Manipulation of the Cellular Membrane-Cytoskeleton Network for RNA Virus Replication and Movement in Plants

Abstract

Viruses infect all cellular life forms and cause various diseases and significant economic losses worldwide. The majority of viruses are positive-sense RNA viruses. A common feature of infection by diverse RNA viruses is to induce the formation of altered membrane structures in infected host cells. Indeed, upon entry into host cells, plant-infecting RNA viruses target preferred organelles of the cellular endomembrane system and remodel organellar membranes to form organelle-like structures for virus genome replication, termed as the viral replication organelle (VRO) or the viral replication complex (VRC). Different viruses may recruit different host factors for membrane modifications. These membrane-enclosed virus-induced replication factories provide an optimum, protective microenvironment to concentrate viral and host components for robust viral replication. Although different viruses prefer specific organelles to build VROs, at least some of them have the ability to exploit alternative organellar membranes for replication. Besides being responsible for viral replication, VROs of some viruses can be mobile to reach plasmodesmata (PD) via the endomembrane system, as well as the cytoskeleton machinery. Viral movement protein (MP) and/or MP-associated viral movement complexes also exploit the endomembrane-cytoskeleton network for trafficking to PD where progeny viruses pass through the cell-wall barrier to enter neighboring cells.

The mystery remains: How do potyviruses move within and between cells?

“…The formation of potyvirus VRCs and 6K2 vesicles induces drastic endomembrane rearrangements and relies on the early secretory pathway. Indeed, the detachment of 6K2 vesicles from the ER membrane involves the COPII‐mediated formation of transport vesicles, which bud from the ER membrane and deliver cargo to the Golgi cisternae (Brandizzi & Barlowe, 2013 ; He et al, 2023 ; Wei & Wang, 2008 ). In particular, the TuMV 6K2 protein interacts with the COPII coatomer Sec24a, the subunit interacting with cargo proteins for their packaging into COPII vesicles (Jiang et al, 2015 ).…”

A sword or a buffet: plant endomembrane system in viral infections

“…Indeed, RNA viruses induce biogenesis of such membranous replication entities, which display two basic topologies. The first type of viral replication organelles (VROs) is represented by membrane invaginations, also called spherules, while the second type is formed by membrane protrusions to generate tubules or vesicles ( He et al., 2023 ). This is made possible by the ability of viral proteins to induce membrane deformations or to seize host proteins with similar capabilities ( Agaoua et al., 2021 ).…”

“…This is made possible by the ability of viral proteins to induce membrane deformations or to seize host proteins with similar capabilities ( Agaoua et al., 2021 ). For optimal biogenesis and functioning of replication organelles, the RNA viruses coopt host proteins and modify or trigger host cellular pathways to fine tune the lipid and protein composition of these newly formed compartments ( Ketter and Randall, 2019 ; He et al., 2023 ).…”

“…2 Hijacking the plant endomembrane system generate tubules or vesicles (He et al, 2023). This is made possible by the ability of viral proteins to induce membrane deformations or to seize host proteins with similar capabilities (Agaoua et al, 2021).…”

Actomyosin‐driven motility and coalescence of phase‐separated viral inclusion bodies are required for efficient replication of a plant rhabdovirus

“…Accumulating evidence suggests that plant viruses subvert the cytoskeleton to facilitate productive infections (Niehl et al ., 2013; Pitzalis & Heinlein, 2017; He et al ., 2023). The actomyosin motility system plays a crucial role in the intracellular trafficking of viral movement proteins and/or vesicular replication complexes to target plasmodesmata and, consequently, in the cell‐to‐cell movement of many plant viruses (Harries et al ., 2010; Heinlein, 2015).…”