A singleVerticillium dahliaeeffector determines pathogenicity on tomato by targeting auxin response factors

Abstract

SUMMARYVerticillium dahliaeis a xylem-invading fungal pathogen that causes devastating vascular wilt diseases on hundreds of plant hosts, including tomato (Solanum lycopersicum). Although individualV. dahliaestrains are typically characterized by their broad host range, differential pathogenicity occurs on nearly all hosts. Currently, the molecular basis underlying such pathogenicity differences remains unknown. We used comparative genomics to identify a single effector gene that specifically occurs in tomato-pathogenicV. dahliaestrains and is expressed during tomato colonization. Functional analyses showed that this Tom1 effector governs pathogenicity on tomato, asTom1deletion prohibited tomato colonization, while introduction ofTom1into non-pathogenicV. dahliaeor into saprophytic sister speciesV. tricorpusandV. nubilumresulted in disease. Through proteomics-based approaches, auxin response factors (ARFs) were identified asin plantatargets of Tom1. Intriguingly, repression ofSlARF2aexpression by virus-induced gene silencing fully impairedV. dahliaecolonization of tomato, solidifying its role as susceptibility target.Collectively, our findings indicate that a single effector, Tom1, mediates pathogenicity ofV. dahliaeon tomato by targeting auxin response factors.