Abstract
SummaryCell 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.
Highlights
Cell polarity is fundamental for the development of organisms across kingdoms of life
We recently discovered a family of five paralogs called SOSEKI (SOK1–SOK5) in the flowering plant Arabidopsis thaliana
SOSEKI Proteins Are Shared across Land Plants The genome of the flowering plant Arabidopsis thaliana encodes five SOSEKI proteins, each of which shows polar localization during development (Yoshida et al, 2019)
Summary
Cell polarity is fundamental for the development of organisms across kingdoms of life. Individual cell polarity needs to integrate global organismal axes, and be coordinated among neighboring cells within a plane (Butler and Wallingford, 2017). Planar polarity ensures correct morphogenesis of tissues by regulating cell growth and differentiation, as well as through orienting structures protruding from single cells within epithelia, such as hairs and cilia (Butler and Wallingford, 2017). Despite the fundamental importance of cellular and planar polarity for multicellular life, it remains unclear how polarity-determining systems evolved in plants and animals. Do both kingdoms use similar mechanisms derived from their last single-celled common ancestor, or did each lineage evolve independent solutions to the same problem?
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