes may proceed in a wave, as exemplified by type-A inversion in Volvox…The question how the different species of the polyphyletic genus Volvox evolved different ways of turning themselves inside out remains, however. Phylogenetic studies of the volvocine algae show that different inversion types evolved several times independently in different lineages. Additionally, Pocock reported that in V. rousseletii and V. capensis, inversion type depends on the (sexual or asexual) reproduction mode. This may be a manifestation of the poorly understood role of environmental and evolutionary cues in morphogenesis, but such cues remain subject to the mechanical constraints on the respective tissue. [references omitted]
An in-depth comparative study of inversion in the volvocine algae would be fascinating. If we think of inversion as a single trait, it seems clear that it evolved either once (in an ancestor of the Volvocaceae + Goniaceae, with a single loss in Astrephomene) or twice (once in the Volvocaceae and once in Gonium, a scenario that requires no losses). But is inversion a single trait? The type-A and type-B forms are sufficiently different that it’s conceivable they evolved independently (which would make some of my published inferences wrong, BTW). Until we have descriptions as detailed as this, and possibly genetic information as well, for a larger sample of species, answering these questions with a high degree of confidence will be difficult.
*I’m calling the paper “Haas, Höhn, et al. because the first two authors are listed as equal contributors.
Stable links:
Haas, P. A., S. S. M. H. Höhn, A. R. Honerkamp-Smith, J. B. Kirkegaard, and R. E. Goldstein. 2018. The noisy basis of morphogenesis: Mechanisms and mechanics of cell sheet folding inferred from developmental variability. PLoS Biology doi: 10.1371/journal.pbio.2005536
Haas, P. A., S. S. M. H. Höhn, A. R. Honerkamp-Smith, J. B. Kirkegaard, and R. E. Goldstein. 2017. Mechanics and variability of cell sheet folding in the embryonic inversion of Volvox. arXiv 1708.07765.
[…] he studied, among other things, the physics of Volvox inversion. I have written about his work here, here, and […]