Phosphorylation of tobacco mosaic virus cell-to-cell movement protein by a developmentally regulated plant cell wall-associated protein kinase.

Cell–to–cell movement of tobacco mosaic virus (TMV) is used to illustrate macromolecular traffic through plant intercellular connections, the plasmodesmata. This transport process is mediated by a specialized viral movement protein, P30. In the initially infected cell, P30 is produced by transcription of a subgenomic RNA derived from the invading virus. Presumably, P30 then associates with a certain proportion of the viral RNA molecules, sequestering them from replication and mediating their transport into neighbouring uninfected host cells. This nucleoprotein complex is targeted to plasmodesmata, possibly via interaction with the host cell cytoskeleton. Prior to passage through a plasmodesma, the plasmodesmal channel is dilated by the movement protein. It is proposed that targeting of P30–TMV RNA complexes to plasmodesmata involves binding to a specific cell wall–associated receptor molecule. In addition, a cell wall–associated protein kinase, phosphorylates P30 at its carboxy–terminus and minimizes P30–induced interference with plasmodesmatal permeability during viral infection.

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Identification of a Functional Plasmodesmal Localization Signal in a Plant Viral Cell-To-Cell-Movement Protein

mBio ◽

10.1128/mbio.02052-15 ◽

2016 ◽

Vol 7 (1) ◽

Cited By ~ 15

Author(s):

Cheng Yuan ◽

Sondra G. Lazarowitz ◽

Vitaly Citovsky

Keyword(s):

Tobacco Mosaic Virus ◽

Mosaic Virus ◽

Plant Cell ◽

Movement Protein ◽

Protein Sorting ◽

Cell Movement ◽

Cell Transport ◽

Localization Signal ◽

Functional Features ◽

Intercellular Connections

ABSTRACT Our fundamental knowledge of the protein-sorting pathways required for plant cell-to-cell trafficking and communication via the intercellular connections termed plasmodesmata has been severely limited by the paucity of plasmodesmal targeting sequences that have been identified to date. To address this limitation, we have identified the plasmodesmal localization signal (PLS) in the Tobacco mosaic virus (TMV) cell-to-cell-movement protein (MP), which has emerged as the paradigm for dissecting the molecular details of cell-to-cell transport through plasmodesmata. We report here the identification of a bona fide functional TMV MP PLS, which encompasses amino acid residues between positions 1 and 50, with residues Val-4 and Phe-14 potentially representing critical sites for PLS function that most likely affect protein conformation or protein interactions. We then demonstrated that this PLS is both necessary and sufficient for protein targeting to plasmodesmata. Importantly, as TMV MP traffics to plasmodesmata by a mechanism that is distinct from those of the three plant cell proteins in which PLSs have been reported, our findings provide important new insights to expand our understanding of protein-sorting pathways to plasmodesmata. IMPORTANCE The science of virology began with the discovery of Tobacco mosaic virus (TMV). Since then, TMV has served as an experimental and conceptual model for studies of viruses and dissection of virus-host interactions. Indeed, the TMV cell-to-cell-movement protein (MP) has emerged as the paradigm for dissecting the molecular details of cell-to-cell transport through the plant intercellular connections termed plasmodesmata. However, one of the most fundamental and key functional features of TMV MP, its putative plasmodesmal localization signal (PLS), has not been identified. Here, we fill this gap in our knowledge and identify the TMV MP PLS.

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Acquired Resistance in Hypersensitive Tobacco against Tobacco Mosaic Virus, Induced by Plant Cell Wall Components

Journal of Phytopathology ◽

10.1111/j.1439-0434.1985.tb04327.x ◽

1985 ◽

Vol 113 (2) ◽

pp. 165-170 ◽

Cited By ~ 14

Author(s):

P. W. Modderman ◽

C. P. Schot ◽

F. M. Klis ◽

D. H. Wieringa-Brants

Keyword(s):

Cell Wall ◽

Tobacco Mosaic Virus ◽

Mosaic Virus ◽

Plant Cell ◽

Plant Cell Wall ◽

Acquired Resistance ◽

Cell Wall Components ◽

Wall Components

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Plasmodesmata and intercellular transport of viral RNA

Biochemical Society Transactions ◽

10.1042/bst0350142 ◽

2007 ◽

Vol 35 (1) ◽

pp. 142-145 ◽

Cited By ~ 30

Author(s):

C. Hofmann ◽

A. Sambade ◽

M. Heinlein

Keyword(s):

Cell Wall ◽

Tobacco Mosaic Virus ◽

Mosaic Virus ◽

Plant Cell Wall ◽

Movement Protein ◽

Cell Communication ◽

Viral Rna ◽

Intercellular Transport ◽

Cytoplasmic Bridges ◽

Spread Of Infection

Cell-to-cell communication in plants involves the symplastic trafficking of informational protein and RNA macromolecules through cytoplasmic bridges in the plant cell wall known as plasmodesmata. Viruses exploit this route for the spread of infection and are used as a model to study the mechanisms by which macromolecules are targeted to the pore. Studies using tobacco mosaic virus have led to the identification of host components that participate in plasmodesmal targeting of viral RNA and movement protein.

