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

PLOS Biology · 19 authors, 11 centres

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TL;DR

Using imaging, genetics, and in vitro reconstitution in Arabidopsis, this study shows that the plasma membrane lipid-binding protein SFH8 undergoes liquid-to-solid phase transitions driven by separase proteolysis at polar plasma membrane interfaces. The solidified, processed form of SFH8—not the liquid form—interacts with and regulates PIN2 polarity, contributing to robust root development.

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This preclinical study in Arabidopsis used imaging, genetics, and in vitro reconstitution to investigate phase transitions of the SEC14-like protein SFH8 at plasma membranes. SFH8 forms liquid-like phase-separated condensates at the root stem cell niche. Outside this niche, SFH8 associates with the caspase-like protease separase (ESP) and conserved microtubule motors at unique polar plasma membrane interfaces, where separase cleaves SFH8, promoting its liquid-to-solid transition. Lines expressing an uncleavable SFH8 variant or mutants of separase and associated microtubule motors showed similar developmental phenotypes, indicating the transition is functionally important. The processed and solidified form, but not the liquid form, interacts with and regulates polarity of the auxin efflux carrier PINFORMED2. The work establishes an example of LLPS with importance for plasma membrane micropatterning.

STUDY TYPE

other

SPECIALTY

preclinical research

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AI pipeline

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ORIGINAL PAPER

PMC10538751

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

PLOS Biology

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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.

CITATION EXPORT

Chen Liu, Andriani Mentzelopoulou, Fotini Papagavriil et al.. SEC14-like condensate phase transitions at plasma membranes regulate root growth in Arabidopsis. PLOS Biology. (2023). https://doi.org/10.1371/journal.pbio.3002305

AUTHORS

19 · 11 CENTRES

Chen Liu, Andriani Mentzelopoulou, Fotini Papagavriil, Prashanth Ramachandran, Artemis Perraki, Lucas Claus, Sebastian Barg, Peter Dörmann, Yvon Jaillais, Philipp Johnen, Eugenia Russinova, Electra Gizeli, Gabriel Schaaf, Panagiotis Nikolaou Moschou, Ines Alvarez-Garcia, Ines Alvarez-Garcia, Ines Alvarez-Garcia, Ines Alvarez-Garcia, Ines Alvarez-Garcia

1 Department of Biology, University of Crete, Heraklion, Greece
2 Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, Heraklion, Greece
3 Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden
4 Department of Organismal Biology, Physiological Botany, Linnean Centre for Plant Biology, Uppsala University, Uppsala, Sweden
5 Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium
6 Center for Plant Systems Biology, Ghent, Belgium
7 Department of Medical Cell Biology, Uppsala University, Uppsala, Sweden
8 Institute of Molecular Physiology and Biotechnology of Plants, University of Bonn, Bonn, Germany
9 Laboratoire Reproduction et Développement des Plantes, ENS de Lyon, Université Claude Bernard Lyon 1, CNRS, INRAE, Lyon, France
10 Department of Plant Nutrition, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, Germany
University of California San Diego, UNITED STATES

EDITOR / REVIEWER

Mark Estelle

Chen Liu, Andriani Mentzelopoulou, Fotini Papagavriil et al.. SEC14-like condensate phase transitions at plasma membranes regulate root growth in Arabidopsis. PLOS Biology. (2023). https://doi.org/10.1371/journal.pbio.3002305