A plant RNA virus hijacks endocytic proteins to establish its infection in plants

• Published in: The Plant journal : for cell and molecular biology Vol. 101; no. 2; pp. 384 - 400
• Main Authors: Wu, Guanwei, Cui, Xiaoyan, Dai, Zhaoji, He, Rongrong, Li, Yinzi, Yu, Kangfu, Bernards, Mark, Chen, Xin, Wang, Aiming
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.01.2020
• Subjects: adaptor protein 2; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; Biological activity; Dynamin; Dynamins - genetics; Dynamins - metabolism; Endocytosis; Endosomes; Gene Expression Regulation, Plant; Gene Knockout Techniques; host factor; Host-Pathogen Interactions - physiology; Infections; Mutants; Nicotiana - genetics; Nicotiana benthamiana; Plant Diseases; Plant viruses; Plant Viruses - metabolism; Plant Viruses - pathogenicity; Plants, Genetically Modified; Potyvirus; Protein Interaction Domains and Motifs; Proteins; Replication; RNA virus; RNA viruses; RNA Viruses - metabolism; RNA Viruses - pathogenicity; Turnip mosaic virus; Viral Proteins - metabolism; Virus Replication - physiology; virus replication complex; Viruses; Arabidopsis thaliana; adaptor protein 2; Nicotiana benthamiana; Turnip mosaic virus; RNA virus; host factor; endocytosis; potyvirus; virus replication complex; dynamin
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.14549

Summary Endocytosis and endosomal trafficking play essential roles in diverse biological processes including responses to pathogen attack. It is well established that animal viruses enter host cells through receptor‐mediated endocytosis for infection. However, the role of endocytosis in plant virus infection still largely remains unknown. Plant dynamin‐related proteins 1 (DRP1) and 2 (DRP2) are the large, multidomain GTPases that participate together in endocytosis. Recently, we have discovered that DRP2 is co‐opted by Turnip mosaic virus (TuMV) for infection in plants. We report here that DRP1 is also required for TuMV infection. We show that overexpression of DRP1 from Arabidopsis thaliana (AtDRP1A) promotes TuMV infection, and AtDRP1A interacts with several viral proteins including VPg and cylindrical inclusion (CI), which are the essential components of the virus replication complex (VRC). AtDRP1A colocalizes with the VRC in TuMV‐infected cells. Transient expression of a dominant negative (DN) mutant of DRP1A disrupts DRP1‐dependent endocytosis and supresses TuMV replication. As adaptor protein (AP) complexes mediate cargo selection for endocytosis, we further investigated the requirement of AP in TuMV infection. Our data suggest that the medium unit of the AP2 complex (AP2β) is responsible for recognizing the viral proteins as cargoes for endocytosis, and knockout of AP2β impairs intracellular endosomal trafficking of VPg and CI and inhibits TuMV replication. Collectively, our results demonstrate that DRP1 and AP2β are two proviral host factors of TuMV and shed light into the involvement of endocytosis and endosomal trafficking in plant virus infection. Significance Statement Endocytosis proteins DRP1 and AP2β are two proviral host factors of turnip mosaic virus (TuMV). TuMV proteins VPg and cylindrical inclusion (CI) are recognized by the AP2 complex and interact with DRP1/2 to enter the endocytic and endosomal trafficking pathway, which promotes the intracellular trafficking of the viral proteins as well as associated endosomes to the replication site possibly for assembly of the virus replication complex to support robust virus replication.