Mechanical feedback coordinates cell wall expansion and assembly in yeast mating morphogenesis

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.Author summary: All morphogenesis processes, whether at the cell scale or tissue level, require the coordination of growth and mechanics to properly shape functional structures. However, the mechanisms that coordinate these two processes in the sculpting of individual cells, and especially in walled cells, remain unknown. Using yeast mating projection growth as a model system, we show that a genetically-encoded mechanical feedback relays information about the mechanical state of the cell wall to the intracellular processes assembling it, thereby coordinating cell wall expansion and growth during cell morphogenesis. We find that mechanical feedback is essential to stabilize cell growth, but the shape and size of the cell are insensitive to the feedback and independently controlled.