There is more than one way to turn a spherical cellular monolayer inside out: type B embryo inversion in Volvox globator

Abstract

BackgroundEpithelial folding is a common morphogenetic process during the development of multicellular organisms. In metazoans, the biological and biomechanical processes that underlie such three-dimensional (3D) developmental events are usually complex and difficult to investigate. Spheroidal green algae of the genus Volvox are uniquely suited as model systems for studying the basic principles of epithelial folding. Volvox embryos begin life inside out and then must turn their spherical cell monolayer outside in to achieve their adult configuration; this process is called 'inversion.' There are two fundamentally different sequences of inversion processes in Volvocaceae: type A and type B. Type A inversion is well studied, but not much is known about type B inversion. How does the embryo of a typical type B inverter, V. globator, turn itself inside out?ResultsIn this study, we investigated the type B inversion of V. globator embryos and focused on the major movement patterns of the cellular monolayer, cell shape changes and changes in the localization of cytoplasmic bridges (CBs) connecting the cells. Isolated intact, sectioned and fragmented embryos were analyzed throughout the inversion process using light microscopy, confocal laser scanning microscopy, scanning electron microscopy and transmission electron microscopy techniques. We generated 3D models of the identified cell shapes, including the localizations of CBs. We show how concerted cell-shape changes and concerted changes in the position of cells relative to the CB system cause cell layer movements and turn the spherical cell monolayer inside out. The type B inversion of V. globator is compared to the type A inversion in V. carteri.ConclusionsConcerted, spatially and temporally coordinated changes in cellular shapes in conjunction with concerted migration of cells relative to the CB system are the causes of type B inversion in V. globator. Despite significant similarities between type A and type B inverters, differences exist in almost all details of the inversion process, suggesting analogous inversion processes that arose through parallel evolution. Based on our results and due to the cellular biomechanical implications of the involved tensile and compressive forces, we developed a global mechanistic scenario that predicts epithelial folding during embryonic inversion in V. globator.

Origins of multicellular complexity: Volvox and the volvocine algae

“…As inversion occurs in all known members of the Volvocaceae, and as the Volvocaceae are, by most indications, monophyletic, it seems probable that the progenitor of the Volvocaceae underwent inversion. It is quite surprising, then, that at least two very different forms of inversion occur within this family (Hallmann ; Höhn & Hallmann ). The ‘Type A’ inversion of V. carteri moves from anterior to posterior, beginning with the opening of the anterior phialopore, the opening through which the cell sheet moves (Hallmann ).…”

Green Algae and the Origins of Multicellularity in the Plant Kingdom

“…Inversion in many ways parallels gastrulation in animals in which similar cell-shape changes are used to remodel the hollow, ball-like blastula and generate primordial embryonic germ layers of the gastrula (Solnica-Krezel and Sepich 2012). The sequence of events and types of cell-shape changes that drive inversion in V. carteri (termed type A inversion) and V. globator (termed type B inversion) differ substantially (Höhn and Hallmann 2011) and underscore the fact that these two species belong to independent clades of Volvox (Fig. 3A).…”

“…Full inversion of spheroidal colonies has been examined carefully in V. carteri and V. globator (Viamontes and Kirk 1977;Nishii and Ogihara 1999;Nishii 2003;Ueki and Nishii 2009;Höhn and Hallmann 2011), which use different but related mechanisms to invert. In both species, inversion is driven by coordinated cell-shape changes that move through the spheroid along the anteroposterior axis and drive cell sheet bending and involution.…”

Inherent forms and the evolution of evolution

“…Unlike most multicellular algae and land plants, however, the cells of these organisms are not cemented together by rigid matrices. As a consequence, they can undergo morphogenetic movements that are similar to gastrulation in metazoans (Hohn & Hallmann, , ; Matt & Umen, ).…”