Function of microtubules in intercellular transport of plant virus RNA

Boyko, Vitaly; Ferralli, Jacqueline; Ashby, J.; Schellenbaum, Paul; Heinlein, Manfred

doi:10.1038/35041072

Cited by 161 publications

(193 citation statements)

References 47 publications

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“…We cannot exclude the possibility that ABD2:GFP binding to actin filaments interferes with MP:RFP binding. However, since other studies have demonstrated that the filaments to which MP binds in plant and mammalian cells are microtubules (Heinlein et al, 1995(Heinlein et al, , 1998Boyko et al, 2000aBoyko et al, , 2000bAshby et al, 2006;Ferralli et al, 2006), this possibility appears unlikely. Our observation is consistent with the finding that MP does not bind to actin filaments in mammalian cells (Ferralli et al, 2006), and actin is highly conserved between plants and mammals.…”

Section: Mp Does Not Align To Actin Filamentsmentioning

confidence: 84%

Inhibition of Tobacco Mosaic Virus Movement by Expression of an Actin-Binding Protein

et al. 2009

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The tobacco mosaic virus (TMV) movement protein (MP) required for the cell-to-cell spread of viral RNA interacts with the endoplasmic reticulum (ER) as well as with the cytoskeleton during infection. Whereas associations of MP with ER and microtubules have been intensely investigated, research on the role of actin has been rather scarce. We demonstrate that Nicotiana benthamiana plants transgenic for the actin-binding domain 2 of Arabidopsis (Arabidopsis thaliana) fimbrin (AtFIM1) fused to green fluorescent protein (ABD2:GFP) exhibit a dynamic ABD2:GFP-labeled actin cytoskeleton and myosin-dependent Golgi trafficking. These plants also support the movement of TMV. In contrast, both myosin-dependent Golgi trafficking and TMV movement are dominantly inhibited when ABD2:GFP is expressed transiently. Inhibition is mediated through binding of ABD2:GFP to actin filaments, since TMV movement is restored upon disruption of the ABD2:GFP-labeled actin network with latrunculin B. Latrunculin B shows no significant effect on the spread of TMV infection in either wild-type plants or ABD2:GFP transgenic plants under our treatment conditions. We did not observe any binding of MP along the length of actin filaments.Collectively, these observations demonstrate that TMV movement does not require an intact actomyosin system. Nevertheless, actin-binding proteins appear to have the potential to exert control over TMV movement through the inhibition of myosinassociated protein trafficking along the ER membrane.The mechanism by which plant viruses move from cell to cell and systemically to cause systemic infection has been the subject of intense studies (for review, see

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Section: Mp Does Not Align To Actin Filamentsmentioning

confidence: 84%

Inhibition of Tobacco Mosaic Virus Movement by Expression of an Actin-Binding Protein

et al. 2009

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“…For some viruses, e.g. TMV, the MP interacts with plasmodesmata, increasing their size exclusion limit, and possesses non-specific RNA-binding activity that enables it to form a transportable complex with viral RNA (Wolf et al, 1989;Atkins et al, 1991;Citovsky & Zambryski, 1991 and to microtubules (Boyko et al, 2000). Although TMV CP is essential for long-distance movement, it is not required for cell-to-cell movement (see review by Carrington et al, 1996).…”

Section: Cell-to-cell Movementmentioning

confidence: 99%

Molecular biology of umbraviruses: phantom warriors

Taliansky¹,

Robinson²

2003

Journal of General Virology

110

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The genomes of umbraviruses differ from those of most other viruses in that they do not encode a coat protein, and thus no virus particles are formed in infected plants. Protection of umbraviral RNA outside the host plant, during vector transmission, utilizes the coat protein of an assistor luteovirus, but this review focuses on the mechanisms that compensate for the lack of a coat protein in processes within the host plant. As well as an RNA-dependent RNA polymerase, umbravirus genomes encode two other proteins from almost completely overlapping open reading frames. One of these is a cell-to-cell movement protein that can mediate the transport of homologous and heterologous viral RNAs through plasmodesmata without the participation of a coat protein. The other, the ORF3 protein, binds to viral RNA to form filamentous ribonucleoprotein particles that have elements of helical structure. It serves to stabilize the RNA and facilitates its transport through the vascular system of the plant. It may also be involved in protection of the viral RNA from the plant's defensive RNA-silencing response, although it is not a suppressor of silencing. The ORF3 protein also enters the cell nucleus, specifically targeting the nucleolus. Although the function of this localization is unknown, the ORF3 protein may provide a valuable tool for investigating plant nucleolar function. INTRODUCTIONOne of the main characteristics of most viruses is the formation of virus particles or virions, in which the viral genomic nucleic acid (RNA or DNA) is protected by encapsidation with one or more types of capsid (or coat) protein (CP). In virions, molecules of CP are packed into regular uniform structures based on either helical or icosahedral symmetry. In plant viruses, CP is also involved in transmission by biological vectors and often in the spread of viruses in infected plants. Some plant viruses, such as Cowpea mosaic virus (CPMV; Wellink & van Kammen, 1989), Potato virus X (PVX; Santa Cruz et al., 1998) or Cucumber mosaic virus (CMV; Canto et al., 1997), require CP for movement both through plasmodesmata (cell-to-cell movement) and via the phloem (long-distance movement). Others, such as Tobacco mosaic virus (TMV), require CP for long-distance movement but not for cell-to-cell movement (Carrington et al., 1996). Umbraviruses are distinguished from most other viruses by their lack of a gene for CP, and as a result these viruses do not form conventional virus particles.The name of the genus Umbravirus is derived from the Latin umbra, which means shadow, both in the physical sense and in the metaphorical senses of a phantom or an uninvited guest who comes with an invited one. This name reflects the way in which umbraviruses depend for survival in nature on an assistor virus, which is always a member of the family Luteoviridae (referred to here as a 'luteovirus'). For transmission between plants, CP of luteovirus forms aphidtransmissible hybrid virus particles, encapsidating umbraviral RNA (for review, see Taliansky et al., 2000). In nature,...

