A SOSEKI-based coordinate system interprets global polarity cues in Arabidopsis

Abstract

Multicellular development requires coordinated cell polarization relative to body axes, and21 translation to oriented cell division. In plants, it is unknown how cell polarities are connected 22 to organismal axes and translated to division. Here, we identify Arabidopsis SOSEKI (SOK) 23 proteins that integrate apical-basal and radial organismal axes to localize to polar cell edges. 24 Localization does not depend on tissue context, requires cell wall integrity and is defined by 25 a transferrable, protein-specific motif. SOK proteins structurally resemble the DIX 26 oligomerization domain in the animal Dishevelled polarity regulator. The DIX-like domain 27 self-interacts and is required for edge localization and for influencing division orientation. 28 Our work identifies a plant compass, interpreted by SOK proteins. Furthermore, despite 29 fundamental differences, polarity in plants and animals converge upon the same protein 30 domain. 31 Development of multicellular organisms relies on the ability to organize cell differentiation and 32

DIX Domain Polymerization Drives Assembly of Plant Cell Polarity Complexes

“…Equivalent to Dishevelled DIX Previously, we found that the N-terminal part of the DUF966 domain of AtSOK1 is capable of homo-dimerization, and that it may resemble the DIX domains of Dishevelled and Axin, based on secondary structure predictions (Yoshida et al, 2019). The Dishevelled DIX domain undergoes dynamic head-to-tail polymerization, which results in filamentous assemblies that can be observed by electron microscopy and in protein crystals (Madrzak et al, 2015;Schwarz-Romond et al, 2007a).…”

“…The genome of the flowering plant Arabidopsis thaliana encodes five SOSEKI proteins, each of which shows polar localization during development (Yoshida et al, 2019). To identity other SOSEKI proteins in the plant kingdom, we searched the OneKP dataset (Matasci et al, 2014;Wickett et al, 2014) using a bioinformatic pipeline as previously described (Mutte et al, 2018).…”

“…We previously used a misexpression system based on the RPS5A promoter to demonstrate the functional relevance of the N-terminal DUF966 domain in AtSOK1 (Yoshida et al, 2019). When misexpressed, SOK1 localizes to polar edges in any cell it is expressed in, and this misexpression induces aberrations in cell division orientation ( Figure 2B; 70% of independent transgenics show at least one abnormal cell division plane in median cross-section; n = 37), which serves as a readout for biological activity of the SOK1 protein.…”

“…Given the equivalence of their DIX domains, we asked if SOK1 can also form puncta. SOK1 is first expressed in the early embryo (Mö ller et al, 2017;Yoshida et al, 2019), and embryonic cells thus allow visualizing early stages of polarization of SOK1. Indeed, high-resolution imaging of SOK1-YFP, expressed from its natural promoter, in young Arabidopsis embryos showed clear puncta at the membrane, and enriched in the polar edge domain ( Figure 5G).…”

“…Each of these proteins displays robust polar edge localization in multiple cell types throughout development. Polar localization of SOSEKI proteins involves two conserved domains: a central domain required for membrane association that dictates localization to polar edges, and an N-terminal domain required for focused localization at these edges (Yoshida et al, 2019). The N-terminal domain was proposed to contain a DIX domain-like fold, hinting at similarities between animal and plant cell polarity systems.…”