Cleavage furrow-directed cortical flows bias mechanochemical pathways for PAR polarization in the C. elegans germ lineage

Abstract

During development, the conserved PAR polarity network is continuously redeployed, requiring that it adapts to changing cellular contexts and environmental cues. How it does so and the degree to which these adaptations reflect changes in its fundamental design principles remain unclear. Here, we investigate the process of PAR polarization within the highly tractable C. elegans germline P lineage, which undergoes a series of iterative asymmetric stem cell-like divisions. Compared to the zygote, we observe significant differences in the pattern of polarity emergence, including an inversion of the initial unpolarized state, changes in symmetry breaking cues, and the timings with which anterior and posterior PARs segregate. Beneath these differences, however, polarity establishment remains reliant on the same core pathways identified in the zygote, including conserved roles for cortical actin flows and PAR-dependent self-organization. Intriguingly, we find that cleavage furrow-directed cortical actin flows play a similar symmetry-breaking role for the germline cell P1 as centrosome-induced cortical flows in the zygote. Through their ability to induce asymmetric accumulation of PAR-3 clusters, these furrow-directed flows directly couple the geometry of polarization to cell division, which could be a general strategy for cells to ensure proper organization within dynamically growing systems, such as embryos. In summary, our data suggest that coupling of novel symmetry-breaking cues with highly adaptable core mechanochemical circuits enable robust PAR polarity in response to changing developmental contexts.