|
ScienceWeek
CELL BIOLOGY: ON VOLVOX
The following points are made by David L. Kirk (Current Biology 2004 14:R599):
1) The name "Volvox" comes from the Latin volvere, to roll, and -ox, as in atrox, fierce. Volvox is a spherical multicellular green alga, which contains many small biflagellate somatic cells and a few large, non-motile reproductive cells called gonidia, and swims with a characteristic rolling motion.
2) Ever since Anton van Leeuwenhoek (1632-1723) first viewed these algal "fierce rollers" with utter fascination in 1700, one biologist after another has pointed to Volvox as a model organism that could be used to support or refute some important biological concept of the day, such as spontaneous generation, preformation, epigenesis, the continuity of the germ plasm, and so on. All attempts to exploit Volvox as a laboratory model system failed, however, until the 1960s, when Richard Starr's group finally discovered a medium in which the organism would thrive and reproduce in captivity. Starr then circled the globe, bringing into culture all 18 known (and several previously unknown) Volvox species. By 1970, he concluded that a mating pair of isolates of V. carteri from Japan had the best combination of properties to serve as a genetic model system. Most studies of Volvox reported in the last 30 years have used those strains of V. carteri or their descendants.
3) Although V. carteri has a sexual cycle that can be induced and exploited for Mendelian analysis, the sexual cycle is not used for reproduction in nature; it is used to produce dormant, diploid zygotes that are able to survive adverse conditions. During all active phases, Volvox (like other green algae) is haploid and reproduces asexually. In V. carteri, an asexual cycle begins when each mature gonidium initiates a rapid series of cleavage divisions, certain of which are visibly asymmetric and produce large gonidial initials and small somatic initials. The fully cleaved embryo contains all of the cells of both types that will be present in an adult, but it is inside out, and to achieve the adult configuration it must turn right-side-out in a gastrulation-like process called inversion. Cleavage and inversion together take about 8 hours, and the complete asexual cycle takes precisely two days when it is synchronized by a suitable light-dark cycle.
4) Following inversion, both the adult spheroid and the juvenile spheroids within it increase in size (without further cell division) by depositing large quantities of a glycoprotein-based extracellular matrix. Part way through the expansion phase, the juveniles digest their way out of the parental matrix and become free-swimming. By that time, the somatic cells of the parental spheroids, having fulfilled their function, are already moribund, and will soon be history.(1-4)
References:
1. Hallmann, A. (2003). Extracellular matrix and sex-inducing pheromone in Volvox. Int. Rev. Cytol. 227, 131-182. [Medline] Kirk, D.L. (1998). Volvox: Molecular Genetic Origins of Multicellularity and Cellular Differentiation. (New York: Cambridge University Press)
2. Kirk, D.L. (2003). Seeking the ultimate and proximate causes of Volvox multicellularity and cellular differentiation. Integr. Comp. Biol. 43, 247-253
3. Nishii, I., Ogihara, S., and Kirk, D.L. (2003). A kinesin, InvA, plays an essential role in Volvox morphogenesis. Cell 113, 743-753
4. Nozaki, H. (2003). Origin and evolution of the genera Pleodorina and Volvox. Biologia. Bratislava 58, 425-431
Current Biology http://www.current-biology.com
--------------------------------
Related Material:
DEVELOPMENTAL BIOLOGY: VOLVOX EMBRYOLOGY
The following points are made by Roediger Schmitt and Manfred Sumper (Nature 2003 424:499):
1) Something quite remarkable happens to embryos of the multicellular green alga Volvox carteri: they turn completely inside out to establish the adult body plan. This inversion process closely resembles the initial stages of the more complex gastrulation that occurs in animal embryos -- so Volvox could arguably be considered a simple model for analyzing the principles that direct such changes in shape.
2) In the embryos of most multicellular animals, sheets of cells invaginate during gastrulation, neurulation, and organ formation. Gastrulation is the central process in early animal development, and occurs during the blastula stage -- when the embryo consists simply of a hollow ball of cells. It involves complex movements that carry those cells whose descendants will form the future internal organs from their superficial position on the blastula to their definitive positions inside the embryo. Similarly, neurulation in vertebrates involves a complicated curling of a cellular sheet to form the neural tube, which in turn develops into the central nervous system.
3) Gastrulation has fascinated developmental biologists ever since it was recognized in 1874. Nearly 100 years ago, the Italian embryologist Angelo Ruffini (1864-1929) first described the appearance of elongated cells -- known as bottle or flask cells -- at the onset of the process in amphibians. Then, in his classic papers on amphibian gastrulation, Johannes Holtfreter (1901-1992) claimed that the ability to invaginate is an innate property of flask cells. Modern investigations confirm that the number and arrangement of the flask cells are critical factors for proper initiation of invagination. But, as pointed out by Keller (1996), what flask cells do -- and how, in a biomechanical sense, they do it -- remains to be elucidated. Volvox carteri, a much simpler organism, might be the Rosetta Stone that enables researchers to unlock the problem.
