Subversion of the salicylic acid-signaling pathway by the bipartite begomoviral protein BV1 promotes virus infection and vector-mediated transmission

The outbreak of vector-borne plant viruses entails both efficient in planta virus infection and productive vector-mediated transmission. Yet, the factors that concurrently regulate these two key viral traits remain understudied. Here we examine the role of viral proteins and the salicylic acid (SA)-signaling pathway in modulating virus infection and transmission. Infection of plants by the bipartite begomovirus, Sri Lankan cassava mosaic virus (SLCMV), in plants dramatically induces the accumulation of SA, a positive regulator of antiviral defense. As countermeasures, SLCMV DNA-B and the BV1 protein encoded therein interfere with SA-induced antiviral defenses and SA signal transduction. Furthermore, whilst SA induces plant repellence to whitefly vectors, this repellence is mitigated by SLCMV DNA-B and BV1. Mechanistically, BV1 downregulates the transcription of BTB/POZ and TAZ domain-containing protein 1 (BT1), a positive regulator of SA signal transduction, plant antiviral defenses and repellence against whitefly. Finally, these principles of plant-bipartite begomovirus interactions appear to be conserved as they were also documented for another bipartite begomovirus. Together, our data highlight the role of virus-SA interplay in enabling competent interactions among plant hosts, bipartite begomoviruses and their whitefly vectors, and advance our understanding of the molecular mechanisms that promote the persistence of vector-borne plant viruses.