The Cytosolic Nucleoprotein of the Plant-Infecting Bunyavirus Tomato Spotted Wilt Recruits Endoplasmic Reticulum–Resident Proteins to Endoplasmic Reticulum Export Sites

Ribeiro, Daniela; Jung, Maartje; Moling, Sjef; Borst, Jan Willem; Goldbach, Rob; Kormelink, Richard

doi:10.1105/tpc.113.114298

Cited by 25 publications

(32 citation statements)

References 60 publications

(102 reference statements)

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“…These very same studies also unveiled interactions with another chaperone protein, At-4/1, which shares homology with α-helical domains of myosin-, ankyrin-, and kinesin-like proteins (143), which are involved in both intraand extracellular movement (80,86). In situ localization studies on TSWV proteins in plant cells also revealed an actin-dependent intracellular movement of N-RNPs that requires a myosin XI-K motor protein (39,100). In the latter study, and with relevance to possible breeding approaches, plants treated with latrunculin-B, an actin-depolymerizing agent, slowed down TSWV infection in both N. tabacum and Nicotiana benthamiana.…”

Section: Tospovirus-host Plant Interactions: Host Factors and Affectementioning

confidence: 82%

“…During maturation, glycoproteins synthesized at the ER leave from ER export sites (ERES) to the Golgi complex by COPII vesicles. To gather at ERES, an interaction between RNPs and the cytoplasmic tail of Gc suffices, but to escape from ERES to the Golgi complex the additional interaction with the Gn protein is required (98)(99)(100). Without the interaction with RNPs, Gn and Gc are also able to exit from ER as heterodimers, via ERES, to the Golgi complex.…”

Section: A New Taxonomical Framework For the Bunyaviridae?mentioning

confidence: 96%

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Resistance to Tospoviruses in Vegetable Crops: Epidemiological and Molecular Aspects

Turina

Kormelink

Resende

2016

Annu. Rev. Phytopathol.

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During the past three decades, the economic impact of tospoviruses has increased, causing high yield losses in a variety of crops and ornamentals. Owing to the difficulty in combating thrips vectors with insecticides, the best way to limit/prevent tospovirus-induced diseases involves a management strategy that includes virus resistance. This review briefly presents current tospovirus taxonomy, diversity, molecular biology, and cytopathology as an introduction to a more extensive description of the two main resistance genes employed against tospoviruses: the Sw5 gene in tomato and the Tsw in pepper. Natural and experimental resistance-breaking (RB) isolates allowed the identification of the viral avirulence protein triggering each of the two resistance gene products; epidemiology of RB isolates is discussed to reinforce the need for allelic variants and the need to search for new/alternative resistance genes. Ongoing efforts for alternative resistance strategies are described not only for Tomato spotted wilt virus (TSWV) in pepper and tomato but also for other vegetable crops heavily impacted by tospoviruses.

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Section: Tospovirus-host Plant Interactions: Host Factors and Affectementioning

confidence: 82%

Section: A New Taxonomical Framework For the Bunyaviridae?mentioning

confidence: 96%

Resistance to Tospoviruses in Vegetable Crops: Epidemiological and Molecular Aspects

Turina

Kormelink

Resende

2016

Annu. Rev. Phytopathol.

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“…During the membrane envelopment process of the tomato spotted wilt bunyavirus, the viral glycoprotein Gc remains arrested in the ER, but, in the presence of the cytosolic viral nucleoprotein N, its distribution changes from reticular into punctate spots corresponding to ERESs. Concentration of the Gc protein at ERES, which is required for COPII-dependent transport to the Golgi, is mediated by an interaction between its cytoplasmic tail and the N protein (Ribeiro et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

A model for transport of a viral membrane protein through the early secretory pathway: minimal sequence and endoplasmic reticulum lateral mobility requirements

2014

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SUMMARYViral movement proteins exploit host endomembranes and the cytoskeleton to move within the cell via routes that, in some cases, are dependent on the secretory pathway. For example, melon necrotic spot virus p7B, a type II transmembrane protein, leaves the endoplasmic reticulum (ER) through the COPII-dependent Golgi pathway to reach the plasmodesmata. Here we investigated the sequence requirements and putative mechanisms governing p7B transport through the early secretory pathway. Deletion of either the cytoplasmic N-terminal region (CR) or the luminal C-terminal region (LR) led to ER retention, suggesting that they are both essential for ER export. Through alanine-scanning mutagenesis, we identified residues in the CR and LR that are critical for both ER export and for viral cell-to-cell movement. Within the CR, alanine substitution of aspartic and proline residues in the DSSP b-turn motif (D 7 AP 10 A) led to movement of discrete structures along the cortical ER in an actin-dependent manner. In contrast, alanine substitution of a lysine residue in the LR (K 49 A) resulted in a homogenous ER distribution of the movement protein and inhibition of ER-Golgi traffic. Moreover, the ability of p7B to recruit Sar1 to the ER membrane is lost in the D 7 AP 10 A mutant, but enhanced in the K 49 A mutant. In addition, fluorescence recovery after photobleaching revealed that K 49 A but not D 7 AP 10 A dramatically diminished protein lateral mobility. From these data, we propose a model whereby the LR directs actin-dependent mobility toward the cortical ER, where the cytoplasmic DSSP b-turn favors assembly of COPII vesicles for export of p7B from the ER.

