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Mating yeast cells use an intrinsic polarity site to assemble a pheromone-gradient tracking machine
The mating of budding yeast depends on chemotropism, a fundamental cellular process. The two yeast mating types secrete peptide pheromones that bind to GPCRs on cells of the opposite type. Cells find and contact a partner by determining the direction of the pheromone source and polarizing their grow...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Rockefeller University Press
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6829655/ https://www.ncbi.nlm.nih.gov/pubmed/31570500 http://dx.doi.org/10.1083/jcb.201901155 |
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author | Wang, Xin Tian, Wei Banh, Bryan T. Statler, Bethanie-Michelle Liang, Jie Stone, David E. |
author_facet | Wang, Xin Tian, Wei Banh, Bryan T. Statler, Bethanie-Michelle Liang, Jie Stone, David E. |
author_sort | Wang, Xin |
collection | PubMed |
description | The mating of budding yeast depends on chemotropism, a fundamental cellular process. The two yeast mating types secrete peptide pheromones that bind to GPCRs on cells of the opposite type. Cells find and contact a partner by determining the direction of the pheromone source and polarizing their growth toward it. Actin-directed secretion to the chemotropic growth site (CS) generates a mating projection. When pheromone-stimulated cells are unable to sense a gradient, they form mating projections where they would have budded in the next cell cycle, at a position called the default polarity site (DS). Numerous models have been proposed to explain yeast gradient sensing, but none address how cells reliably switch from the intrinsically determined DS to the gradient-aligned CS, despite a weak spatial signal. Here we demonstrate that, in mating cells, the initially uniform receptor and G protein first polarize to the DS, then redistribute along the plasma membrane until they reach the CS. Our data indicate that signaling, polarity, and trafficking proteins localize to the DS during assembly of what we call the gradient tracking machine (GTM). Differential activation of the receptor triggers feedback mechanisms that bias exocytosis upgradient and endocytosis downgradient, thus enabling redistribution of the GTM toward the pheromone source. The GTM stabilizes when the receptor peak centers at the CS and the endocytic machinery surrounds it. A computational model simulates GTM tracking and stabilization and correctly predicts that its assembly at a single site contributes to mating fidelity. |
format | Online Article Text |
id | pubmed-6829655 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Rockefeller University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-68296552020-05-04 Mating yeast cells use an intrinsic polarity site to assemble a pheromone-gradient tracking machine Wang, Xin Tian, Wei Banh, Bryan T. Statler, Bethanie-Michelle Liang, Jie Stone, David E. J Cell Biol Research Articles The mating of budding yeast depends on chemotropism, a fundamental cellular process. The two yeast mating types secrete peptide pheromones that bind to GPCRs on cells of the opposite type. Cells find and contact a partner by determining the direction of the pheromone source and polarizing their growth toward it. Actin-directed secretion to the chemotropic growth site (CS) generates a mating projection. When pheromone-stimulated cells are unable to sense a gradient, they form mating projections where they would have budded in the next cell cycle, at a position called the default polarity site (DS). Numerous models have been proposed to explain yeast gradient sensing, but none address how cells reliably switch from the intrinsically determined DS to the gradient-aligned CS, despite a weak spatial signal. Here we demonstrate that, in mating cells, the initially uniform receptor and G protein first polarize to the DS, then redistribute along the plasma membrane until they reach the CS. Our data indicate that signaling, polarity, and trafficking proteins localize to the DS during assembly of what we call the gradient tracking machine (GTM). Differential activation of the receptor triggers feedback mechanisms that bias exocytosis upgradient and endocytosis downgradient, thus enabling redistribution of the GTM toward the pheromone source. The GTM stabilizes when the receptor peak centers at the CS and the endocytic machinery surrounds it. A computational model simulates GTM tracking and stabilization and correctly predicts that its assembly at a single site contributes to mating fidelity. Rockefeller University Press 2019-11-04 2019-09-30 /pmc/articles/PMC6829655/ /pubmed/31570500 http://dx.doi.org/10.1083/jcb.201901155 Text en © 2019 Wang et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/). |
spellingShingle | Research Articles Wang, Xin Tian, Wei Banh, Bryan T. Statler, Bethanie-Michelle Liang, Jie Stone, David E. Mating yeast cells use an intrinsic polarity site to assemble a pheromone-gradient tracking machine |
title | Mating yeast cells use an intrinsic polarity site to assemble a pheromone-gradient tracking machine |
title_full | Mating yeast cells use an intrinsic polarity site to assemble a pheromone-gradient tracking machine |
title_fullStr | Mating yeast cells use an intrinsic polarity site to assemble a pheromone-gradient tracking machine |
title_full_unstemmed | Mating yeast cells use an intrinsic polarity site to assemble a pheromone-gradient tracking machine |
title_short | Mating yeast cells use an intrinsic polarity site to assemble a pheromone-gradient tracking machine |
title_sort | mating yeast cells use an intrinsic polarity site to assemble a pheromone-gradient tracking machine |
topic | Research Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6829655/ https://www.ncbi.nlm.nih.gov/pubmed/31570500 http://dx.doi.org/10.1083/jcb.201901155 |
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