SEC14-like condensate phase transitions at plasma membranes regulate root growth in Arabidopsis

PLoS Biol. 2023 Sep 18;21(9):e3002305. doi: 10.1371/journal.pbio.3002305. eCollection 2023 Sep.

Abstract

Protein function can be modulated by phase transitions in their material properties, which can range from liquid- to solid-like; yet, the mechanisms that drive these transitions and whether they are important for physiology are still unknown. In the model plant Arabidopsis, we show that developmental robustness is reinforced by phase transitions of the plasma membrane-bound lipid-binding protein SEC14-like. Using imaging, genetics, and in vitro reconstitution experiments, we show that SEC14-like undergoes liquid-like phase separation in the root stem cells. Outside the stem cell niche, SEC14-like associates with the caspase-like protease separase and conserved microtubule motors at unique polar plasma membrane interfaces. In these interfaces, SEC14-like undergoes processing by separase, which promotes its liquid-to-solid transition. This transition is important for root development, as lines expressing an uncleavable SEC14-like variant or mutants of separase and associated microtubule motors show similar developmental phenotypes. Furthermore, the processed and solidified but not the liquid form of SEC14-like interacts with and regulates the polarity of the auxin efflux carrier PINFORMED2. This work demonstrates that robust development can involve liquid-to-solid transitions mediated by proteolysis at unique plasma membrane interfaces.

Grants and funding

Funding for this work was through the Vetenskapsrådet (VR) (298264-2015 to PNM), Svenska Forskningsrådet Formas (MOP-86675 to PNM), Hellenic Foundation for Research & Innovation (HFRI)-Always Strive for Excellence-Theodore Papazoglou (1624 to PNM), Hellenic Foundation of Research and Innovation (HFRI) (06526 to AM), National Secretariat of research and innovation (GR) (Τ2ΕΔΚ-00597 to PNM), H2020 Marie Skłodowska-Curie Actions (RISE 872969 PANTHEON to PNM), Foundation for Research and Technology (FORTH-IMBB) Start-Up Funding (to PNM), and by the Deutsche Forschungsgemeinschaft (SCHA 1274/5-1, 841 Germany’s Excellence Strategy EXC-2070-390732324 PhenoRob to GS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.