DIX Domain Polymerization Drives Assembly of Plant Cell Polarity Complexes

Cell polarity is fundamental for tissue morphogenesis in multicellular organisms. Plants and animals evolved multicellularity independently, and it is unknown whether their polarity systems are derived from a single-celled ancestor. Planar polarity in animals is conferred by Wnt signaling, an ancient signaling pathway transduced by Dishevelled, which assembles signalosomes by dynamic head-to-tail DIX domain polymerization. In contrast, polarity-determining pathways in plants are elusive. We recently discovered Arabidopsis SOSEKI proteins, which exhibit polar localization throughout development. Here, we identify SOSEKI as ancient polar proteins across land plants. Concentration-dependent polymerization via a bona fide DIX domain allows these to recruit ANGUSTIFOLIA to polar sites, similar to the polymerization-dependent recruitment of signaling effectors by Dishevelled. Cross-kingdom domain swaps reveal functional equivalence of animal and plant DIX domains. We trace DIX domains to unicellular eukaryotes and thus show that DIX-dependent polymerization is an ancient mechanism conserved between kingdoms and central to polarity proteins. [Display omitted] •SOSEKI proteins are deeply conserved polar proteins in land plants•A DIX domain mediates polymerization and polarization of SOSEKI proteins•SOSEKI polymerization allows polar recruitment of an effector protein•DIX-dependent polymerization is shared between animal and plant polarity proteins The identities of cell polarity determinants are not conserved between animals and plants; however, characterization of a DIX-domain containing protein in land plants reveals that the physical principles of polar complex assembly are preserved across eukaryotes.