Abstract
BackgroundThe 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.ResultsIn this study we characterized the inversion of initially bowl-shaped embryos of the 64- to 128-celled volvocine species Pleodorina californica. We focused on the movement patterns of the cell sheet, cell shape changes and changes in the localization of cytoplasmic bridges (CBs) connecting the cells. The development of living embryos was recorded using time-lapse light microscopy. Moreover, fixed and sectioned embryos throughout inversion and at successive stages of development were analyzed by light and transmission electron microscopy. We generated three-dimensional models of the identified cell shapes including the localization of CBs.ConclusionsIn contrast to descriptions concerning volvocine embryos with lower cell numbers, the embryonic cells of P. californica undergo non-simultaneous and non-uniform cell shape changes. In P. californica, cell wedging in combination with a relocation of the CBs to the basal cell tips explains the curling of the cell sheet during inversion. In volvocine genera with lower organismal complexity, the cell shape changes and relocation of CBs are less pronounced in comparison to P. californica, while they are more pronounced in all members of the genus Volvox. This finding supports an increasing significance of the temporal and spatial regulation of cell shape changes and CB relocations with both increasing cell number and organismal complexity during evolution of differentiated multicellularity.Electronic supplementary materialThe online version of this article (doi:10.1186/s12861-016-0134-9) contains supplementary material, which is available to authorized users.
Highlights
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
We provide a detailed characterization of cell shape changes, cell sheet deformations and the relative position of cell-cell connections
We first describe the movement patterns of the entire cell sheet throughout inversion in chronological order and in a second pass through the inversion process, we take a close look at the successive cell shape changes
Summary
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. In other multicellular volvocine genera, relatively few reproductive cells are derived from biflagellate cells that originally look and function like somatic cells before they enlarge and divide to form new progeny One example of this is Pleodorina, which is intermediate in organismal complexity between Volvox and its unicellular volvocine relatives (e.g., Chlamydomonas and Vitreochlamys) (Fig. 1, Additional file 1). The differences in organismal complexity between volvocine algae include, for instance, the cell number, the grade of germ-soma differentiation, the complexity of cell sheet deformations and the grade of extracellular matrix expansion (Additional file 1) [4,5,6,7,8] This situation makes the volvocine algae an excellent model to study the transition from unicellularity to multicellularity with division of labor between different cell types. In multicellular volvocine species, offspring cells stay linked to each other by cytoplasmic bridges throughout the rest of embryogenesis due to an incomplete cytokinesis [12,13,14,15,16,17,18]
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