Evolutionary history of AvrRvi6, the first avirulence gene identified in the apple scab fungus Venturia inaequalis

The management of fungal diseases of apple depends largely on the use of chemical. In apple orchards an average of 20 treatments are required each year to combat its main pathogen, the apple scab fungus Venturia inaequalis. The use of cultivars carrying resistance (R) genes, which rely on the recognition of the product of avirulence (AVR) genes from the pathogen, known as gene-for-gene interactions is an environmentally friendly alternative to chemicals. Although 17 gene-for-gene relationships have been reported in this pathosystem, only two resistance genes, Rvi6 and Rvi15, have been cloned, and nothing is known about V. inaequalis AVR genes. Only one major apple R gene, Rvi6, has been extensively deployed in orchards. Rvi6 was introgressed into domesticated apple (Malus x domestica) from the related ornamental crabapple Malus floribunda. Recently, a population genetics analysis of V. inaequalis european populations indicated that VIR alleles that have circumvented the Rvi6-mediated resistance in cultivated orchards originate from standing genetic variation in a wild population. Here we report the identification of the first V. inaequalis AVR gene, AvrRvi6, by means of genetics, genomics and functional approaches. Transient expression assays in Nicotiana benthamiana allowed the functional characterization of the recognition of AvrRvi6 by Rvi6, and population genomics of Avr locus polymorphism approaches revealed the exact evolutionary history of Rvi6 circumvention at the European scale.