Limits...
Myosins VIII and XI play distinct roles in reproduction and transport of tobacco mosaic virus.

Amari K, Di Donato M, Dolja VV, Heinlein M - PLoS Pathog. (2014)

Bottom Line: The inactivation of myosin XI-2 but not of myosin XI-K affected the localization pattern of the 126k replicase subunit and the level of TMV accumulation.The inhibition of myosins VIII-1, VIII-2 and VIII-B abolished MP localization to PD and caused its retention at the plasma membrane.Thus, TMV appears to recruit distinct myosins for different steps in the cell-to-cell spread of the infection.

View Article: PubMed Central - PubMed

Affiliation: Zürich-Basel Plant Science Center, Botany, Department of Environmental Sciences, University of Basel, Basel, Switzerland.

ABSTRACT
Viruses are obligatory parasites that depend on host cellular factors for their replication as well as for their local and systemic movement to establish infection. Although myosin motors are thought to contribute to plant virus infection, their exact roles in the specific infection steps have not been addressed. Here we investigated the replication, cell-to-cell and systemic spread of Tobacco mosaic virus (TMV) using dominant negative inhibition of myosin activity. We found that interference with the functions of three class VIII myosins and two class XI myosins significantly reduced the local and long-distance transport of the virus. We further determined that the inactivation of myosins XI-2 and XI-K affected the structure and dynamic behavior of the ER leading to aggregation of the viral movement protein (MP) and to a delay in the MP accumulation in plasmodesmata (PD). The inactivation of myosin XI-2 but not of myosin XI-K affected the localization pattern of the 126k replicase subunit and the level of TMV accumulation. The inhibition of myosins VIII-1, VIII-2 and VIII-B abolished MP localization to PD and caused its retention at the plasma membrane. These results suggest that class XI myosins contribute to the viral propagation and intracellular trafficking, whereas myosins VIII are specifically required for the MP targeting to and virus movement through the PD. Thus, TMV appears to recruit distinct myosins for different steps in the cell-to-cell spread of the infection.

Show MeSH

Related in: MedlinePlus

Model illustrating the role of the actomyosin system in the intra- and intercellular movement of TMV.Myosins XI-2 and XI-K provide motility to the ER and facilitate the concentration of VRCs at cortical ER sites in the vicinity of the PM (a). VRCs are concentrated and stabilized by the 126k through myosin XI-2 function to enhance viral replication and silencing suppression (a). Class VIII myosins are involved in the targeting of the MP/VRCs from the cortical ER sites to the PM and subsequently to PD. This process may involve endocytic recycling (b), diffusion of the MP/VRC along the PM (c), stabilization of MP/VRC at PD (d) and active transport through the channel into the adjacent cell (e).
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4199776&req=5

ppat-1004448-g010: Model illustrating the role of the actomyosin system in the intra- and intercellular movement of TMV.Myosins XI-2 and XI-K provide motility to the ER and facilitate the concentration of VRCs at cortical ER sites in the vicinity of the PM (a). VRCs are concentrated and stabilized by the 126k through myosin XI-2 function to enhance viral replication and silencing suppression (a). Class VIII myosins are involved in the targeting of the MP/VRCs from the cortical ER sites to the PM and subsequently to PD. This process may involve endocytic recycling (b), diffusion of the MP/VRC along the PM (c), stabilization of MP/VRC at PD (d) and active transport through the channel into the adjacent cell (e).

Mentions: Together with previous studies, our work supports a more detailed mechanistic model of the interplay between TMV and the actomyosin system (Figure 10). This model proposes that the myosins XI-2 and XI-K mobilize the dynamic ER-actin network and facilitate concentration of VRCs at C-MERs, specific sites of the cortical ER adjacent to the PM. The 126k protein stabilizes the VRC cluster at these sites with support of myosin XI-2 and thus enhances viral amplification. An endocytic recyling pathway that links the cortical ER-associated VRC clusters to the PM domain at or near PD, maintains the localization of MP within this domain and thus facilitates directed macromolecular transport from the ER to PD and into the adjacent cell. Myosin VIII is a principal driver of these final steps of viral transport between cells that activates endosomal trafficking and also prevents the distribution of the MP along the PM. In conclusion, our data show that individual myosins VIII and XI provide distinct functional contributions to specific steps in TMV intra- and intercellular movement.


