Sequential breakdown of the complexCf-9leaf mould resistance locus in tomato byFulvia fulva

Abstract

SummaryLeaf mould, caused byFulvia fulva, is a devastating disease of tomato plants. In many commercial tomato cultivars, resistance to this disease is governed by theCf-9locus, which comprises five paralogous genes (Cf-9A–9E) that encode receptor-like proteins. Two of these proteins contribute to resistance: Cf-9C recognizes the previously identifiedF. fulvaeffector Avr9 and provides resistance during all plant growth stages, while Cf-9B recognises the yet-unidentifiedF. fulvaeffector Avr9B and provides mature plant resistance only. In recent years,F. fulvastrains have emerged that have overcome theCf-9locus, withCf-9Ccircumvented throughAvr9deletion. To understand howCf-9Bis circumvented, we set out to identifyAvr9B.Comparative genomics,in plantatransient expression assays and gene complementation experiments were used to identifyAvr9B, while gene sequencing was used to assessAvr9Ballelic variation across a worldwide strain collection.A strict correlation betweenAvr9deletion and resistance-breaking mutations inAvr9Bwas observed in strains recently collected fromCf-9cultivars, whereasAvr9deletion but no mutations inAvr9Bwere observed in older strains.This research showcases howF. fulvahas evolved to sequentially break down the two functional resistance genes of the complexCf-9locus and highlights that this locus now has limited value for controlling leaf mould disease in worldwide commercial tomato production.