Symmetry Breaking in Spore Germination Relies on an Interplay between Polar Cap Stability and Spore Wall Mechanics

The morphogenesis of single cells depends on their ability to coordinate surface mechanics and polarity. During germination, spores of many species develop a polar tube that hatches out of a rigid outer spore wall (OSW) in a process termed outgrowth. However, how these awakening cells reorganize to stabilize this first growth axis remains unknown. Here, using quantitative experiments and modeling, we reveal the mechanisms underlying outgrowth in fission yeast. We find that, following an isotropic growth phase during which a single polarity cap wanders around the surface, outgrowth occurs when spores have doubled their volume, concomitantly with the stabilization of the cap and a singular rupture in the OSW. This rupture happens when OSW mechanical stress exceeds a threshold, releases the constraints of the OSW on growth, and stabilizes polarity. Thus, outgrowth exemplifies a self-organizing morphogenetic process in which reinforcements between growth and polarity coordinate mechanics and internal organization. [Display omitted] •Gradual growth of fission yeast spores determines an abrupt developmental transition•Mechanical stress caused by spore growth ruptures the outer spore wall (OSW)•OSW rupture converts an initial unstable wandering polarity into stable polarization•OSW rupture thus locks self-organizing polarity for subsequent growth and development By studying the developing polarity and morphogenesis of single fission yeast spores, Bonazzi et al. reveal a feedback between spore growth and polarity that links changes in cell-wall surface mechanics with internal spatial organization.