Chapter category: Channels and Transporters
Cytoplasmic Bridges in Volvox and Its Relatives
Cell-Cell Channels
Edited by: Frantisek Baluska, Dieter Volkmann and Peter W. BarlowISBN: 0-387-36058-1
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Chapter authors:
Harold J. Hoops, Ichiro Nishii and David L. Kirk
The volvocaceans are a closely related group of green flagellates that range in size and complexity from colonial forms that contain a small number of identical cells, to Volvox in which there is a division of labor between several thousand terminally differentiated somatic cells and a small number of asexual reproductive cells called gonidia. Similar cytoplasmic bridges link the cells of all volvocacean embryos, but the formation, structure and function of such bridges have been studied most extensively during Volvox carteri embryogenesis. Each mature V. carteri gonidium produces an embryo that executes 11-12 rounds of rapid, stereotyped, synchronous cleavage divisions in the absence of any growth. Large numbers of cytoplasmic bridges are formed in each cleavage furrow as a result of incomplete cytokinesis. The bridges are tightly packed in bands that are concentric with the inner surface of the hollow embryo, and the bridge bands of all cells are linked to form a single, coherent cytoplasmic-bridge system that runs through the entire embryo and holds it together. A fully cleaved embryo contains all of the cells that will be present in an adult of the next generation, but it is inside-out with respect to the adult configuration: its gonidia are on the outside and the flagellar ends of its somatic cells are on the inside. This awkward arrangement is corrected by inversion, in which the embryo rapidly turns itself right-side-out through a combination of cell shape changes and movements. The cytoplasmic-bridge system plays a central role in inversion by providing the physical framework against which the cells exert force to reverse the curvature of the cellular sheet. Recent studies show that a kinesin located in the cytoplasmic bridges appears to provide the critical driving force of inversion. Inversion is a defining characteristic of the volvocaceans, and all of the volvocaceans that have been tested have a gene product that is homologous to the kinesin that drives inversion in V. carteri. So we think that the mechanism of inversion is probably similar in all of them. In all of the smaller volvocaceans, and in about half of all Volvox species, the cytoplasmic bridges disappear soon after inversion has been completed and a newly formed ECM has taken over the job of holding the organism together. However, three lineages of Volvox have independently evolved the trait of retaining cytoplasmic bridges throughout the life of the adult. And in each case this trait has coevolved with a novel form of embryonic development in which embryos begin to divide while they are still quite small, and then grow between successive divisions—all the while remaining connected to the adult somatic cells. Here we provide new information about the formation and the structure of persistent cytoplasmic bridges in one such species of Volvox, and review the evidence that leads us to believe that adult cytoplasmic bridges serve as conduits to convey nutrients from somatic cells to developing embryos.
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