Chemotactic movement of a polarity site enables yeast cells to find their mates

Ghose, Debraj; Jacobs, Katherine C.; Ramirez, Samuel A.; Elston, Timothy C.; Lew, Daniel J.

doi:10.1073/pnas.2025445118

Cited by 17 publications

(25 citation statements)

References 62 publications

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“…Wandering of the polar cap is important for sensitive gradient tracking (Dyer et al, 2013), and so the small difference in the ability to track the gradient very well that we see in the p*RGS mutant (Fig 1) may be because of its decreased offset between the receptor-driven large G-protein and the Cdc42 driven polarity machinery. In addition, an offset between receptor signaling and the polar cap has recently been proposed to play a role in gradient tracking (Ghose et al, 2021), and although we did not see an effect on gradient tracking here, under more difficult tracking conditions, the observed Gα offset may enhance chemotropic growth.…”

Section: The Role Of Rgs Phosphorylation In the Pheromone Responsecontrasting

confidence: 56%

Phosphorylation of RGS regulates MAP kinase localization and promotes completion of cytokinesis

et al. 2022

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Yeast use the G-protein–coupled receptor signaling pathway to detect and track the mating pheromone. The G-protein–coupled receptor pathway is inhibited by the regulator of G-protein signaling (RGS) Sst2 which induces Gα GTPase activity and inactivation of downstream signaling. G-protein signaling activates the MAPK Fus3, which phosphorylates the RGS; however, the role of this modification is unknown. We found that pheromone-induced RGS phosphorylation peaks early; the phospho-state of RGS controls its localization and influences MAPK spatial distribution. Surprisingly, phosphorylation of the RGS promotes completion of cytokinesis before pheromone-induced growth. Completion of cytokinesis in the presence of pheromone is promoted by the kelch-repeat protein, Kel1 and antagonized by the formin Bni1. We found that RGS complexes with Kel1 and prefers the unphosphorylatable RGS mutant. We also found overexpression of unphosphorylatable RGS exacerbates cytokinetic defects, whereas they are rescued by overexpression of Kel1. These data lead us to a model where Kel1 promotes completion of cytokinesis before pheromone-induced polarity but is inhibited by unphosphorylated RGS binding.

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Section: The Role Of Rgs Phosphorylation In the Pheromone Responsecontrasting

confidence: 56%

Phosphorylation of RGS regulates MAP kinase localization and promotes completion of cytokinesis

et al. 2022

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“…Induction of Ste5-CTM expression caused cells to arrest in G1 and make a strong but mobile polarity site (Fig. 5B) (McClure et al, 2015;Ghose et al, 2021). We quantified how long it took polarity sites of partner cells to encounter each other in mating mixes, and asked if encounters resulted in commitment (cessation of movement).…”

Section: Mating Without Mapk-mediated Adaptive Pathwaysmentioning

confidence: 99%

“…1Cii). This hypothesis is based on the observation that the direction of polarity site movement is biased by the Far1 pathway responding to local pheromone gradients (Ghose et al, 2021). Simulations have shown that the pheromone gradient is very steep when the polarity sites in partner cells are near each other (Clark-Cotton et al, 2021), but upon reaching alignment there would be no net gradient across the well-centered polarity site.…”

Section: Introductionmentioning

confidence: 99%

“…A different way to explain why polarity site movement ceases upon alignment is based on the pheromone gradients (rather than absolute pheromone concentrations) across the polarity site: we will call this the “gradient trap” hypothesis ( Figure 1Cii ). This hypothesis is based on the observation that the direction of polarity site movement is biased by the Far1 pathway responding to local pheromone gradients ( Ghose et al. , 2021 ).…”

Section: Introductionmentioning

confidence: 99%

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Mechanism of commitment to a mating partner in Saccharomyces cerevisiae

Jacobs

Gorman

Lew

2022

MBoC

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Many cells detect and follow gradients of chemical signals to perform their functions. Yeast cells use gradients of extracellular pheromones to locate mating partners, providing a tractable model to understand how cells decode the spatial information in gradients. To mate, yeast cells must orient polarity toward the mating partner. Polarity sites are mobile, exploring the cell cortex until they reach the proper position, where they stop moving and “commit” to the partner. A simple model to explain commitment posits that a high concentration of pheromone is only detected upon alignment of partner cells’ polarity sites, and causes polarity site movement to stop. Here we explore how yeast cells respond to partners that make different amounts of pheromone. Commitment was surprisingly robust to varying pheromone levels, ruling out the simple model. We also tested whether adaptive pathways were responsible for the robustness of commitment, but our results show that cells lacking those pathways were still able to accommodate changes in pheromone. To explain this robustness, we suggest that the steep pheromone gradients near each mating partner's polarity site trap the polarity site in place.

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“…Although we have focused on the gradient generated by the regulation of ATPase, the regulation of the concentration gradient via phosphorylation-dephosphorylation reactions is ubiquitous. Therefore, the chemophoresis engine resulting from the regulation of the hydrolysis of other factors, such as GTPase, should work for a variety of intracellular processes [77][78][79][80].…”

Section: Discussionmentioning

confidence: 99%

Chemophoresis engine: A general mechanism of ATPase-driven cargo transport

Sugawara

Kaneko

2022

PLoS Comput Biol

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Cell polarity regulates the orientation of the cytoskeleton members that directs intracellular transport for cargo-like organelles, using chemical gradients sustained by ATP or GTP hydrolysis. However, how cargo transports are directly mediated by chemical gradients remains unknown. We previously proposed a physical mechanism that enables directed movement of cargos, referred to as chemophoresis. According to the mechanism, a cargo with reaction sites is subjected to a chemophoresis force in the direction of the increased concentration. Based on this, we introduce an extended model, the chemophoresis engine, as a general mechanism of cargo motion, which transforms chemical free energy into directed motion through the catalytic ATP hydrolysis. We applied the engine to plasmid motion in a ParABS system to demonstrate the self-organization system for directed plasmid movement and pattern dynamics of ParA-ATP concentration, thereby explaining plasmid equi-positioning and pole-to-pole oscillation observed in bacterial cells and in vitro experiments. We mathematically show the existence and stability of the plasmid-surfing pattern, which allows the cargo-directed motion through the symmetry-breaking transition of the ParA-ATP spatiotemporal pattern. We also quantitatively demonstrate that the chemophoresis engine can work even under in vivo conditions. Finally, we discuss the chemophoresis engine as one of the general mechanisms of hydrolysis-driven intracellular transport.

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Chemotactic movement of a polarity site enables yeast cells to find their mates

Cited by 17 publications

References 62 publications

Phosphorylation of RGS regulates MAP kinase localization and promotes completion of cytokinesis

Phosphorylation of RGS regulates MAP kinase localization and promotes completion of cytokinesis

Mechanism of commitment to a mating partner in Saccharomyces cerevisiae

Chemophoresis engine: A general mechanism of ATPase-driven cargo transport

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