Plant Virus Movement and the Impact of RNA Silencing

Abstract

Plant virus‐encoded movement proteins support the spread of viral genomes through plasmodesmata and thus represent keys to the molecular mechanisms underlying macromolecular trafficking and intercellular communication. Although Tobacco mosaic virus employs a movement mechanism involving the endoplasmic reticulum (ER)/actin network and microtubules, other viruses interact with membranes of the secretory or endocytic pathways. In addition to replication and targeting of plasmodesmata, efficient virus movement depends on the ability of the virus to interact with the ribonucleic acid (RNA) silencing machinery. Viruses generally encode proteins that suppress silencing and, thus, enhance replication and systemic movement. However, new findings suggest that viruses may also be able to subvert the host silencing machinery to manipulate gene expression in cells to be invaded. Thus, successful virus movement relies on orchestrated interactions of virus‐encoded proteins with the cellular transport and RNA silencing immune systems of the plant.

Key concepts

  • Viruses and other macromolecules are transported through plasmodesmata.

  • Virus movement requires virus‐encoded proteins and interacting host factors.

  • Viruses use different strategies of movement.

  • Viruses interfere with RNA silencing in complex ways.

Keywords: plant virus; plasmodesmata; RNA silencing; membranes; cytoskeleton; movement protein

Figure 1.

PD and viral strategies for movement. (a) Structure of PD. The endoplasmic reticulum (ER) and the plasma membrane (PM) are continuous through the pore. In its central cavity, the ER is connected to the desmotubule (DT). The cytoplasmic space between PM and DT may represent the major pathway for the exchange of molecules between adjacent cells. Proteins embedded in the PM and ER may form microchannels that act as molecular sieves to restrict the free diffusion of macromolecules (CW, cell wall). (b) Virus movement in the form of a nonencapsidated MP:vRNA (vRNP) complex, as exemplified by TMV. The MP of this virus increases the size exclusion limit of PD but otherwise does not induce strong structural changes in PD. (c) Movement of ‘tubule‐forming’ viruses, like GFLV, CPMV or CaMV. The DT is replaced by a tubule consisting of assembled MP subunits and through which virion particles are transported.

Figure 2.

Examples of nonencapsidated and encapsidated viral delivery to PD. (a) Mechanism used by TMV. Nonencapsidated MP:vRNA (vRNP) complexes are part of ER‐associated viral replication complexes (VRCs) that are transported by lateral diffusion in the ER membrane to PD. ER‐associated actin filaments support ER‐associated movement of the complexes in a manner controlled by actin‐associated proteins. Interactions between MP and microtubules (MT) may be involved in the formation of movement–competent complexes and in the guidance of the complexes to PD. CW, cell wall; MT, microtubules; ER, endoplasmic reticulum. (b) Mechanism used by GFLV. This virus replicates in association with the ER and the targeting of the MP to PD for tubule formation depends on the secretory pathway (depicted as Golgi complex with vesicles). This pathway may function in the PD targeting of MP (1) or of a plant protein (2), which acts as a receptor for MP at PD.

Figure 3.

Mechanisms of MP‐mediated delivery of vRNA to PD. (a) and (b) Example of TMV. In cells at the leading front of spreading infection sites in leaves (a) the MP is produced in ER‐associated viral replication complexes (VRCs) where it binds vRNA to form a MP:vRNA (vRNP) complex. The vRNP‐associated VRCs form distinct particles that are released from microtubule anchorage sites for ER‐mediated transport to PD. Release may involve microtubule polymerization and interactions of MP with EB1. The VRCs also release MP for vRNP‐independent transport to PD and interaction with a plasmodesmal receptor. The MP or its interaction with the receptor leads to an increase in the SEL of PD, thus allowing the mobile VRC or VRC‐derived particle to move into the adjacent, noninfected cell. ER‐associated actin filaments provide motility to the ER network and may contribute to ER‐mediated transport with myosin motors. Moreover, the ER‐aligned actin filaments may exert control over ER‐mediated transport by association with actin‐binding proteins. In cells behind the leading front of infection (b) the MP no longer increases the SEL of PD. In addition, the MP accumulates on microtubules, thus interfering with the release and motility of the VRC particle. Accumulation of MP on microtubules is enhanced by interaction with MPB2C, which thus acts as a negative regulator in TMV movement. (c) Example of PVX. PVX encodes three proteins required for the delivery of vRNA to PD. TGBp2 and TGBp3 are integral membrane proteins that form a complex that associates with the TGBp1:vRNA complex for ER/actin‐mediated transport to PD. At the PD, the TGBp1 acts to dilate the PD channel and the TGBp1:vRNA complex is released from pTGB2/pTGB3 for intercellular movement. Subsequently, the TGBp2 and TGBp3 proteins are recycled to the ER via endocytic vesicles.

Figure 4.

Virus movement may involve the spread of virus‐derived siRNAs ahead of the infection front. (a) Dicer cleavage of viral dsRNA produced during replication results in the formation of 21 nt siRNAs which programs AGO‐containing RNA‐induced silencing complexes (RISC) for degradation of cognate viral RNA. The siRNAs spread through PD and associate with RISC complexes in adjacent cells and thus cause immunization of cells to be infected. (b) Dicer‐mediated cleavage of viral dsRNA leads to production of siRNAs that target host mRNA transcripts for degradation, thus resulting in the reprogramming of gene expression in infected cells. Spreading of these siRNAs through PD triggers the degradation of host transcripts in cells ahead of the infection front (subversion). The spread of virus‐ or host‐derived siRNAs and, thus, the subversion of gene expression in cells ahead of the infection front may represent a viral strategy to create an optimal environment in cells to be infected. Modified from Ding and Voinnet , with permission from Elsevier.

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Further Reading

Heinlein M (2008) Microtubules and viral movement. In: Nick P (ed.) Plant Microtubules, Plant Cell Monographs, vol. 11 pp. 141–173. Berlin: Springer.

Heinlein M and Epel BL (2004) Macromolecular transport and signaling through plasmodesmata. International Review of Cytology 235: 93–164.

Morozov SY and Solovyev AG (2003) Triple gene block: modular design of a multifunctional machine for plant virus movement. Journal of General Virology 84: 1351–1366.

Oparka K (ed.) (2005) Plasmodesmata. Annual Plant Reviews, vol. 18. Oxford: Blackwell Publishing.

Ruiz‐Ferrer V and Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annual Review in Plant Biology 60: 485–510.

Waigmann E and Heinlein M (eds) (2007) Viral Transport in Plants. Plant Cell Monographs, vol. 7. Berlin, Heidelberg: Springer.

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Heinlein, Manfred(Dec 2009) Plant Virus Movement and the Impact of RNA Silencing. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021262]