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“…To date, MP has been shown to bind TMV RNA (Citovsky et al, 1990(Citovsky et al, , 1992, associate with the cytoskeleton (Heinlein et al, 1995;McLean et al, 1995;Boyko et al, 2000) and endoplasmic reticulum (ER; Heinlein et al, 1998;Reichel and Beachy, 1999), target to plasmodesmata within plant cell walls (Tomenius et al, 1987;Ding et al, 1992a), increase plasmodesmal permeability (Wolf et al, 1989;Waigmann et al, 1994), and undergo negative regulation by phosphorylation (Citovsky et al, 1993;Waigmann et al, 2000;Trutnyeva et al, 2005). To perform many of these functions, TMV MP most likely cooperates with different cellular factors, some of which, such as cell wall pectin methylesterases (PME; Dorokhov et al, 1999;Chen et al, 2000), microtubules (MTs) and actin filaments (Heinlein et al, 1995;McLean et al, 1995;Boyko et al, 2000), and a RIO protein kinase (Yoshioka et al, 2004), are known, while others remain to be discovered. It would be especially interesting to determine whether cellular proteins exist that not only recognize TMV MP but also coreside with it within plasmodesmata.…”

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confidence: 99%

Effects of Calreticulin on Viral Cell-to-Cell Movement

et al. 2005

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Cell-to-cell tobacco mosaic virus movement protein (TMV MP) mediates viral spread between the host cells through plasmodesmata. Although several host factors have been shown to interact with TMV MP, none of them coresides with TMV MP within plasmodesmata. We used affinity purification to isolate a tobacco protein that binds TMV MP and identified it as calreticulin. The interaction between TMV MP and calreticulin was confirmed in vivo and in vitro, and both proteins were shown to share a similar pattern of subcellular localization to plasmodesmata. Elevation of the intracellular levels of calreticulin severely interfered with plasmodesmal targeting of TMV MP, which, instead, was redirected to the microtubular network. Furthermore, in TMV-infected plant tissues overexpressing calreticulin, the inability of TMV MP to reach plasmodesmata substantially impaired cell-to-cell movement of the virus. Collectively, these observations suggest a functional relationship between calreticulin, TMV MP, and viral cell-to-cell movement.Following initial infection (usually by mechanical inoculation), many plant viruses, such as tobacco mosaic virus (TMV), spread from cell to cell through plasmodesmata (for review, see Heinlein, 2002;Waigmann et al., 2004), presumably utilizing the existing cellular pathways of plasmodesmal transport. In the case of TMV, this virus encodes a specific cell-to-cell movement protein (MP), which mediates the transport of the viral genomic RNA through plasmodesmata (Deom et al., 1987). To date, MP has been shown to bind TMV RNA (Citovsky et al., 1990(Citovsky et al., , 1992, associate with the cytoskeleton (Heinlein et al., 1995;McLean et al., 1995;Boyko et al., 2000) and endoplasmic reticulum (ER; Heinlein et al., 1998;Reichel and Beachy, 1999), target to plasmodesmata within plant cell walls (Tomenius et al., 1987;Ding et al., 1992a), increase plasmodesmal permeability (Wolf et al., 1989;Waigmann et al., 1994), and undergo negative regulation by phosphorylation (Citovsky et al., 1993;Waigmann et al., 2000;Trutnyeva et al., 2005). To perform many of these functions, TMV MP most likely cooperates with different cellular factors, some of which, such as cell wall pectin methylesterases (PME; Dorokhov et al., 1999;Chen et al., 2000), microtubules (MTs) and actin filaments (Heinlein et al., 1995;McLean et al., 1995;Boyko et al., 2000), and a RIO protein kinase (Yoshioka et al., 2004), are known, while others remain to be discovered. It would be especially interesting to determine whether cellular proteins exist that not only recognize TMV MP but also coreside with it within plasmodesmata.Using TMV MP as specific ligand in a biochemical purification protocol, we showed that it interacts with plant calreticulin. Calreticulin is a Ca 21 -sequestering protein that is highly conserved between different species, including plants ( Nelson et al., 1997; Borisjuk et al., 1998, and refs. therein;Michalak et al., 1998). Functionally, calreticulin is involved in Ca 21 storage and signaling, chaperone activity, cell ad...

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Function of microtubules in intercellular transport of plant virus RNA

Cited by 161 publications

References 47 publications

Inhibition of Tobacco Mosaic Virus Movement by Expression of an Actin-Binding Protein

Inhibition of Tobacco Mosaic Virus Movement by Expression of an Actin-Binding Protein

Molecular biology of umbraviruses: phantom warriors

Effects of Calreticulin on Viral Cell-to-Cell Movement

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