Replication and trafficking of a plant virus are coupled at the entrances of plasmodesmata

Tilsner, Jens; Linnik, Olga; Louveaux, Marion; Roberts, I. M.; Chapman, Sean; Oparka, Karl J.

doi:10.1083/jcb.201304003

Cited by 148 publications

(193 citation statements)

References 69 publications

(186 reference statements)

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“…Pumilio-based RNA imaging has enabled subcellular detection of the mRNAs of mitochondrial NADH dehydrogenase and -actin, as well as retroviral RNA in mammalian cultured cells (20)(21)(22)(23), and of the genomes of Tobacco mosaic virus, Potato virus X and Turnip mosaic virus in live plant tissue (24)(25)(26)(27). Of particular relevance to the topic of this volume, Pumilio-based RNA imaging has recently shown that Potato virus X is present in membrane structures at the entrances of plasmodesmata that also contain the viral replicase (27).…”

Section: Rna-binding Domain Of Pumilio Proteinsmentioning

confidence: 99%

“…This principle is the only form of Pumilio-based RNA imaging so far applied in plants ( [24][25][26][27].…”

Section: Choice Of Reporter Systemmentioning

confidence: 99%

“…PUM-BiFC imaging can be used in two different modes: PUMHDs can be modified to bind to the native RNA of interest (20,21,(23)(24)(25), or the RNA can be tagged with recognition motifs of previously characterised PUMHD variants (22,24,26,27,33) (Table 1). As described in the introduction, leaving the RNA unmodified has the advantage of avoiding potential RNA processing and localisation artefacts that could be caused by a tag, and by the expression of the tagged construct from an artificial genomic context.…”

Section: Choice Of Target Sequences and Pumhd Variantsmentioning

confidence: 99%

“…In principle, PUM-BiFC reporter constructs can be stably expressed, but so far all Pumilio-based RNA imaging in plants has been done with transient expression systems (agroinfiltration or microprojectile bombardment) (24)(25)(26)(27). Since nonspecific background fluorescence increases with the accumulation of the PUM-BiFC fusions, transient expression may be preferable as it permits limiting background fluorescence by reducing the expression time (see 3.3.…”

Section: Choice Of Expression Systemmentioning

confidence: 99%

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Pumilio-Based RNA In Vivo Imaging

Tilsner

2014

Methods in Molecular Biology

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SummarySubcellular, sequence-specific detection of RNA in vivo is a powerful tool to study the macromolecular transport that occurs through plasmodesmata. The RNA binding domain of Pumilio proteins can be engineered to bind RNA sequences of choice and fused to fluorescent proteins for RNA imaging. This chapter describes the construction of a Pumilio-based imaging system to track the RNA of Tobacco mosaic virus in vivo, and practical aspects of RNA live-cell imaging.

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Section: Rna-binding Domain Of Pumilio Proteinsmentioning

confidence: 99%

“…This principle is the only form of Pumilio-based RNA imaging so far applied in plants ( [24][25][26][27].…”

Section: Choice Of Reporter Systemmentioning

confidence: 99%

Section: Choice Of Target Sequences and Pumhd Variantsmentioning

confidence: 99%

Section: Choice Of Expression Systemmentioning

confidence: 99%

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Pumilio-Based RNA In Vivo Imaging

Tilsner

2014

Methods in Molecular Biology

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“…One can speculate that after TGB1-induced structural transition this protein region might also appear to be located on the outer surface of transport-competent TGB1-bound virions similar to the localization of C-terminal PVX CP region to the outer virion surface upon protease treatment (Baratova et al, 1992), and to directly participate in interactions required for viral movement. It should be kept in mind that potexvirus cell-to-cell transport is coupled with the replication of viral RNA (Tilsner et al, 2013). Since an Ala residue in the C-terminal region of BaMV CP has been found to be involved in the CP interaction with viral replicase, and point mutations of this residue in both BaMV and Foxtail mosaic virus CPs result in the virus being unable to move from cell to cell , it is conceivable that the viral replicase binds to the CP Ctermini exposed on one end of the virion, competing therefore with the TGB1 protein.…”

