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

被引:60
作者
Cheng, Guangyuan [1 ]
Yang, Zongtao [1 ]
Zhang, Hai [1 ]
Zhang, Jisen [1 ,2 ]
Xu, Jingsheng [1 ]
机构
[1] Fujian Agr & Forestry Univ, Minist Agr, Key Lab Sugarcane Biol & Genet Breeding, Natl Engn Res Ctr Sugarcane, Fuzhou 350002, Fujian, Peoples R China
[2] Fujian Agr & Forestry Univ, Fujian Prov Key Lab Haixia Appl Plant Syst Biol, Ctr Genom & Biotechnol, HIST, Fuzhou 350002, Fujian, Peoples R China
基金
中国国家自然科学基金;
关键词
actin filaments; cell-to-cell movement; Potyvirus; Remorin; VPg; MEMBRANE CONTACT SITES; POLLEN-TUBE GROWTH; PLASMA-MEMBRANE; ACTIN-FILAMENTS; ENDOPLASMIC-RETICULUM; TRANSIENT EXPRESSION; ARABIDOPSIS-THALIANA; HOST INTERACTIONS; VIRAL-INFECTION; S-ACYLATION;
D O I
10.1111/nph.16285
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
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 Ca2+ 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.
引用
收藏
页码:2122 / 2139
页数:18
相关论文
共 104 条
[1]   Contribution of Host Intracellular Transport Machineries to Intercellular Movement of Turnip Mosaic Virus [J].
Agbeci, Maxime ;
Grangeon, Romain ;
Nelson, Richard S. ;
Zheng, Huanquan ;
Laliberte, Jean-Francois .
PLOS PATHOGENS, 2013, 9 (10)
[2]   A Family of Plasmodesmal Proteins with Receptor-Like Properties for Plant Viral Movement Proteins [J].
Amari, Khalid ;
Boutant, Emmanuel ;
Hofmann, Christina ;
Schmitt-Keichinger, Corinne ;
Fernandez-Calvino, Lourdes ;
Didier, Pascal ;
Lerich, Alexander ;
Mutterer, Jerome ;
Thomas, Carole L. ;
Heinlein, Manfred ;
Mely, Yves ;
Maule, Andrew J. ;
Ritzenthaler, Christophe .
PLOS PATHOGENS, 2010, 6 (09)
[3]   Remorins form a novel family of coiled coil-forming oligomeric and filamentous proteins associated with apical, vascular and embryonic tissues in plants [J].
Bariola, PA ;
Retelska, D ;
Stasiak, A ;
Kammerer, RA ;
Fleming, A ;
Hijri, M ;
Franks, S ;
Farmer, EE .
PLANT MOLECULAR BIOLOGY, 2004, 55 (04) :579-594
[4]   From shaping organelles to signalling platforms: the emerging functions of plant ER-PM contact sites [J].
Bayer, Emmanuelle M. ;
Sparkes, Imogen ;
Vanneste, Steffen ;
Rosado, Abel .
CURRENT OPINION IN PLANT BIOLOGY, 2017, 40 :89-96
[5]   Symplastic Intercellular Connectivity Regulates Lateral Root Patterning [J].
Benitez-Alfonso, Yoselin ;
Faulkner, Christine ;
Pendle, Ali ;
Miyashima, Shunsuke ;
Helariutta, Yka ;
Maule, Andrew .
DEVELOPMENTAL CELL, 2013, 26 (02) :136-147
[6]   Plasmodesmata: Gateways to Local and Systemic Virus Infection [J].
Benitez-Alfonso, Yoselin ;
Faulkner, Christine ;
Ritzenthaler, Christophe ;
Maule, Andrew J. .
MOLECULAR PLANT-MICROBE INTERACTIONS, 2010, 23 (11) :1403-1412
[7]   Virus-host interactions during movement processes [J].
Boevink, P ;
Oparka, KJ .
PLANT PHYSIOLOGY, 2005, 138 (04) :1815-1821
[8]   Plant autophagy: mechanisms and functions [J].
Bozhkov, Peter V. .
JOURNAL OF EXPERIMENTAL BOTANY, 2018, 69 (06) :1281-1285
[9]   Multiple C2 domains and transmembrane region proteins (MCTPs) tether membranes at plasmodesmata [J].
Brault, Marie L. ;
Petit, Jules D. ;
Immel, Francoise ;
Nicolas, William J. ;
Glavier, Marie ;
Brocard, Lysiane ;
Gaston, Amelia ;
Fouche, Mathieu ;
Hawkins, Timothy J. ;
Crowet, Jean-Marc ;
Grison, Magali S. ;
Germain, Veronique ;
Rocher, Marion ;
Kraner, Max ;
Alva, Vikram ;
Claverol, Stephane ;
Paterlini, Andrea ;
Helariutta, Yka ;
Deleu, Magali ;
Lins, Laurence ;
Tilsner, Jens ;
Bayer, Emmanuelle M. .
EMBO REPORTS, 2019, 20 (08)
[10]   Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains [J].
Buecherl, Christoph A. ;
Jarsch, Iris K. ;
Schudoma, Christian ;
Segonzac, Cecile ;
Mbengue, Malik ;
Robatzek, Silke ;
MacLean, Daniel ;
Ott, Thomas ;
Zipfel, Cyril .
ELIFE, 2017, 6