Algal Morphogenesis: How Volvox Turns Itself Inside-Out Dispatch
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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Current Biology, Vol. 13, R770–R772, September 30, 2003, ©2003 Elsevier Science Ltd. All rights reserved. DOI 10.1016/j.cub.2003.09.019 Algal Morphogenesis: How Volvox Dispatch Turns Itself Inside-Out 1 2 Douglas G. Cole and Mark V. Reedy 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 During its development, the multicellular green alga propagate the turn into a full inversion, the tip of each Volvox undergoes inversion, in which spherical flask cell must be brought close to the tips of adja- embryos turn their multicellular sheet completely cent flask cells (Figure 1B). This is achieved by the inside out. A mutant analysis has revealed that a inward movement of flask cells with respect to the novel kinesin motor protein is essential for complet- sphere. Because each cell moves perpendicularly to ing this process. the plane of the epithelium while the cytoplasmic bridges remain stationary relative to the cellular sheet, this causes a relative displacement of the cell In some colony like Volvox there once lay hidden the such that the cytoplasmic bridges are now found at secret of the body and mind of man — JS Huxley, the slender end of the flask cells, and forces a sharp 1912 [1]. 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] The coordinated movements of epithelial tissues play used a temperature-sensitive Volvox transposon vital roles in a variety of processes, from embryonic Jordan [8] — named after the US basketball star, development to wound healing. The multicellular green because of its jumping abilities — to generate a panel alga Volvox carteri is a useful model organism for of Volvox mutants that failed to complete inversion. studying one such movement: epithelial bending [2]. One of the mutant alleles identified, InvA, was cloned During embryogenesis, the immature spheroid Volvox and found to encode a novel type of kinesin that is undergoes a process known as inversion whereby it expressed only in the embryo during late cleavage turns itself completely inside out [3]. The recent dis- and inversion. Expression of HA-tagged InvA in Volvox covery by David Kirk and colleagues [4] that a kinesin showed that the protein is exclusively localized at the is essential for this process provides new clues for how cytoplasmic bridges, regardless of whether the bridge a cellular sheet can make a sharp bend. is at the fat or slender portion of the cell. In the InvA An adult Volvox consists of 2,000–4,000 somatic cells mutant, the cells never move relative to one another in a single spherical sheet surrounding 16 larger, repro- and the cytoplasmic bridges remain at the fat portion ductive cells known as gonidia [5]. During asexual of the cell (Figure 1C). As flask cell formation is not reproduction, each mature gonidium within the spher- blocked, the first stages of inversion where the cellu- oid undergoes 11 or 12 rapid rounds of cell division. lar sheet starts to bend back still occurs. But without Because cytokinesis is incomplete during these early the movement of flask cells relative to the cytoplasmic cleavage stages, the resulting somatic cells are actually bridges, the cellular sheet is unable to propagate a a syncytium connected by a network of cytoplasmic sharp turn (Figure 2A,B). bridges [6,7]. By the end of cleavage, there may be as How does the InvA kinesin function? A regular many as 100,000 total bridges in an embryo, with nearly network of rootlet and cortical microtubules originate 25 bridges linking the average cell to its neighbors. from the basal body region and runs the length of The immature Volvox, though, is an ‘inside-out’ each somatic cell. These cortical microtubule tracks sphere, with its nascent gonidia on the external surface lie very close to the cytoplasmic bridges, and extend and the flagella of its somatic cells facing inside the all the way to the tips of the slender ends of flask organism. In order to achieve its final adult form, each cells [7,9]. The model proposed by Nishii et al. [4] embryonic Volvox must effectively turn itself inside-out, argues that during inversion, the InvA kinesin, while a process known as inversion (Figure 1A). The cell- anchored at cytoplasmic bridges, moves along corti- sheet bending that occurs during Volvox inversion cal microtubules toward the slender ends of flask begins at a specific site known as the phialopore, a cells (Figure 2C). Effectively, this moves the cytoplas- swastika-shaped opening found at the anterior pole of mic bridge to the slender end, forcing the slender the embryo. To initiate inversion, cells at the edges of ends of neighboring cells to be adjacent and, thus, the phialopore adopt an asymmetric flask-like shape forcing a sharp bend of the