Coordinating cell polarization and morphogenesis through mechanical feedback

PLoS Comput Biol. 2021 Jan 28;17(1):e1007971. doi: 10.1371/journal.pcbi.1007971. eCollection 2021 Jan.

Abstract

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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Biomechanical Phenomena / physiology
  • Cell Movement / physiology
  • Cell Polarity / physiology*
  • Cell Wall / physiology
  • Computational Biology
  • Computer Simulation
  • Feedback, Physiological / physiology*
  • Models, Biological*
  • Morphogenesis / physiology*
  • Saccharomyces cerevisiae / cytology
  • Saccharomyces cerevisiae / metabolism
  • cdc42 GTP-Binding Protein, Saccharomyces cerevisiae / metabolism

Substances

  • cdc42 GTP-Binding Protein, Saccharomyces cerevisiae