6K2-induced vesicles can move cell to cell during turnip mosaic virus infection

Grangeon, Romain; Jiang, Jianan; Wan, Juan; Agbeci, Maxime; Zheng, Huanquan; Laliberté, Jean‐François

doi:10.3389/fmicb.2013.00351

Cited by 88 publications

(92 citation statements)

References 57 publications

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“…Results of intercellular movement studies employing individual MP genes transiently expressed in the absence of virus infection should be interpreted in view of the recently accepted idea that virus replication complexes (and the replicase itself) are involved in the cell‐to‐cell spread of viral genomic RNA. The data supporting this model have been reported for both single gene‐based transport systems (Amari et al ., ; Guenoune‐Gelbart et al ., ; Heinlein, ; Kaido et al ., ; Kawakami et al ., ) and more complex transport systems (Grangeon et al ., ; Park et al ., ; Tilsner et al ., ). However, viral transport may not involve specific protein–protein binding of MPs to replication complexes (Tilsner et al ., ).…”

Section: Discussionmentioning

confidence: 98%

A novel block of plant virus movement genes

Lazareva

Lezzhov

Komarova

et al. 2016

Molecular Plant Pathology

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Hibiscus green spot virus (HGSV) is a recently discovered and so far poorly characterized bacilliform plant virus with a positive-stranded RNA genome consisting of three RNA species. Here, we demonstrate that the proteins encoded by the ORF2 and ORF3 in HGSV RNA2 are necessary and sufficient to mediate cell-to-cell movement of transport-deficient Potato virus X in Nicotiana benthamiana. These two genes represent a specialized transport module called a 'binary movement block' (BMB), and ORF2 and ORF3 are termed BMB1 and BMB2 genes. In agroinfiltrated epidermal cells of N. benthamiana, green fluorescent protein (GFP)-BMB1 fusion protein was distributed diffusely in the cytoplasm and the nucleus. However, in the presence of BMB2, GFP-BMB1 was directed to cell wall-adjacent elongated bodies at the cell periphery, to cell wall-embedded punctate structures co-localizing with callose deposits at plasmodesmata, and to cells adjacent to the initially transformed cell. Thus, BMB2 can mediate the transport of BMB1 to and through plasmodesmata. In general, our observations support the idea that cell-to-cell trafficking of movement proteins involves an initial delivery to membrane compartments adjacent to plasmodesmata, subsequent entry of the plasmodesmata cavity and, finally, transport to adjacent cells. This process, as an alternative to tubule-based transport, has most likely evolved independently in triple gene block (TGB), double gene block (DGB), BMB and the single gene-coded transport system.

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Section: Discussionmentioning

confidence: 98%

A novel block of plant virus movement genes

Lazareva

Lezzhov

Komarova

et al. 2016

Molecular Plant Pathology

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“…Of central importance to the above processes are viral movement proteins. These proteins facilitate intercellular translocation of viral genomes through plasmodesmata, thus they facilitate spreading of the infection (Grangeon et al, 2013). Moreover, movement proteins also play active roles in the assembly of viral replication complexes (Tilsner et al, 2013).…”

Section: Viral Entry Intracellular Targeting and Intercellular Traffmentioning

confidence: 99%

Biotechnological aspects of cytoskeletal regulation in plants

Komis

Luptovčiak

Doskočilová

et al. 2015

Biotechnology Advances

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“…The perinuclear structure is a collection of numerous 100-nm vesicles and is functionally linked to the peripheral motile ER-derived vesicles (25). These vesicles traffic on transvacuolar strands and actin filaments toward PD and move through these channels to the neighboring cells (26,27).…”

mentioning

confidence: 99%

The Vesicle-Forming 6K ₂ Protein of Turnip Mosaic Virus Interacts with the COPII Coatomer Sec24a for Viral Systemic Infection

Jiang

Patarroyo

Cabanillas

et al. 2015

J Virol

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100

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Positive-sense RNA viruses remodel host cell endomembranes to generate quasi-organelles known as "viral factories" to coordinate diverse viral processes, such as genome translation and replication. It is also becoming clear that enclosing viral RNA (vRNA) complexes within membranous structures is important for virus cell-to-cell spread throughout the host. In plant cells infected by turnip mosaic virus (TuMV), a member of the family Potyviridae, peripheral motile endoplasmic reticulum (ER)-derived viral vesicles are produced that carry the vRNA to plasmodesmata for delivery into adjacent noninfected cells. The viral protein 6K 2 is responsible for the formation of these vesicles, but how 6K 2 is involved in their biogenesis is unknown. We show here that 6K 2 is associated with cellular membranes. Deletion mapping and site-directed mutagenesis experiments defined a soluble N-terminal 12-amino-acid stretch, in particular a potyviral highly conserved tryptophan residue and two lysine residues that were important for vesicle formation. When the tryptophan residue was changed into an alanine in the viral polyprotein, virus replication still took place, albeit at a reduced level, but cell-to-cell movement of the virus was abolished. Yeast (Saccharomyces cerevisiae) two-hybrid and coimmunoprecipitation experiments showed that 6K 2 interacted with Sec24a, a COPII coatomer component. Appropriately, TuMV systemic movement was delayed in an Arabidopsis thaliana mutant line defective in Sec24a. Intercellular movement of TuMV replication vesicles thus requires ER export of 6K 2 , which is mediated by the interaction of the N-terminal domain of the viral protein with Sec24a. IMPORTANCEMany plant viruses remodel the endoplasmic reticulum (ER) to generate vesicles that are associated with the virus replication complex. The viral protein 6K 2 of turnip mosaic virus (TuMV) is known to induce ER-derived vesicles that contain vRNA as well as viral and host proteins required for vRNA synthesis. These vesicles not only sustain vRNA synthesis, they are also involved in the intercellular trafficking of vRNA. In this investigation, we found that the N-terminal soluble domain of 6K 2 is required for ER export of the protein and for the formation of vesicles. ER export is not absolutely required for vRNA replication but is necessary for virus cell-to-cell movement. Furthermore, we found that 6K 2 physically interacts with the COPII coatomer Sec24a and that an Arabidopsis thaliana mutant line with a defective Sec24a shows a delay in the systemic infection by TuMV. P ositive-strand RNA viruses replicate on cellular membranes in order to achieve efficient virus production. These membranous structures have been termed "viral factories" and are associated with virus replication complexes (VRCs) (1, 2). Electron microscopy coupled to tomography has recently been used to get an elaborate three-dimensional view of animal virus-induced membranous structures. For instance, picorna-, corona-, and arteriviruses induce the formation of endopla...

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6K2-induced vesicles can move cell to cell during turnip mosaic virus infection

Cited by 88 publications

References 57 publications

A novel block of plant virus movement genes

A novel block of plant virus movement genes

Biotechnological aspects of cytoskeletal regulation in plants

The Vesicle-Forming 6K ₂ Protein of Turnip Mosaic Virus Interacts with the COPII Coatomer Sec24a for Viral Systemic Infection

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6K2-induced vesicles can move cell to cell during turnip mosaic virus infection

Cited by 88 publications

References 57 publications

A novel block of plant virus movement genes

A novel block of plant virus movement genes

Biotechnological aspects of cytoskeletal regulation in plants

The Vesicle-Forming 6K 2 Protein of Turnip Mosaic Virus Interacts with the COPII Coatomer Sec24a for Viral Systemic Infection

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The Vesicle-Forming 6K ₂ Protein of Turnip Mosaic Virus Interacts with the COPII Coatomer Sec24a for Viral Systemic Infection