epithelial sheet. (Figure 1B,C). The rearrangement of epithelial sheets is a reoccur- ring theme in animal development [10] and Volvox inversion bears striking similarity to certain morpho- 1Department of Microbiology, Molecular Biology and genetic processes in animal embryos. For example, Biochemistry, Life Science South 142, University of Idaho, the dramatic reorganization of tissues during inversion Moscow, Idaho 83844-3052, USA. 2Biology Department, is reminiscent of tissue movements witnessed during Creighton University, 2500 California Plaza, Omaha, Nebraska vertebrate gastrulation. Obvious analogies can also be 68178, USA. made between flask cells and phialopore formation in Current Biology R771 Figure 1. Volvox inversion. (A) Volvox embryo initiating inversion. (B) Wild-type flask cells with cytoplasmic bridges at slender end (arrows). (C) InvA mutant flask cells, where cell movement relative to cytoplasmic bridges is blocked (arrows). Volvox and bottle cells and blastopore formation in that in the former, the neural folds bend inwards (medi- gastrulating amphibian embryos. ally) as they elevate, rather than outwards. The direc- The formation and elevation of the neural folds during tionality of bending, however, is largely the result of primary neurulation in amniote embryos is also quite external forces driven by other tissues acting on the similar to Volvox inversion [11]. In a process similar to elevating neural folds, as isolated avian neural plates in flask cell formation in Volvox, columnar epithelial cells vitro do, in fact, bend outwards and roll ‘inside-out’ [12]. at the lateral edges of the neural plate narrow at their What relevance then, if any, do the results of Nishii et apical ends, causing the edges of the neural plate to ini- al. [4] have to our understanding of morphogenetic tiate bending upwards and inwards. The edges of the movements in animal embryos? The organization of neural plate, now referred to as neural folds, continue epithelial sheets in early Volvox embryos is quite to elevate and ultimately meet medially, where they different from that of metazoan embryos, which fuse to form the neural tube. The major difference generally lack the cytoplasmic bridges and associated between neural fold elevation and Volvox inversion is cortical microtubule networks seen in Volvox. In A C Model Wild type Basal bodies Cortical microtubules InvA kinesin in bridges Cell elongation Inversion plus movement of continues cells relative to the cytoplasmic bridge system Cytoplasmic B bridge InvA mutant Cell elongation Inversion but no movement is arrested of cells relative to the cytoplasmic bridge system Current Biology Figure 2. The role of InvA in Volvox inversion. Diagrammatic representations of inverting wild-type (A) and InvA mutant (B) embryos, viewed in midsaggital section. The red line rep- resents the cytoplasmic bridges that link all cells. In the absence of InvA kinesin (B), the cells fail to move relative to the bridges and inversion is arrested. (C) Anchored to the cytoplasmic bridges, the InvA kinesin is hypothesized [4] to move along the cortical micro- tubules, resulting in the net movement of the cell relative to the bridge network. Dispatch R772 addition, there do not appear to be any obvious homo- logues or orthologues of InvA in any of the vertebrate genomes sequenced to date. Together, these observa- tions suggest that the mechanisms of Volvox inversion and vertebrate gastrulation or neurulation will be quite different, despite their phenomenological similarities. Nevertheless, the implication of a novel kinesin family member in epithelial bending should be of interest to embryologists studying epithelial morphogenesis, and might suggest that those researchers take a closer look at the potential for microtubule-driven cytoskeletal activities to play a role in those processes. References 1. Huxley, J.S. (1912). The Individual in the animal kingdom. Cam- bridge University Press. 2. Kirk, D.L., and Nishii, I. (2001). Volvox carteri as a model for study- ing the genetic and cytological control of morphogenesis. Dev. Growth Differ. 43, 621-631. 3. Kuschakewisch, S. (1923). Zur Kenntnis derEntwickslungs- geschichte von Volvox. Bull de I'Acad dSc de I'Oukraine 1, 32-40. 4. Nishii, I., Ogihara, S., and Kirk, D.L. (2003). A kinesin, InvA, plays an essential role in Volvox morphogenesis. Cell 113, 743-753. 5. Kirk, D.L. (1998). Volvox: Molecular genetic origins of multicellular- ity and cellular differentiation. (New York: Cambridge University Press.) 6. Green, K.J., and Kirk, D.L. (1981). Cleavage patterns, cell lineages, and development of a cytoplasmic bridge system in Volvox embryos. J. Cell Biol. 91, 743-755. 7. Green, K.J., Viamontes, G.I., and Kirk, D.L. (1981). Mechanism of formation, ultrastructure, and function of the cytoplasmic bridge system during morphogenesis in Volvox.