Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina

Abstract

Background: The multicellular volvocine alga Pleodorina is intermediate in organismal complexity between its unicellular relative, Chlamydomonas, and its multicellular relative, Volvox, which shows complete division of labor between different cell types. The volvocine green microalgae form a group of genera closely related to the genus Volvox within the order Volvocales (Chlorophyta). Embryos of multicellular volvocine algae consist of a cellular monolayer that, depending on the species, is either bowl-shaped or comprises a sphere. During embryogenesis, multicellular volvocine embryos turn their cellular monolayer right-side out to expose their flagella. This process is called 'inversion' and serves as simple model for epithelial folding in metazoa. While the development of spherical Volvox embryos has been the subject of detailed studies, the inversion process of bowl-shaped embryos is less well understood. Therefore, it has been unclear how the inversion of a sphere might have evolved from less complicated processes.

The Origin of Animal Multicellularity and Cell Differentiation

“…(B) Early embryonic development of the calcareous sponge Sycon ciliatum , including amphiblastula inversion, from (Franzen 1988). (C) Early embryonic development of the volvocale Pleodorina californica (Höhn and Hallmann 2016). In other volvocales such as Volvox , an additional developmental stage is intercalated, in which the embryo first forms a sphere with flagella pointing inward, which later opens up into a continuously bending sheet that finally closes into a sphere with flagella pointing outward.…”

“…This constraint seems to apply to any spherical colony formed by clonal division of motile flagellated cells: in flagellated volvocale green algae, a similar folding process takes place (Höhn and Hallmann 2016). It plausibly applied to the first animal embryos as well: indeed, a similar series of steps takes place during the early development of calcareous sponges, which first form as concave sheets and secondarily fold into spherical embryos called “amphiblastulae” (Figure 4B) (Franzen 1988; Ereskovsky 2010; Arendt et al 2015).…”

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

“…Inversion in Volvox [ 44 , 45 ] and in related species [ 46 – 49 ] results from cell shape changes only, without the complicating additional processes found in metazoan development discussed above. This simplification facilitates the study of morphogenesis.…”

Embryonic inversion inVolvox carteri: The flipping and peeling of elastic lips

“…The questions how these different features -formation of lips and separately regulated inversion subprocesses -evolved, and in particular, whether they were lost from an ancestral alga, remain widely open. The recent observation that inversion in the genus Pleodorina features non-uniform cell shape changes [31], shared with type-B inversion [14] but absent from type-A inversion, might begin to shed some light on these issues. the shell moments are…”