Section: Role Of Virions In Cell-to-cell Transport Of Filamentous Virmentioning

confidence: 99%

Helical capsids of plant viruses: architecture with structural lability

Solovyev

Makarov

2016

Journal of General Virology

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Capsids of numerous filamentous and rod-shaped plant viruses possess helical symmetry. In positive-stranded RNA viruses, helical capsids are typically composed of many identical subunits of the viral capsid protein (CP), encapsidating a molecule of viral genomic RNA. Current progress in structural studies of helical plant viruses has revealed differences between filamentous and rod-shaped viruses, both in structural folds of their CPs and in the interactions of CP molecules in their capsids. Many filamentous and rod-shaped viruses have functionally similar lateral inter-subunit contacts on the outer virion surface. Additionally, the extreme Nterminal CP region in filamentous viruses is intrinsically disordered. Taken together, the available data establish a link between the structural features of molecular interactions of CP molecules and the physical properties of helical virions ranging from rigidity to flexibility. Overall, the structure of helical plant viruses is significantly more labile than previously thought, often allowing structural transitions, remodelling and the existence of alternative structural forms of virions. These properties of virions are believed to be functionally significant at certain stages of the viral life cycle, such as during translational activation and cell-to-cell transport. In this review, we discuss structural and functional features of filamentous and rod-shaped virions, highlight their shared features and differences, and lay emphasis on the relationships between the molecular structure of viral capsids and their properties including virion shape, lability and capability of structural remodelling.

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Plasmodesmata

Faulkner

Oparka

2016

Encyclopedia of Life Sciences

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Plasmodesmata are plasma membrane‐lined pores that span the adjoining walls of plant cells. They permit the intercellular passage of molecules and signals and play a central role in plant physiology and development. Evidence suggests that small molecules can pass from cell to cell by passive diffusion and that this is controlled by regulation of the pore itself. This contributes to processes such as the transport of sugars between cells and tissues. Many endogenous plant proteins and ribonucleic acid (RNA)‐based signals also utilise plasmodesmata for cell‐to‐cell and long‐distance movement. Recent data suggests that plasmodesmata are tightly controlled during development and in response to environmental changes. There is increasing evidence that this regulation is controlled by proteins that have specific plasmodesmata‐associated functions in stimulus perception and signalling. In addition, many viruses exploit plasmodesmata for cell‐to‐cell spread during infection and their encoded viral movement proteins manipulate the pores to facilitate this process. Key Concepts Plant cells are connected to each other by cytoplasmic bridges called plasmodesmata. The continuous interconnected cytoplasm in plants is referred to as the symplasm. A tube of endoplasmic reticulum passes through plasmodesmata and connects the endoplasmic reticulum of neighbouring cells, thus providing endomembrane continuity between cells. Primary plasmodesmata are formed at cytokinesis when strands of endoplasmic reticulum are trapped between fusing vesicles in the developing cell wall. Secondary plasmodesmata are formed across existing cell walls, including those at graft unions, and usually arise immediately adjacent to existing plasmodesmata. Molecules smaller than the size exclusion limit (SEL) of plasmodesmata are able to move freely through the cytoplasmic channel of plasmodesmata by simple diffusion. The SEL of plasmodesmata may increase or decrease to allow changes in plasmodesmatal conductance. This may occur under different conditions, for example, in response to intracellular factors such as cytoplasmic calcium levels or pathogen perception. Some endogenous proteins and some movement proteins encoded by plant viruses are able to increase the SEL of plasmodesmata to facilitate their own passage into neighbouring cells. This enables these proteins to function in cells in which they are not normally expressed. Groups of cells may be connected by plasmodesmata that share an SEL different to that of neighbouring cells. These regions of cells are called symplasmic domains. Some proteins and RNA molecules pass into the plant's translocation stream and move over long distances. These macromolecules traffic through the plasmodesmata that join sieve elements (SE) and companion cells within the phloem. These macromolecules may have a site of action distant to their site of expression and synthesis.

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Replication and trafficking of a plant virus are coupled at the entrances of plasmodesmata

Abstract: Plant virus movement proteins compartmentalize replication complexes at plasmodesmata for localized RNA synthesis and directional trafficking of the virus between cells.

Cited by 148 publications

References 69 publications

Pumilio-Based RNA In Vivo Imaging

Pumilio-Based RNA In Vivo Imaging

Helical capsids of plant viruses: architecture with structural lability

Plasmodesmata

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