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Update on Virus-Host Interactions during Movement

Virus-Host Interactions during Movement Processes1
Petra Boevink* and Karl J. Oparka Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, United Kingdom (P.B.); and Institute of Molecular Plant Sciences, University of Edinburgh, Mayfield Road, Edinburgh EH9 3JH, United Kingdom (K.J.O.)

Plant viruses must invade and infect as muchof their hosts as possible to maximize their chances of successful perpetuation. They move cell to cell via plasmodesmata (PD), which they modify to a greater or lesser extent, and to distant parts of the plant through the vascular system. Plant viruses encode one or more nonstructural proteins specifically required for movement within their hosts and many also require their capsid (coat)protein(s). Classically, a viral movement protein (MP) is defined by its ability to increase the plasmodesmal size exclusion limit (SEL) and to move cell to cell; however, other viral proteins that do not themselves move may be essential for the movement process. Viruses that infect plants have developed a variety of strategies to move from cell to cell and are heavily dependent on endogenous host transportsystems during movement, as with all aspects of their life cycles. Rather than attempt to cover all reported virus-host interactions during movement, in this short review, we would like to focus on some common themes that appear in the literature regarding each of the steps involved in viral cell-to-cell movement. These are the use of the endoplasmic reticulum (ER)/actin network as anintracellular transport pathway, recognition of adhesion sites at the cell periphery, modification of PD by alteration of the cell wall structure, heat shock protein (Hsp) 70-class chaperones as potential translocation factors, and regulation of movement. We will discuss how the movement processes of different viruses may utilize these steps in different ways or may not involve all of these steps. Otherreviewers have covered different aspects of short and long distance movement processes, such as the role of the cytoskeleton and the requirement for suppression of host defense responses (for example, Reichel et al., 1999; Oparka, 2004; Waigmann et al., 2004; Voinnet, 2005).
INTRACELLULAR MOVEMENT USING THE ER

With the constant streaming of the plant cell cytoplasm, one could imagine that viral MPswould only
1 This work was supported by the Scottish Executive Environment and Rural Affairs Department. * Corresponding author; e-mail petra.boevink@scri.ac.uk; fax 44– 1382–562426. www.plantphysiol.org/cgi/doi/10.1104/pp.105.066761.

need to go with the flow and bind to PD or other peripheral target sites when they encounter proteins that they recognize. Evidence from numerous studies suggeststhat this is not generally the case, although one cannot discount that a proportion of any MP may arrive at its destination in this way. Cell-to-cell movement is generally an early event in the infection process, occurring in 4 h for tobacco rattle virus in Nicotiana clevelandii or 5 h for tobacco mosaic virus (TMV) in N. tabacum (Fannin and Shaw, 1987; Derrick et al., 1992), and the level of MPproduced in the first few hours is likely to be quite low. Thus, random movement with the cytoplasmic flow may be too inefficient. Many viruses form replication centers enriched in ER (for examples, see Schaad et al., 1997; Heinlein et al., 1998; Mas and Beachy, 1999; Carette et al., 2000; Ritzenthaler et al., 2002), and many viral proteins required for movement appear to be membrane proteins, oftenshown to locate to the ER. For example, the triple gene block (TGB) proteins 2 and 3 of potato mop top virus (PMTV) and potato virus X (PVX) when fused to fluorescent proteins label the ER (Solovyev et al., 2000; Cowan et al., 2002; Krishnamurthy et al., 2003; Mitra et al., 2003; Haupt et al., 2005). Only TGB2 of poa semilatent virus locates to the ER (Solovyev et al., 2000; Zamyatnin et al.,...
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