Three-dimensional cellularization in chytrid fungi uses distinct mechanisms from those driving one- and two-dimensional cytokinesis in animals and yeast.

Abstract

Chytrid fungi provide a model for studying three-dimensional cellularization, where nuclei that are dispersed throughout the cytoplasm are synchronously compartmentalized into daughter cells. This organization poses geometric challenges not faced by cells undergoing conventional cytokinesis or Drosophila cellularization, where nuclei are organized in one- or two-dimensional arrangements. We use the chytrid Spizellomyces punctatus to show that chytrid cellularization begins with nuclei and centrosomes migrating to the plasma membrane, where centrosome-associated vesicles define sites of membrane invagination. The resulting tubular furrows extend, creating a foam-like tessellation of polyhedral compartments, each with a nucleus and cilium. Using inhibitors and laser ablation, we show that actomyosin networks drive cellularization, while microtubules pattern but are not essential for cellularization. Finally, we suggest that chytrids may have incorporated mechanisms associated with ciliogenesis in animals to coordinate the association of internal nuclei with actomyosin networks and membranes to solve the unique challenges associated with three-dimensional cellularization.