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“…NPs of Tomato spotted wilt virus (TSWV), another (-)RNA plant virus, have been reported to form cytoplasmic agglomerates (60,61) and to move along the actin/ER network (16). Since these features are quite similar to those of FMV NP, we considered the possibility that ER streaming also mediates TSWV NP movement.…”

Section: Discussionmentioning

confidence: 99%

Nucleocapsid Protein from Fig Mosaic Virus Forms Cytoplasmic Agglomerates That Are Hauled by Endoplasmic Reticulum Streaming

Ishikawa

Miura

Maejima

et al. 2015

J Virol

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Although many studies have demonstrated intracellular movement of viral proteins or viral replication complexes, little is known about the mechanisms of their motility. In this study, we analyzed the localization and motility of the nucleocapsid protein (NP) of Fig mosaic virus (FMV), a negative-strand RNA virus belonging to the recently established genus Emaravirus. Electron microscopy of FMV-infected cells using immunogold labeling showed that NPs formed cytoplasmic agglomerates that were predominantly enveloped by the endoplasmic reticulum (ER) membrane, while nonenveloped NP agglomerates also localized along the ER. Likewise, transiently expressed NPs formed agglomerates, designated NP bodies (NBs), in close proximity to the ER, as was the case in FMV-infected cells. Subcellular fractionation and electron microscopic analyses of NP-expressing cells revealed that NBs localized in the cytoplasm. Furthermore, we found that NBs moved rapidly with the streaming of the ER in an actomyosin-dependent manner. Brefeldin A treatment at a high concentration to disturb the ER network configuration induced aberrant accumulation of NBs in the perinuclear region, indicating that the ER network configuration is related to NB localization. Dominant negative inhibition of the class XI myosins, XI-1, XI-2, and XI-K, affected both ER streaming and NB movement in a similar pattern. Taken together, these results showed that NBs localize in the cytoplasm but in close proximity to the ER membrane to form enveloped particles and that this causes passive movements of cytoplasmic NBs by ER streaming. IMPORTANCEIntracellular trafficking is a primary and essential step for the cell-to-cell movement of viruses. To date, many studies have demonstrated the rapid intracellular movement of viral factors but have failed to provide evidence for the mechanism or biological significance of this motility. Here, we observed that agglomerates of nucleocapsid protein (NP) moved rapidly throughout the cell, and we performed live imaging and ultrastructural analysis to identify the mechanism of motility. We provide evidence that cytoplasmic protein agglomerates were passively dragged by actomyosin-mediated streaming of the endoplasmic reticulum (ER) in plant cells. In virus-infected cells, NP agglomerates were surrounded by the ER membranes, indicating that NP agglomerates form the basis of enveloped virus particles in close proximity to the ER. Our work provides a sophisticated model of macromolecular trafficking in plant cells and improves our understanding of the formation of enveloped particles of negative-strand RNA viruses.T he actomyosin system is essential for the intracellular transport of endomembranes and other macromolecular complexes and for the spatial arrangement of organelles (1). Trafficking along actin filaments is primarily mediated by molecular motor myosins. Myosins of Arabidopsis thaliana are divided into the two subfamilies, class VIII and class XI myosins. Class XI myosins provide the motive force for the movement of org...

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The Cytosolic Nucleoprotein of the Plant-Infecting Bunyavirus Tomato Spotted Wilt Recruits Endoplasmic Reticulum–Resident Proteins to Endoplasmic Reticulum Export Sites

Cited by 25 publications

References 60 publications

Resistance to Tospoviruses in Vegetable Crops: Epidemiological and Molecular Aspects

Resistance to Tospoviruses in Vegetable Crops: Epidemiological and Molecular Aspects

A model for transport of a viral membrane protein through the early secretory pathway: minimal sequence and endoplasmic reticulum lateral mobility requirements

Nucleocapsid Protein from Fig Mosaic Virus Forms Cytoplasmic Agglomerates That Are Hauled by Endoplasmic Reticulum Streaming

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