Coordinating cell polarization and morphogenesis through mechanical feedback.

Many cellular processes require cell polarization to be maintained as the cell changes shape, grows or moves. Without feedback mechanisms relaying information about cell shape to the polarity molecular machinery, the coordination between cell polarization and morphogenesis, movement or growth would...

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Main Authors: Samhita P Banavar, Michael Trogdon, Brian Drawert, Tau-Mu Yi, Linda R Petzold, Otger Campàs
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-01-01
Series:PLoS Computational Biology
Online Access:https://doi.org/10.1371/journal.pcbi.1007971
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author Samhita P Banavar
Michael Trogdon
Brian Drawert
Tau-Mu Yi
Linda R Petzold
Otger Campàs
author_facet Samhita P Banavar
Michael Trogdon
Brian Drawert
Tau-Mu Yi
Linda R Petzold
Otger Campàs
author_sort Samhita P Banavar
collection DOAJ
description Many cellular processes require cell polarization to be maintained as the cell changes shape, grows or moves. Without feedback mechanisms relaying information about cell shape to the polarity molecular machinery, the coordination between cell polarization and morphogenesis, movement or growth would not be possible. Here we theoretically and computationally study the role of a genetically-encoded mechanical feedback (in the Cell Wall Integrity pathway) as a potential coordination mechanism between cell morphogenesis and polarity during budding yeast mating projection growth. We developed a coarse-grained continuum description of the coupled dynamics of cell polarization and morphogenesis as well as 3D stochastic simulations of the molecular polarization machinery in the evolving cell shape. Both theoretical approaches show that in the absence of mechanical feedback (or in the presence of weak feedback), cell polarity cannot be maintained at the projection tip during growth, with the polarization cap wandering off the projection tip, arresting morphogenesis. In contrast, for mechanical feedback strengths above a threshold, cells can robustly maintain cell polarization at the tip and simultaneously sustain mating projection growth. These results indicate that the mechanical feedback encoded in the Cell Wall Integrity pathway can provide important positional information to the molecular machinery in the cell, thereby enabling the coordination of cell polarization and morphogenesis.
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spelling doaj.art-e34c6226ee824aeba51118c8455e54332022-12-21T21:27:17ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582021-01-01171e100797110.1371/journal.pcbi.1007971Coordinating cell polarization and morphogenesis through mechanical feedback.Samhita P BanavarMichael TrogdonBrian DrawertTau-Mu YiLinda R PetzoldOtger CampàsMany cellular processes require cell polarization to be maintained as the cell changes shape, grows or moves. Without feedback mechanisms relaying information about cell shape to the polarity molecular machinery, the coordination between cell polarization and morphogenesis, movement or growth would not be possible. Here we theoretically and computationally study the role of a genetically-encoded mechanical feedback (in the Cell Wall Integrity pathway) as a potential coordination mechanism between cell morphogenesis and polarity during budding yeast mating projection growth. We developed a coarse-grained continuum description of the coupled dynamics of cell polarization and morphogenesis as well as 3D stochastic simulations of the molecular polarization machinery in the evolving cell shape. Both theoretical approaches show that in the absence of mechanical feedback (or in the presence of weak feedback), cell polarity cannot be maintained at the projection tip during growth, with the polarization cap wandering off the projection tip, arresting morphogenesis. In contrast, for mechanical feedback strengths above a threshold, cells can robustly maintain cell polarization at the tip and simultaneously sustain mating projection growth. These results indicate that the mechanical feedback encoded in the Cell Wall Integrity pathway can provide important positional information to the molecular machinery in the cell, thereby enabling the coordination of cell polarization and morphogenesis.https://doi.org/10.1371/journal.pcbi.1007971
spellingShingle Samhita P Banavar
Michael Trogdon
Brian Drawert
Tau-Mu Yi
Linda R Petzold
Otger Campàs
Coordinating cell polarization and morphogenesis through mechanical feedback.
PLoS Computational Biology
title Coordinating cell polarization and morphogenesis through mechanical feedback.
title_full Coordinating cell polarization and morphogenesis through mechanical feedback.
title_fullStr Coordinating cell polarization and morphogenesis through mechanical feedback.
title_full_unstemmed Coordinating cell polarization and morphogenesis through mechanical feedback.
title_short Coordinating cell polarization and morphogenesis through mechanical feedback.
title_sort coordinating cell polarization and morphogenesis through mechanical feedback
url https://doi.org/10.1371/journal.pcbi.1007971
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