Abstract
In Volvox carteri development, visibly asymmetric cleavage divisions set apart large embryonic cells that will become asexual reproductive cells (gonidia) from smaller cells that will produce terminally differentiated somatic cells. Three mechanisms have been proposed to explain how asymmetric division leads to cell specification in Volvox: (a) by a direct effect of cell size (or a property derived from it) on cell specification, (b) by segregation of a cytoplasmic factor resembling germ plasm into large cells, and (c) by a combined effect of differences in cytoplasmic quality and cytoplasmic quantity. In this study a variety of V. carteri embryos with genetically and experimentally altered patterns of development were examined in an attempt to distinguish among these hypotheses. No evidence was found for regionally specialized cytoplasm that is essential for gonidial specification. In all cases studied, cells with a diameter > approximately 8 microns at the end of cleavage--no matter where or how these cells had been produced in the embryo--developed as gonidia. Instructive observations in this regard were obtained by three different experimental interventions. (a) When heat shock was used to interrupt cleavage prematurely, so that presumptive somatic cells were left much larger than they normally would be at the end of cleavage, most cells differentiated as gonidia. This result was obtained both with wild-type embryos that had already divided asymmetrically (and should have segregated any cytoplasmic determinants involved in cell specification) and with embryos of a mutant that normally produces only somatic cells. (b) When individual wild-type blastomeres were isolated at the 16-cell stage, both the anterior blastomeres that normally produce two gonidia each and the posterior blastomeres that normally produce no gonidia underwent modified cleavage patterns and each produced an average of one large cell that developed as a gonidium. (c) When large cells were created microsurgically in a region of the embryo that normally makes only somatic cells, these large cells became gonidia. These data argue strongly for a central role of cell size in germ/soma specification in Volvox carteri, but leave open the question of how differences in cell size are actually transduced into differences in gene expression.
Highlights
In Volvox carteri development, visibly asymmetric cleavage divisions set apart large embryonic cells that will become asexual reproductive cells from smaller cells that will produce terminally differentiated somatic cells
Because there was no obvious way to modify cytoplasmic quality in a way that would necessarily be relevant, we took several differentapproaches to modify the distribution of cell sizes present at the end of cleavage as a way of testing the differing predictions made by these three hypotheses
It appeared obvious that information about the sizes of prospective germ and somatic cells at various stages of development in control, wild-type V. carteri embryos should contribute to the interpretation of the outcome of experiments in which cell size was altered
Summary
In Volvox carteri development, visibly asymmetric cleavage divisions set apart large embryonic cells that will become asexual reproductive cells (gonidia) from smaller cells that will produce terminally differentiated somatic cells. The Journal of Ceil Biology, Volume 123, Number 1, October 1993 191-208 sigma factor is inactive in the predivision cell because of the unfavorable ratio of a membrane-bound activator to a cytoplasmic inhibitor, but that this ratio suddenly shifts in the direction of activation when the small cell, with its elevated membrane/cytoplasmic ratio, is produced by asymmetric division (Margolis et al, 1991) This appears to be a rather exceptional situation; there are few if any cases in eukaryotes in which a difference in cell size has been shown to play a causal role in differential gene expression and/or dichotomous cytodifferentiation of two sister cells. It remains true that there are many cases in which it has been strongly inferred that a difference in cytoplasmic quality between sister blastomeres is causally important in differential cell specification, and few if any cases in which it has been inferred that a difference in blastomere size is the cause of differential cell specification
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