Sci. Signal., 15 January 2013
Cell Biology Fungal Wanderlust
Annalisa M. VanHook
Science Signaling, AAAS, Washington, DC 20005, USA
In order to mate, both the budding yeast Saccharomyces cerevisiae and the fission yeast Schizosaccharomyces pombe polarize their growth toward cells of the opposite mating type and preferentially mate with nonsister cells. Polarized growth ("shmooing") is oriented into the gradient of mating pheromone that emanates from potential partners and may be initiated anywhere on the cell surface. Pheromone-mediated activation of G protein–coupled receptors frees Gβ, which recruits the Rho-family guanosine triphosphatase Cdc42. Cdc42 modifies the actin cytoskeleton to direct the exocytic events that drive growth. Polarity patches, which are clusters of polarity regulators that include Cdc42, have been observed to move around the periphery of mutant cells that are defective in pheromone perception or budding, but it has been unclear whether such "wandering" polarity patches play any role in mating under normal conditions. Dyer et al. and Bendezú et al. reported that polarity patches wandered in wild-type yeasts and appeared to help the cells locate appropriate mating partners. Using fluorescently labeled versions of Cdc42 and its associated scaffolding protein Bem1, Dyer et al. found that movement of polarity patches in S. cerevisiae occurred mainly on the side of the cell facing a pheromone source and that, before shmooing, polarity patches moved over a larger area in low, as compared to high, uniform pheromone concentrations. Movement of the polarity patches required the actin cytoskeleton, and vesicle trafficking proteins colocalized with polarity patches. Computational modeling and experiments with mutant and transgenic cells suggested that directed exocytosis at polarity patches dilutes polarity factors to promote their movement, thus enabling S. cerevisiae to track a shallow gradient. Bendezú et al. reported that Cdc42 and its associated partners also participated in polarity patch movement in S. pombe. In low uniform concentrations of mating pheromone, active Cdc42, the Cdc42 guanine nucleotide exchange factor Scd1, the scaffolding protein Scd2, and downstream components involved in actin reorganization and exocytosis colocalized in dynamic patches that moved around the cell periphery until shmooing was initiated. Enzymes required for the synthesis of cell wall components localized to the patches after the wandering phase to promote polarized growth. Imaging analysis indicated that these patches formed by repeated cycles of assembly and disassembly rather than by sliding. High concentrations of synthetic pheromone or mutations that increased pheromone signaling eliminated polarity patch wandering and instead promoted growth at the poles of these rod-shaped cells and mating with sister cells. The data from both papers point to a model in which low concentrations of mating pheromone induce the formation of wandering polarity patches, which sample the cell periphery to identify the source of the signal, and then the cells grow toward that source. As discussed in commentary by Arkowitz, this method enables these nonmotile cells to track a shallow chemical gradient, such as they would encounter in nature, to find a suitable mate.
J. M. Dyer, N. S. Savage, M. Jin, T. R. Zyla, T. C. Elston, D. J. Lew, Tracking shallow chemical gradients by actin-driven wandering of the polarization site. Curr. Biol. 23, 32–41 (2013). [PubMed]
F. O. Bendezú, S. G. Martin, Cdc42 explores the cell periphery for mate selection in fission yeast. Curr. Biol. 23, 42–47 (2013). [PubMed]
R. A. Arkowitz, Cell polarity: Wanderful exploration in yeast sex. Curr. Biol. 23, R10–R12 (2013). [Online Journal]
Citation: A. M. VanHook, Fungal Wanderlust. Sci. Signal. 6, ec15 (2013).
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