The βC1 protein encoded in betasatellites promotes begomovirus-whitefly coexistence by subverting vector infestation-induced plant antiviral defenses

Abstract

The transmission of many plant viruses depends on arthropod vectors, which acquire viruses while feeding on infected plants and subsequently inoculate un-infected hosts. Efficient virus acquisition, particularly for persistently transmitted viruses, requires sustained vector feeding on infected plants. However, how vector infestation influences plant-virus interactions and the modulation of these impacts by viral factors remains poorly understood. Here, we show that whitefly infestation on begomovirus-infected plants activates host antiviral defenses through inducing salicylic acid (SA) accumulation. Betasatellites associated with begomoviruses, specifically the βC1 protein encoded therein, suppress these whitefly-induced defenses by interfering with SA accumulation and signaling. Mechanistically, βC1 interacts with Nicotiana benthamiana ENHANCED DISEASE SUSCEPTIBILITY 1 (NbEDS1), disrupting its interaction with NbPAD4 to reduce SA accumulation. Additionally, βC1 interferes with the association between NbEDS1 and NbTGA2, thereby attenuating NbTGA2-mediated transcription of SA-responsive genes. Our findings unravel a novel mechanism by which βC1 promotes begomovirus-whitefly compatibility, offering new insights into insect vector-mediated transmission of plant viruses.