Remorin interacting with PCaP1 impairs Turnip mosaic virus intercellular movement but is antagonised by VPg

Abstract

Group 1 Remorins (REMs) are extensively involved in virus trafficking through plasmodesmata (PD). However, their roles in Potyvirus cell-to-cell movement are not known. The plasma membrane (PM)-associated Ca 2+ binding protein 1 (PCaP1) interacts with the P3N-PIPO of Turnip mosaic virus (TuMV) and is required for TuMV cell-to-cell movement, but the underlying mechanism remains elusive.The mutant plants with overexpression or knockout of REM1.2 were used to investigate its role in TuMV cell-to-cell movement. Arabidopsis thaliana complementary mutants of pcap1 were used to investigate the role of PCaP1 in TuMV cell-to-cell movement. Yeast-two-hybrid, bimolecular fluorescence complementation, co-immunoprecipitation and RT-qPCR assays were employed to investigate the underlying molecular mechanism.The results show that TuMV-P3N-PIPO recruits PCaP1 to PD and the actin filament-severing activity of PCaP1 is required for TuMV intercellular movement. REM1.2 negatively regulates the cell-to-cell movement of TuMV via competition with PCaP1 for binding actin filaments. As a counteractive response, TuMV mediates REM1.2 degradation via both 26S ubiquitin-proteasome and autophagy pathways through the interaction of VPg with REM1.2 to establish systemic infection in Arabidopsis.This work unveils the actin cytoskeleton and PM nanodomain-associated molecular events underlying the cell-to-cell movement of potyviruses.

A hetero-oligomeric remorin-receptor complex regulates plant development

“…Even though an involvement of Group 1 remorins in phytohormone controlled processes has been suggested (Alliotte et al, 1989; Yamada et al, 1998; Demir et al, 2013; Gui et al, 2016; Huang et al, 2019), the molecular function of these proteins remains elusive. Several studies have independently demonstrated that Group 1 remorins regulate viral spreading (Raffaele et al, 2009; Son et al, 2015; Perraki et al, 2018; Cheng et al, 2020), possibly by either regulating plasmodesmatal (PD) conductance (Perraki et al, 2014; Gronnier et al, 2017; Huang et al, 2019) and/or even PD biogenesis (Wei et al, 2020). However, considering that the subcellular localization of Group 1 remorins is not limited to PDs (Raffaele et al, 2009; Jarsch et al, 2014), it appears likely that they play additional roles.…”

Small hydrophobic viral proteins involved in intercellular movement of diverse plant virus genomes

“…These inclusion bodies at structurally modified PDs may serve as docking and conducting structures coordinating different viral proteins in the intercellular movement of viral replication vesicles and virions. In addition, VPg also may positively influence cell-to-cell potyvirus movement inducing proteasome-mediated degradation of plant protein remorin, thus preventing formation of remorin-specific plasma membrane nanodomains, which reduce membrane plasticity, and subsequent PD closure [5] – [7] , [44] , [60] , [86] – [90] .…”

Emerging Roles of the Selective Autophagy in Plant Immunity and Stress Tolerance

“…Recent reports indicated that Aquaporin PIP2 proteins are also subjected to degradation by selective autophagy in response to water stress [69][70][71]. Turnip mosaic virus (TuMV) mediates Remorin1.2 (REM1.2) degradation via both the 26S proteasome and autophagy pathways [72]. The VPg (Viral protein genome-linked) of potyvirus, a potent RNA-silencing suppressor, antagonizes host defense through targeting Suppressor of Gene Silencing 3 (SGS3), a key silencing player functioning in double-stranded RNA synthesis, for degradation by both UPS and autophagy pathways [73].…”

“…TuMV VPg (Nuclear inclusion protein) and the small integral membrane protein 6K2 (6 kDa protein 2) antagonize host defense by blocking the NBR1-mediated autophagic degradation of HCpro [56]. In addition, TuMV VPg interacts with and mediates the degradation of REM1.2, a protein that negatively regulates the size exclusion limit (SEL) of plasmodesmata (PD), probably via both the 26S proteasome and autophagy pathways to facilitate the cell-to-cell movement of TuMV [72]. The S-acylation of NbREM1.4/OsREM1.4 is required for their targeting to PD (104).…”