Interactions between Cucumber mosaic virus proteins and host proteins

Abstract

Cucumber mosaic virus (CMV) infects over a thousand plant species including many crops. CMV is mainly transmitted between plants by aphids, insects with probing mouthparts that introduce virus particles directly into host cells. The 2b viral suppressor of RNA silencing (VSR) encoded by CMV is a potent counterdefence and pathogenicity factor that inhibits antiviral silencing by titration of short double-stranded RNAs. The 2b VSR not only influences infection, but also host interactions with one of the main insect vectors of CMV, the generalist aphid Myzus persicae. The 2b protein disrupts microRNA-mediated regulation of host gene expression by binding ARGONAUTE 1 (AGO1). In Arabidopsis, complete inhibition of AGO1 activity is counterproductive to CMV since this triggers antibiosis against aphids and stimulates resistance mechanisms by AGO2. The CMV 1a protein (a replicase component) is able to moderate antibiosis induction by the 2b VSR. This ensures that aphid vectors are deterred from feeding but not poisoned when they feed on CMV-infected Arabidopsis plants. I found that the CMV 1a protein is able to directly inhibit the 2b-AGO1 interaction. By binding 2b protein molecules and sequestering them in processing-bodies, the 1a protein decreases the proportion of 2b protein molecules available for binding AGO1. This ameliorates 2b-induced viral symptoms and moderates the induction of aphid resistance. However, the 1a-2b protein interaction does not inhibit the VSR activity of the 2b protein. The interaction between the CMV 1a and 2b proteins represents a novel viral regulatory system for VSRs. The finding also provides a mechanism that may explain how CMV, and possibly other viruses, modulate symptom induction and manipulate host-vector interactions.