Background <p>Plant viral movement protein (MP) function is decisive for virus cell-to-cell movement. Often, MPs also induce membrane alterations, which are believed to play a role for the establishment of viral replication compartments. Despite these central roles in virus infection, knowledge of the underlying molecular mechanisms by which MPs cause changes in plasmodesmata (PD) size exclusion limit and contribute to the formation of viral replication compartments remain far from being complete.</p> Methods <p>To further identify host processes subverted by viral MPs, we here characterized the MP of Japanese soil-borne wheat mosaic virus (JSBWMV). We used confocal fluorescence microscopy to study the subcellular localization of MP^JSBWMV and to address its functionality in promoting virus cell-to-cell movement. Using the biochemical and biophysical methods co-immunoprecipitation, fluorescence lifetime imaging, microscale thermophoresis and RNA immunoprecipitation we investigate the capacity of MP^JSBWMV to multimerize and to bind viral and cellular RNAs.</p> Results <p>MP^JSBWMV localized to PD, promoted cell-to-cell movement by complementing a movement-deficient unrelated virus, formed multimers <i>in-vivo</i> and bound to viral RNA with high affinity. Using RNA immunoprecipitation, we identified host RNAs associated with the viral MP. Within the MP-RNA complexes we found RNAs encoding proteins with key functions in membrane modification, signaling, protein folding, and degradation. We propose that binding of MP to these RNAs during infection and regulation of their spatio-temporal translation may represent a mechanism for MPs to achieve PD and host control during replication and movement.</p> Conclusion <p>This study provides new insight into the complex interactions between viral MPs and host cellular processes.</p>