An actin remodeling role for Arabidopsis processing bodies revealed by their proximity interactome

• Published in: The EMBO journal Vol. 42; no. 9; pp. e111885 - n/a
• Main Authors: Liu, Chen, Mentzelopoulou, Andriani, Muhammad, Amna, Volkov, Andriy, Weijers, Dolf, Gutierrez‐Beltran, Emilio, Moschou, Panagiotis N
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 02-05-2023; Blackwell Publishing Ltd; John Wiley and Sons Inc
• Subjects: Actin; Actin-Related Protein 2-3 Complex - metabolism; Actins - metabolism; Apexes; Arabidopsis; Arabidopsis - metabolism; Arabidopsis Proteins - metabolism; ARP2–ARP3; Biotinylation; Cell Biology; Cell size; Cellbiologi; Composition; Condensates; EMBO05; EMBO30; EMBO36; Genetics; Graph theory; Interfaces; Life Sciences; Liquidity; LLPS; Localization; Membranes; Modules; Nucleation; Phosphorylation; Plant growth; plasma membrane domains; Processing Bodies; Protein composition; Proteins; Proteomics; Proximity; Resource; SCAR–WAVE; Wave interaction; LLPS; condensates; ARP2–ARP3; plasma membrane domains; SCAR–WAVE; ARP2-ARP3; SCAR-WAVE
• ISSN: 0261-4189; 1460-2075; 1460-2075
• DOI: 10.15252/embj.2022111885

Cellular condensates can comprise membrane‐less ribonucleoprotein assemblies with liquid‐like properties. These cellular condensates influence various biological outcomes, but their liquidity hampers their isolation and characterization. Here, we investigated the composition of the condensates known as processing bodies (PBs) in the model plant
Arabidopsis thaliana
through a proximity‐biotinylation proteomics approach. Using
in situ
protein–protein interaction approaches, genetics and high‐resolution dynamic imaging, we show that processing bodies comprise networks that interface with membranes. Surprisingly, the conserved component of PBs, DECAPPING PROTEIN 1 (DCP1), can localize to unique plasma membrane subdomains including cell edges and vertices. We characterized these plasma membrane interfaces and discovered a developmental module that can control cell shape. This module is regulated by DCP1, independently from its role in decapping, and the actin‐nucleating SCAR–WAVE complex, whereby the DCP1–SCAR–WAVE interaction confines and enhances actin nucleation. This study reveals an unexpected function for a conserved condensate at unique membrane interfaces.
Synopsis
Processing body (PB) composition remains incompletely characterized. Here, proximity interactome profiling of
Arabidopsis
PBs describes their dynamic nature and identifies the role of PB components in actin‐dependent regulation of tissue growth.
The protein composition and proximity‐dependent interactome (“proxitome”) of plant processing bodies are determined by proximity biotinylation approaches.
Plant processing bodies are dynamic and include proteins linked to membrane remodeling and actin dynamics.
Processing body component DCP1 associates with the plasma membrane and the actin‐nucleating complex SCAR/WAVE at cell vertices.
DCP1 phosphorylation status regulates its localization and root growth.
Graphical Abstract
Plant processing body component DCP1 interacts with the actin‐nucleating complex SCAR/WAVE at the plasma membrane to regulate cell shape and tissue growth.