Myosins VIII and XI play distinct roles in reproduction and transport of tobacco mosaic virus.

Amari K, Di Donato M, Dolja VV, Heinlein M - PLoS Pathog. (2014)

Model illustrating the role of the actomyosin system in the intra- and intercellular movement of TMV.Myosins XI-2 and XI-K provide motility to the ER and facilitate the concentration of VRCs at cortical ER sites in the vicinity of the PM (a). VRCs are concentrated and stabilized by the 126k through myosin XI-2 function to enhance viral replication and silencing suppression (a). Class VIII myosins are involved in the targeting of the MP/VRCs from the cortical ER sites to the PM and subsequently to PD. This process may involve endocytic recycling (b), diffusion of the MP/VRC along the PM (c), stabilization of MP/VRC at PD (d) and active transport through the channel into the adjacent cell (e).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4199776&req=5

ppat-1004448-g010: Model illustrating the role of the actomyosin system in the intra- and intercellular movement of TMV.Myosins XI-2 and XI-K provide motility to the ER and facilitate the concentration of VRCs at cortical ER sites in the vicinity of the PM (a). VRCs are concentrated and stabilized by the 126k through myosin XI-2 function to enhance viral replication and silencing suppression (a). Class VIII myosins are involved in the targeting of the MP/VRCs from the cortical ER sites to the PM and subsequently to PD. This process may involve endocytic recycling (b), diffusion of the MP/VRC along the PM (c), stabilization of MP/VRC at PD (d) and active transport through the channel into the adjacent cell (e).
Mentions: Together with previous studies, our work supports a more detailed mechanistic model of the interplay between TMV and the actomyosin system (Figure 10). This model proposes that the myosins XI-2 and XI-K mobilize the dynamic ER-actin network and facilitate concentration of VRCs at C-MERs, specific sites of the cortical ER adjacent to the PM. The 126k protein stabilizes the VRC cluster at these sites with support of myosin XI-2 and thus enhances viral amplification. An endocytic recyling pathway that links the cortical ER-associated VRC clusters to the PM domain at or near PD, maintains the localization of MP within this domain and thus facilitates directed macromolecular transport from the ER to PD and into the adjacent cell. Myosin VIII is a principal driver of these final steps of viral transport between cells that activates endosomal trafficking and also prevents the distribution of the MP along the PM. In conclusion, our data show that individual myosins VIII and XI provide distinct functional contributions to specific steps in TMV intra- and intercellular movement.

Bottom Line: The inactivation of myosin XI-2 but not of myosin XI-K affected the localization pattern of the 126k replicase subunit and the level of TMV accumulation.The inhibition of myosins VIII-1, VIII-2 and VIII-B abolished MP localization to PD and caused its retention at the plasma membrane.Thus, TMV appears to recruit distinct myosins for different steps in the cell-to-cell spread of the infection.

View Article: PubMed Central - PubMed

Affiliation: Zürich-Basel Plant Science Center, Botany, Department of Environmental Sciences, University of Basel, Basel, Switzerland.

ABSTRACT
Viruses are obligatory parasites that depend on host cellular factors for their replication as well as for their local and systemic movement to establish infection. Although myosin motors are thought to contribute to plant virus infection, their exact roles in the specific infection steps have not been addressed. Here we investigated the replication, cell-to-cell and systemic spread of Tobacco mosaic virus (TMV) using dominant negative inhibition of myosin activity. We found that interference with the functions of three class VIII myosins and two class XI myosins significantly reduced the local and long-distance transport of the virus. We further determined that the inactivation of myosins XI-2 and XI-K affected the structure and dynamic behavior of the ER leading to aggregation of the viral movement protein (MP) and to a delay in the MP accumulation in plasmodesmata (PD). The inactivation of myosin XI-2 but not of myosin XI-K affected the localization pattern of the 126k replicase subunit and the level of TMV accumulation. The inhibition of myosins VIII-1, VIII-2 and VIII-B abolished MP localization to PD and caused its retention at the plasma membrane. These results suggest that class XI myosins contribute to the viral propagation and intracellular trafficking, whereas myosins VIII are specifically required for the MP targeting to and virus movement through the PD. Thus, TMV appears to recruit distinct myosins for different steps in the cell-to-cell spread of the infection.

Show MeSH
Related in: MedlinePlus