Cell shape changes and the mechanism of inversion in Volvox.

Abstract

Inversion is a dominant aspect of morphogenesis in Volvox. In this process, the hollow, spheroidal Volvox embryo turns inside-out through a small opening called the phialopore to bring flagella from its inner to its outer surface. Analyses of intact, sectioned, and fragmented embryos by light, scanning electron, and transmission electron microscopy, suggest that shape changes preprogrammed into the cells cause inversion. First, cells throughout the embryo change from pear to spindle shape, which causes the embryo to contract and the phialopore to open. Then cells adjacent to the phialopore become flask-shaped, with long, thin stalks at their outer ends. Simultaneously, the cytoplasmic bridges joining all adjacent cells migrate from the midpoint of the cells to the stalk tips. Together, these changes cause the lips of cells at the phialopore margin to cud outward. Now cells progressively more distal to the phialopore become flask-shaped while the more proximal cells become columnar, causing the lips to curl progressively further over the surface of the embryo until the latter has turned completely inside-out. Fine structural analysis reveals a peripheral cytoskeleton of microtubules that is apparently involved in cellular elongation. Cell clusters isolated before inversion undergo a similar program of shape changes; this suggests that the changes in cellular shape are the cause rather than an effect of the inversion process. KEY WORDS cell shape changes eytoskeleton inversion microtubules morphogenesis VolvoxEmbryonic morphogenesis, or the development of form, is frequently accompanied by specific, sequential shape changes in the various cells that participate in the elaboration of the forming structures (2-4, 15). Many of these changes in cell shape can be attributed to the action of cytoskeletal elements such as microtubules and actinlike microfilaments (1,6,17,22,23). But how are such cytoskeletal changes controlled in a cell-and stage-specific manner? Since the form of an adult individual and its component parts are heritable features, it seems obvious that many aspects of morphogenesis, as well as the cellular processes responsible for them, must be under genetic control. However, we have at present little knowledge of the mechanisms by which specific genes control the spatial and temporal coordination of cytoskeletal elements to generate characteristic form. We have chosen to study morphogenesis in Volvox because it offers unique possibilities for obtaining fresh insights into this problem.Members of the genus Volvox are simple, multicellular, eukaryotic, photoautotrophic organisms composed of only two cell types (somatic and THE JOURNAL OF CELL B~LOGu VOLUME 75,

Computational modeling of morphogenesis regulated by mechanical feedback

“…Examples include inversion in volvox embryos (Viamontes and Kirk, 1977;Viamontes et al, 1979) and archenteron formation during gastrulation in the sea urchin (Davidson et al, 1995). Figure 7 illustrates how increased stiffness of the active region can lead to snap-through (buckling) in a spherical shell.…”

Shroom family proteins regulate γ-tubulin distribution and microtubule architecture during epithelial cell shape change

“…Apical localization and contraction of actin and myosin appear to be universal, driving apical constriction in Volvox, Drosophila, Caenorhabditis elegans and vertebrates (Hildebrand, 2005;Lee and Goldstein, 2003;Nance and Priess, 2002;Nishii and Ogihara, 1999;Young et al, 1993). Likewise, an increase in cell length is observed in apically constricting cells across taxa, including Volvox, Drosophila, shrimps, sand dollars, mice, chicks and frogs (Burnside, 1973;Hertzler and Clark, Jr, 1992;Kam et al, 1991;Kominami and Takata, 2000;Nishii and Ogihara, 1999;Schoenwolf and Franks, 1984;Schroeder, 1970;Sweeton et al, 1991;Viamontes and Kirk, 1977).…”

“…An increase in cell length is observed in apically constricting cells in organisms ranging from Volvox to arthropods and vertebrates (e.g. Schroeder, 1970;Sweeton et al, 1991;Viamontes and Kirk, 1977).…”

Green Algae and the Origins of Multicellularity in the Plant Kingdom

“…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.…”