Stephanie Höhn and Armin Hallmann have published a detailed study of the developmental process of inversion in Pleodorina californica. Pleodorina is one of the two genera we usually refer to as ‘partially differentiated’ (the other is Astrephomene), meaning that some of their cells are specialized for motility and never reproduce (soma) and some perform both motility and reproductive functions. P. californica is pretty big, up to about 1/3 of a millimeter, easily visible to the naked eye (though you’d need better vision than mine to make out any details).
Stephanie Höhn sampling a pond near Cambridge University during the Volvox 2015 meeting.
Like all members of the family Volvocaceae, P. californica undergoes complete inversion during development:
After the completion of the cell division phase and before inversion, the embryos of Gonium, Pandorina, Eudorina and Pleodorina consist of a bowl-shaped cell sheet, whereas the embryonic cells of Volvox form a spherical cell sheet. With exception of the genus Astrephomene, all multicellular volvocine embryos face the same “problem”: the flagellar ends of all the cells point toward the interior of the bowl-shaped or spherical cell sheet rather than to the exterior, where they need to be later to function during locomotion. [References removed]
Here’s a cool video from the paper: Höhn&Hallmann_Pleodorina_inversion_video.
I’ve written previously about Dr. Höhn’s work on inversion in Volvox, and I’m glad to see that she’s continuing with other volvocine genera.
Figure 1 from Höhn & Hallmann 2016. Schematic representations of cell sheet configurations of volvocine algae before and after embryonic inversion mapped on a phylogenetic tree.
As in Volvox, P. californica inversion involves a combination of changes in cell shape and movements relative to the cytoplasmic bridges:
Figure 11 from Höhn & Hallmann 2016. Model of the inversion process and subsequent development in P. californica. Cell content is shown in green; red lines indicate the position of the cytoplasmic bridges; nuclei are shown in blue. The directions of the cell layer movements are indicated by black arrows. a Pre-inversion stage. b, c Early inversion stage: the peripheral (anterior) region of the plakea bends outwards. d-f Mid-inversion stage: Bending of the peripheral region of the cell sheet continuous and, simultaneously, the centrally located posterior region of the plakea moves towards the opening of the bowl-shaped cell sheet. g, h Late inversion stage: the entire cell sheet proceeds to bend so that the previously concave plakea becomes more and more convex; at the end of inversion the cell sheet is two-thirds closed. i-k Post-inversion stage: the cells round up and the opening (phialopore) closes; ECM biosynthesis begins. l Young adult shortly after release from its mother spheroid.
But the inversion process in Pleodorina is substantially different from that in smaller, undifferentiated algae in the same family:
According to the previous descriptions of Gonium, Pandorina and Eudorina, all cells of their embryos likewise undergo simultaneous and uniform cell wedging and the basal cell ends become conical. It appears that uniform and simultaneous cell shape changes are sufficient to fold the formerly flat cell sheet in P[latydorina] caudata and the initially bowl-shaped embryos of Gonium, Pandorina and Eudorina. In contrast, we observed non-simultaneous, non-uniform cell shape changes in the 64- to 128-celled Pleodorina embryos. Our observation suggests that Pleodorina embryos have passed a threshold in cell number and embryo size that requires a more complex inversion process. [Referenced removed]
Leading Höhn and Hallmann to conclude:
Compared to species with lower or higher cell number, inversion in P. californica shows intermediate complexity. With increasing cell number of multicellular volvocine genera there is a trend towards more complex inversion processes. Not only does the inversion of the cell sheet become more complex but also the appearing cell shapes show increasingly more spatially and temporally distinct differences and different cell shapes occur in different regions of the cell sheet.
These comparisons lead them to infer
….a gradual increase in complexity of the application of the same basic cellular mechanisms.
We don’t know what the genetic basis for inversion is in P. californica, but there’s good reason to suspect that it’s similar to that in Volvox carteri. The invA gene, which is necessary for V. carteri inversion, has a homolog in Chlamydomonas with high amino acid sequence similarity (Nishii et al. 2003), so some version of this gene was probably present in the most recent common ancestor of the Volvocaceae. If so, it seems unlikely that Pleodorina would have reinvented the wheel, so to speak.
Regardless of the genetic basis, though, it does seem that the ‘basic cellular mechanisms’ of inversion are conserved among the volvocine species in which it has been characterized: changes in cell shape combined with movements relative to the cytoplasmic bridges. Whether the ‘gradual increase in complexity’ results from changes in protein-coding sequences, from changes in gene expression, or as a physical consequence of larger size remains to be seen.
Stable links:
Höhn S and Hallmann A 2016 Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina BMC Dev. Biol. 16:35.
Nishii I, Ogihara S and Kirk D L 2003 A kinesin, invA, plays an essential role in Volvox morphogenesis. Cell 113:743–753
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