Algal Morphogenesis: How Volvox Turns Itself Inside-Out

The coordinated movements of epithelial tissues play vital roles in a variety of processes, from embryonic development to wound healing. The multicellular green alga Volvox carteri is a useful model organism for studying one such movement: epithelial bending [2]. During embryogenesis, the immature spheroid Volvox undergoes a process known as inversion whereby it turns itself completely inside out [3]. The recent discovery by David Kirk and colleagues [4] that a kinesin is essential for this process provides new clues for how a cellular sheet can make a sharp bend. An adult Volvox consists of 2,000–4,000 somatic cells in a single spherical sheet surrounding 16 larger, reproductive cells known as gonidia [5]. During asexual reproduction, each mature gonidium within the spheroid undergoes 11 or 12 rapid rounds of cell division. Because cytokinesis is incomplete during these early cleavage stages, the resulting somatic cells are actually a syncytium connected by a network of cytoplasmic bridges [6,7]. By the end of cleavage, there may be as many as 100,000 total bridges in an embryo, with nearly 25 bridges linking the average cell to its neighbors. The immature Volvox, though, is an ‘inside-out’ sphere, with its nascent gonidia on the external surface and the flagella of its somatic cells facing inside the organism. In order to achieve its final adult form, each embryonic Volvox must effectively turn itself inside-out, a process known as inversion (Figure 1A). The cellsheet bending that occurs during Volvox inversion begins at a specific site known as the phialopore, a swastika-shaped opening found at the anterior pole of the embryo. To initiate inversion, cells at the edges of the phialopore adopt an asymmetric flask-like shape (Figure 1B,C). This shape change by cells of the phialopore is sufficient to initiate bending of the epithelial sheet. In order for the cellular sheet to create a sharp arc and propagate the turn into a full inversion, the tip of each flask cell must be brought close to the tips of adjacent flask cells (Figure 1B). This is achieved by the inward movement of flask cells with respect to the sphere. Because each cell moves perpendicularly to the plane of the epithelium while the cytoplasmic bridges remain stationary relative to the cellular sheet, this causes a relative displacement of the cell such that the cytoplasmic bridges are now found at the slender end of the flask cells, and forces a sharp bend in the epithelium [7]. How exactly does this displacement come about? One of the advantages of studying Volvox is that it is a genetically tractable model organism. Nishii et al. [4] used a temperature-sensitive Volvox transposon Jordan [8] — named after the US basketball star, because of its jumping abilities — to generate a panel of Volvox mutants that failed to complete inversion. One of the mutant alleles identified, InvA, was cloned and found to encode a novel type of kinesin that is expressed only in the embryo during late cleavage and inversion. Expression of HA-tagged InvA in Volvox showed that the protein is exclusively localized at the cytoplasmic bridges, regardless of whether the bridge is at the fat or slender portion of the cell. In the InvA mutant, the cells never move relative to one another and the cytoplasmic bridges remain at the fat portion of the cell (Figure 1C). As flask cell formation is not blocked, the first stages of inversion where the cellular sheet starts to bend back still occurs. But without the movement of flask cells relative to the cytoplasmic bridges, the cellular sheet is unable to propagate a sharp turn (Figure 2A,B). How does the InvA kinesin function? A regular network of rootlet and cortical microtubules originate from the basal body region and runs the length of each somatic cell. These cortical microtubule tracks lie very close to the cytoplasmic bridges, and extend all the way to the tips of the slender ends of flask cells [7,9]. The model proposed by Nishii et al. [4] argues that during inversion, the InvA kinesin, while anchored at cytoplasmic bridges, moves along cortical microtubules toward the slender ends of flask cells (Figure 2C). Effectively, this moves the cytoplasmic bridge to the slender end, forcing the slender ends of neighboring cells to be adjacent and, thus, forcing a sharp bend of the epithelial sheet. The rearrangement of epithelial sheets is a reoccurring theme in animal development [10] and Volvox inversion bears striking similarity to certain morphogenetic processes in animal embryos. For example, the dramatic reorganization of tissues during inversion is reminiscent of tissue movements witnessed during vertebrate gastrulation. Obvious analogies can also be made between flask cells and phialopore formation in Current Biology, Vol. 13, R770–R772, September 30, 2003, ©2003 Elsevier Science Ltd. All rights reserved.