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Actin Cytoskeleton Is Involved in Targeting of a Viral Hsp70 Homolog to the Cell Periphery

Journal of Virology ◽

10.1128/jvi.79.22.14421-14428.2005 ◽

2005 ◽

Vol 79 (22) ◽

pp. 14421-14428 ◽

Cited By ~ 62

Author(s):

Alexey I. Prokhnevsky ◽

Valera V. Peremyslov ◽

Valerian V. Dolja

Keyword(s):

Actin Cytoskeleton ◽

Tobacco Mosaic Virus ◽

Mosaic Virus ◽

Movement Protein ◽

Fluorescent Proteins ◽

Cell Movement ◽

Plant Viruses ◽

Cell Periphery ◽

Virus Particles ◽

Shock Proteins

ABSTRACT The cell-to-cell movement of plant viruses involves translocation of virus particles or nucleoproteins to and through the plasmodesmata (PDs). As we have shown previously, the movement of the Beet yellows virus requires the concerted action of five viral proteins including a homolog of cellular ∼70-kDa heat shock proteins (Hsp70h). Hsp70h is an integral component of the virus particles and is also found in PDs of the infected cells. Here we investigate subcellular distribution of Hsp70h using transient expression of Hsp70h fused to three spectrally distinct fluorescent proteins. We found that fluorophore-tagged Hsp70h forms motile granules that are associated with actin microfilaments, but not with microtubules. In addition, immobile granules were observed at the cell periphery. A pairwise appearance of these granules at the opposite sides of cell walls and their colocalization with the movement protein of Tobacco mosaic virus indicated an association of Hsp70h with PDs. Treatment with various cytoskeleton-specific drugs revealed that the intact actomyosin motility system is required for trafficking of Hsp70h in cytosol and its targeting to PDs. In contrast, none of the drugs interfered with the PD localization of Tobacco mosaic virus movement protein. Collectively, these findings suggest that Hsp70h is translocated and anchored to PDs in association with the actin cytoskeleton.

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Cell wall localization of Red clover necrotic mosaic virus movement protein is required for cell-to-cell movement

Virology ◽

10.1016/j.virol.2004.12.019 ◽

2005 ◽

Vol 333 (1) ◽

pp. 10-21 ◽

Cited By ~ 18

Author(s):

Douglas Tremblay ◽

Andrew A. Vaewhongs ◽

Katherine A. Turner ◽

Tim L. Sit ◽

Steven A. Lommel

Keyword(s):

Cell Wall ◽

Mosaic Virus ◽

Movement Protein ◽

Cell Movement ◽

Red Clover ◽

Virus Movement

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Mimicking carboxyterminal phosphorylation differentially effects subcellular distribution and cell-to-cell movement of Tobacco mosaic virus movement protein

Virology ◽

10.1016/j.virol.2004.11.040 ◽

2005 ◽

Vol 332 (2) ◽

pp. 563-577 ◽

Cited By ~ 32

Author(s):

Kateryna Trutnyeva ◽

Radostina Bachmaier ◽

Elisabeth Waigmann

Keyword(s):

Tobacco Mosaic Virus ◽

Mosaic Virus ◽

Subcellular Distribution ◽

Movement Protein ◽

Cell Movement ◽

Virus Movement

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Dysfunctionality of a tobacco mosaic virus movement protein mutant mimicking threonine 104 phosphorylation

Journal of General Virology ◽

10.1099/vir.0.18972-0 ◽

2003 ◽

Vol 84 (3) ◽

pp. 727-732 ◽

Cited By ~ 23

Author(s):

E. M. Karger ◽

O. Yu. Frolova ◽

N. V. Fedorova ◽

L. A. Baratova ◽

T. V. Ovchinnikova ◽

...

Keyword(s):

Endoplasmic Reticulum ◽

Tobacco Mosaic Virus ◽

Mosaic Virus ◽

Movement Protein ◽

Cell Movement ◽

Specific Protein ◽

Virus Movement ◽

Wild Type ◽

Molecular Masses

Replication of tobacco mosaic virus (TMV) is connected with endoplasmic reticulum (ER)-associated membranes at early stages of infection. This study reports that TMV movement protein (MP)-specific protein kinases (PKs) associated with the ER of tobacco were capable of phosphorylating Thr104 in TMV MP. The MP-specific PKs with apparent molecular masses of about 45–50 kDa and 38 kDa were revealed by gel PK assays. Two types of mutations were introduced in TMV MP gene of wild-type TMV U1 genome to substitute Thr104 by neutral Ala or by negatively charged Asp. Mutation of Thr104 to Ala did not affect the size of necrotic lesions induced by the mutant virus in Nicotiana tabacum Xanthi nc. plants. Conversely, mutation of Thr to Asp mimicking Thr104 phosphorylation strongly inhibited cell-to-cell movement. The possible role of Thr104 phosphorylation in TMV MP function is discussed.

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