Yeast Dynamically Modify Their Environment to Achieve Better Mating Efficiency

Department of Biochemistry and Biophysics, University of North Carolina, Chapel Hill, NC 27599, USA.
Science Signaling (Impact Factor: 6.28). 08/2011; 4(186):ra54. DOI: 10.1126/scisignal.2001763
Source: PubMed


The maintenance and detection of signaling gradients are critical for proper development and cell migration. In single-cell organisms, gradient detection allows cells to orient toward a distant mating partner or nutrient source. Budding yeast expand their growth toward mating pheromone gradients through a process known as chemotropic growth. MATα cells secrete α-factor pheromone that stimulates chemotropism and mating differentiation in MATa cells and vice versa. Paradoxically, MATa cells secrete Bar1, a protease that degrades α-factor and that attenuates the mating response, yet is also required for efficient mating. We observed that MATa cells avoid each other during chemotropic growth. To explore this behavior, we developed a computational platform to simulate chemotropic growth. Our simulations indicated that the release of Bar1 enabled individual MATa cells to act as α-factor sinks. The simulations suggested that the resultant local reshaping of pheromone concentration created gradients that were directed away from neighboring MATa cells (self-avoidance) and that were increasingly amplified toward partners of the opposite sex during elongation. The behavior of Bar1-deficient cells in gradient chambers and mating assays supported these predictions from the simulations. Thus, budding yeast dynamically remodel their environment to ensure productive responses to an external stimulus and avoid nonproductive cell-cell interactions.

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Available from: Henrik G Dohlman, Jun 27, 2014
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    • "Adaptation mechanisms target the pheromone response pathway at many levels. First, MATa cells secrete the protease Bar1 to degrade a factor, lower its concentration in the medium, and sharpen the local pheromone gradient toward the nearest mating partner (Jin et al., 2011; Sprague and Herskowitz, 1981). Second, the regulator of G-protein-signaling protein, Sst2, attenuates signaling through interactions with both the receptor and the guanosine triphosphate-bound Ga protein (Dohlman , 2009). "
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    ABSTRACT: Cellular behavior is frequently influenced by the cell's history, indicating that single cells may memorize past events. We report that budding yeast permanently escape pheromone-induced cell-cycle arrest when experiencing a deceptive mating attempt, i.e., not reaching their putative partner within reasonable time. This acquired behavior depends on super-assembly and inactivation of the G1/S inhibitor Whi3, which liberates the G1 cyclin Cln3 from translational inhibition. Super-assembly of Whi3 is a slow response to pheromone, driven by polyQ and polyN domains, counteracted by Hsp70, and stable over generations. Unlike prion aggregates, Whi3 super-assemblies are not inherited mitotically but segregate to the mother cell. We propose that such polyQ- and polyN-based elements, termed here mnemons, act as cellular memory devices to encode previous environmental conditions.
    Cell 12/2013; 155(6):1244-57. DOI:10.1016/j.cell.2013.10.046 · 32.24 Impact Factor
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    • "In addition to producing pheromones, yeast cells also produce proteases that cleave and inactivate pheromones, thus actively remodelling the pheromone landscape in their environment. In particular, the alpha-factor protease Bar1, which is released by MATa cells, helps these cells avoid each other [32,33]. Simplified setups, such as release of pheromone through micropipette or microfluidic devices, have been used to show that MATa cells orient growth towards the source of an artificial pheromone gradient [34–37]. "
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    ABSTRACT: Many cells are able to orient themselves in a non-uniform environment by responding to localized cues. This leads to a polarized cellular response, where the cell can either grow or move towards the cue source. Fungal haploid cells secrete pheromones to signal mating, and respond by growing a mating projection towards a potential mate. Upon contact of the two partner cells, these fuse to form a diploid zygote. In this review, we present our current knowledge on the processes of mating signalling, pheromone-dependent polarized growth and cell fusion in Saccharomyces cerevisiae and Schizosaccharomyces pombe, two highly divergent ascomycete yeast models. While the global architecture of the mating response is very similar between these two species, they differ significantly both in their mating physiologies and in the molecular connections between pheromone perception and downstream responses. The use of both yeast models helps enlighten both conserved solutions and species-specific adaptations to a general biological problem.
    Open Biology 03/2013; 3(3):130008. DOI:10.1098/rsob.130008 · 5.78 Impact Factor
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    • "This indicates that reproduction began with an active nutrient uptake mechanism in heterospecifics and that the mechanism evolved to become symbiogenesis in the conspecifics of asexual organisms (Margulis, 1998). In yeasts, epigenetic changes driven by nutrition might then have led to the creation of novel cell types, which are required at evolutionary advent of sexual reproduction (Jin et al., 2011). These epigenetic changes probably occur across the evolutionary continuum that includes both nutrition-dependent reproduction in unicellular organisms and sexual reproduction in mammals. "
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    ABSTRACT: Olfactory cues directly link the environment to gene expression. Two types of olfactory cues, food odors and social odors, alter genetically predisposed hormone-mediated activity in the mammalian brain. The honeybee is a model organism for understanding the epigenetic link from food odors and social odors to neural networks of the mammalian brain, which ultimately determine human behavior. Pertinent aspects that extend the honeybee model to human behavior include bottom-up followed by top-down gene, cell, tissue, organ, organ-system, and organism reciprocity; neurophysiological effects of food odors and of sexually dimorphic, species-specific social odors; a model of motor function required for social selection that precedes sexual selection; and hormonal effects that link current neuroscience to social science affects on the development of animal behavior. As the psychological influence of food odors and social orders is examined in detail, the socioaffective nature of olfactory cues on the biologically based development of sexual preferences across all species that sexually reproduce becomes clearer.
    03/2012; 2:17338. DOI:10.3402/snp.v2i0.17338
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