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.
Highlights
Epithelial folding is a common morphogenetic process during the development of multicellular organisms
To describe the major aspects of inversion separately but in ontogenetic order of appearance, we go through the inversion process several times by calling attention to the relevant panels of Figures 2, 3, 4 and 5; each of these figures shows an image series of inversion in ontogenetic order made with four different techniques: light microscopy (LM) time-lapse in vivo imaging (Figure 2), scanning electron microscopy (SEM) (Figure 3), LM of mechanical, midsagittal sections (Figure 4) and optical sections by confocal laser scanning microscopy (Figure 5)
The spheroidal embryo exhibits sporadic movements of the cell monolayer, and several dents quickly appear and disappear (Figure 6A). This phenomenon was observed in V. carteri, V. aureus and V. rousseletii embryos and is known as ‘denting’ [20,26,39]
Summary
Epithelial folding is a common morphogenetic process during the development of multicellular organisms. The bending and folding of a sheet of cells is fundamentally a biomechanical, supercellular process involving coordinated changes in the shapes of many neighboring cells that interact; the biological and biomechanical processes that underlie such threedimensional (3D) morphogenetic events in metazoans are usually complex and difficult to investigate [2,3,4,5,6,7,9,10,11,12,13,14,15,16,17,18,19]. The similarities between the morphogenetic process of inversion in Volvox carteri and epithelial folding events in metazoans include cell adherence, cell shape changes, cell movements, transmission of forces between neighboring cells and the involvement of cytoskeletal elements [20,22,23,24,26,27,28,29]. Concerted movements of cells with respect to the CB system are crucial for the process of inversion in V. carteri [20,22,23,24,26,27,28,29]
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