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Systematic analysis of F-box proteins reveals a new branch of the yeast mating pathway.

ABSTRACT: The mating pathway in yeast Saccharomyces cerevisiae has long been used to reveal new mechanisms of signal transduction. The pathway comprises a pheromone receptor, a heterotrimeric G protein, and intracellular effectors of morphogenesis and transcription. Polarized cell growth, in the direction of a potential mating partner, is accomplished by the G-protein ?? subunits and the small G-protein Cdc42. Transcription induction, needed for cell-cell fusion, is mediated by G?? and the mitogen-activated protein kinase (MAPK) scaffold protein Ste5. A potential third pathway is initiated by the G-protein ? subunit Gpa1. Gpa1 signaling was shown previously to involve the F-box adaptor protein Dia2 and an endosomal effector protein, the phosphatidylinositol 3-kinase Vps34. Vps34 is also required for proper vacuolar sorting and autophagy. Here, using a panel of reporter assays, we demonstrate that mating pheromone stimulates vacuolar targeting of a cytoplasmic reporter protein and that this process depends on Vps34. Through a systematic analysis of F-box deletion mutants, we show that Dia2 is required to sustain pheromone-induced vacuolar targeting. We also found that other F-box proteins selectively regulate morphogenesis (Ydr306, renamed Pfu1) and transcription (Ucc1). These findings point to the existence of a new and distinct branch of the pheromone-signaling pathway, one that likely leads to vacuolar engulfment of cytoplasmic proteins and recycling of cellular contents in preparation for mating.

SUBMITTER: Rangarajan N

PROVIDER: S-EPMC6779436 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Systematic analysis of F-box proteins reveals a new branch of the yeast mating pathway.

Rangarajan Nambirajan N Gordy Claire L CL Askew Lauren L Bevill Samantha M SM Elston Timothy C TC Errede Beverly B Hurst Jillian H JH Kelley Joshua B JB Sheetz Joshua B JB Suzuki Sara Kimiko SK Valentin Natalie H NH Young Everett E Dohlman Henrik G HG

The Journal of biological chemistry 20190809 40

The mating pathway in yeast <i>Saccharomyces cerevisiae</i> has long been used to reveal new mechanisms of signal transduction. The pathway comprises a pheromone receptor, a heterotrimeric G protein, and intracellular effectors of morphogenesis and transcription. Polarized cell growth, in the direction of a potential mating partner, is accomplished by the G-protein βγ subunits and the small G-protein Cdc42. Transcription induction, needed for cell-cell fusion, is mediated by Gβγ and the mitogen- ...[more]

PMID: 31399514

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Project description:Mating of budding yeast cells is a model system for studying cell-cell interactions. Haploid yeast cells secrete mating pheromones that are sensed by the partner which responds by growing a mating projection toward the source. The two projections meet and fuse to form the diploid. Successful mating relies on precise coordination of dynamic extracellular signals, signaling pathways, and cell shape changes in a noisy background. It remains elusive how cells mate accurately and efficiently in a natural multi-cell environment. Here we present the first stochastic model of multiple mating cells whose morphologies are driven by pheromone gradients and intracellular signals. Our novel computational framework encompassed a moving boundary method for modeling both a-cells and ?-cells and their cell shape changes, the extracellular diffusion of mating pheromones dynamically coupled with cell polarization, and both external and internal noise. Quantification of mating efficiency was developed and tested for different model parameters. Computer simulations revealed important robustness strategies for mating in the presence of noise. These strategies included the polarized secretion of pheromone, the presence of the ?-factor protease Bar1, and the regulation of sensing sensitivity; all were consistent with data in the literature. In addition, we investigated mating discrimination, the ability of an a-cell to distinguish between ?-cells either making or not making ?-factor, and mating competition, in which multiple a-cells compete to mate with one ?-cell. Our simulations were consistent with previous experimental results. Moreover, we performed a combination of simulations and experiments to estimate the diffusion rate of the pheromone a-factor. In summary, we constructed a framework for simulating yeast mating with multiple cells in a noisy environment, and used this framework to reproduce mating behaviors and to identify strategies for robust cell-cell interactions.

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Systematic analysis of F-box proteins reveals a new branch of the yeast mating pathway.

Publications

Systematic analysis of F-box proteins reveals a new branch of the yeast mating pathway.

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