4) Volvox is a multicellular green alga that exhibits the simplest kind of differentiation -- the division of labor between just two types of cell. The adult organism consists of about 2,000 mortal somatic cells, which make up the surface of a hollow sphere, and 16 larger, potentially immortal reproductive cells just below the surface. The development of Volvox starts with a single reproductive cell, which undergoes a patterned sequence of 11 cell divisions. The first five divisions are symmetrical, resulting in an embryo consisting of 32 cells of similar sizes. But the sixth division of the 16 most anterior cells is asymmetric, and results in the production of 16 cell pairs of unequal size. The larger cells will become the new reproductive cells.
5) As a result of geometrical constraints, at the end of the 11 cell divisions the embryo is inside out with respect to the adult configuration: the large reproductive cells protrude from the surface, and the bases of the developing flagella of all the somatic cells point to the interior of the hollow sphere. So cell division is followed by inversion, in which the curvature of the embryo is reversed to establish the adult configuration. Development of Volvox therefore resembles that of classic models of animal development, such as sea urchins and nematode worms, in that an important differentiating cell division is visibly asymmetric, and the adult configuration is attained by a gastrulation-like event.
Nature http://www.nature.com/nature
--------------------------------
Related Material:
BIODEVELOPMENT: CELL DIVISION AND GASTRULATION
The following points are made by T. Duncan and T.T. Su (Current Biology 2004 14:R305):
1) Embryogenesis requires the production of sufficient cells, the correct placement of these cells within the embryo, and the assignment to them of appropriate identities. Complications arise because cell division and cell migration seem incompatible. Mitosis requires the assembly and disassembly of a complex microtubule network to ensure faithful DNA segregation, and cytokinesis requires remodeling of the actin network. These events appear incompatible with the cytoskeletal re-arrangements required for the cell movement, adhesion and morphology integral to gastrulation.
2) It is noteworthy that the disruptive influence of cell division and cell movement on each other is not mutual: failure to undergo cell division does not necessarily disrupt cell migration. For example, in Drosophila embryos mutant in an activator of cyclin-dependent kinase 1 (Cdk1), cells arrest permanently in G2 at about 3 hours into embryogenesis, yet gastrulation occurs [2]. This is unsurprising, because the interphase cytoskeleton should be compatible with cell migration. It is when cell division occurs inappropriately that cell movements are disrupted.
3) The disruptive consequences of undergoing cell division when gastrulation should be occurring have been well documented in Drosophila. Mutations in the tribbles gene allow future mesodermal cells to enter mitosis ahead of schedule and in doing so disrupt mesoderm invagination[3-5]. New work in Xenopus[1] has extended this relationship to vertebrates, and suggests that inhibitory phosphorylation of Cdk1 is a conserved mechanism for coordinating mitosis and gastrulation between insects and amphibians.
4) Cdks are key regulators of cell cycle phases and are subject to multiple mechanisms of regulation specific to cell type and cell cycle stage. For example, changes in Cdk levels, cyclin association and abundance, subcellular localization, substrate availability, activating phosphorylation, inhibitory phosphorylation and binding of inhibitors can all affect Cdk activity. Although many mechanisms might have evolved to ensure that cell cycle duration is appropriately regulated at morphogenetic transitions, it appears that at least in Xenopus and Drosophila a common control mechanism is the regulation of Cdk1 activity via phosphorylation and dephosphorylation of tyrosine 15 (Y15). Phosphorylation of Y15 inhibits Cdk1 activity, while dephosphorylation by Cdc25 family phosphatases activates Cdk1. The tribbles gene encodes a kinase-like protein that lowers the level of String (Cdc25): in tribbles mutants, String accumulates prematurely in the future mesoderm; consequently these cells enter mitosis prematurely and mesoderm invagination fails [4].
References (abridged):
1. Murakami, M.S., Moody, S.A., Daar, I.O., and Morrison, D.K. (2004). Morphogenesis during Xenopus gastrulation requires Wee1-mediated inhibition of cell proliferation. Development 131, 571-580
2. Edgar, B.A. and O'Farrell, P.H. (1990). The three postblastoderm cell cycles of Drosophila embryogenesis are regulated in G2 by string. Cell 62, 469-480
3. Grosshans, J. and Wieschaus, E. (2000). A genetic link between morphogenesis and cell division during formation of the ventral furrow in Drosophila. Cell 101, 523-531
4. Mata, J., Curado, S., Ephrussi, A., and Rorth, P. (2000). Tribbles coordinates mitosis and morphogenesis in Drosophila by regulating string/CDC25 proteolysis. Cell 101, 511-522
5. Seher, T.C. and Leptin, M. (2000). Tribbles, a cell-cycle brake that coordinates proliferation and morphogenesis during Drosophila gastrulation. Curr. Biol. 10, 623-629
Current Biology http://www.current-biology.com
ScienceWeek http://scienceweek.com
|