Abstract

The shaping of individual cells requires a tight coordination of cell mechanics and growth. However, it is unclear how information about the mechanical state of the wall is relayed to the molecular processes building it, thereby enabling the coordination of cell wall expansion and assembly during morphogenesis. Combining theoretical and experimental approaches, we show that a mechanical feedback coordinating cell wall assembly and expansion is essential to sustain mating projection growth in budding yeast (Saccharomyces cerevisiae). Our theoretical results indicate that the mechanical feedback provided by the Cell Wall Integrity pathway, with cell wall stress sensors Wsc1 and Mid2 increasingly activating membrane-localized cell wall synthases Fks1/2 upon faster cell wall expansion, stabilizes mating projection growth without affecting cell shape. Experimental perturbation of the osmotic pressure and cell wall mechanics, as well as compromising the mechanical feedback through genetic deletion of the stress sensors, leads to cellular phenotypes that support the theoretical predictions. Our results indicate that while the existence of mechanical feedback is essential to stabilize mating projection growth, the shape and size of the cell are insensitive to the feedback.

Highlights

  • From cell division to polarization and growth, cells constantly change their shapes to perform specific tasks [1,2,3]

  • Normalizing all variables, we find 5 dimensionless parameters that control the dynamical regimes of the system (Table 1), namely koff =k0X, k0D=k0X, λD/λX, Γ, and the ratio (PρwλX)/(12μ0mwρ0kp), which corresponds to the ratio λX/λm of the exocytosis length scale λX and a length scale λm 12μ0 mw ρ0 kp/Pρw set by the expansion mechanics of the cell wall

  • While deletion of Wsc1 and Mid2 strongly affects mating projection stability (Fig 2E), our measurements show that it does not affect the size of the mating projection (Fig 5E). These results indicate that the mechanical feedback is essential to sustain stable mating projection growth, but it does not affect mating projection size, which is controlled by the exocytosis profile, as predicted theoretically (Fig 5B)

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Summary

Introduction

From cell division to polarization and growth, cells constantly change their shapes to perform specific tasks [1,2,3] These morphological changes are achieved through remodeling of the structures that mechanically sustain the cell, such as the cytoskeleton in animal cells and the cell wall in walled cells. Studies of the mechanics of walled cell morphogenesis have predominantly focused on tipgrowing cells of plant and fungal species because of their large size, simpler geometry and fast growth rates [8,9,10] In this highly polarized growth mode, cells adopt a tubular shape that extends only at the apical region (Fig 1).

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