Subversion of the salicylic acid signaling pathway by the bipartite begomoviral protein BV1 promotes virus infection and vector preference to virus-infected plants

Abstract

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 vector preference to virus-infected plants. Infection of plants by the bipartite begomovirus, Sri Lankan cassava mosaic virus (SLCMV), 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. Mechanistic explorations in N. benthamiana plants reveal that BV1 downregulates the transcription of BTB/POZ and TAZ domain-containing protein 1 (BT1), a positive regulator of plant SA signal transduction, antiviral defenses and repellence against whitefly. Finally, these principles of plant-bipartite begomovirus interactions are 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.