The Rpi-mcq1 resistance gene family recognizes Avr2 of Phytophthora infestans but is distinct from R2

Potato late blight, which is caused by the destructive oomycete pathogen Phytophthora infestans, is a major threat to global food security. Several nucleotide binding, leucine-rich repeat (NLR) Resistance to P. infestans (Rpi) genes have been introgressed into potato cultivars from wild Solanum species that are native to Mexico, but these were quickly defeated. Positional cloning in Solanum mochiquense, combined with allele mining in Solanum huancabambense, were used to identify a new family of Rpi genes from Peruvian Solanum species. Rpi-mcq1, Rpi-hcb1.1 and Rpi-hcb1.2 confer race-specific resistance to a panel of P. infestans isolates. Effector assays showed that the Rpi-mcq1 family mediates a hypersensitive response upon recognition of the RXLR effector AVR2, which had previously been found to be exclusively recognized by the family of R2 resistance proteins. The Rpi-mcq1 and R2 genes are distinct and reside on chromosome IX and IV, respectively. This is the first report of two unrelated R protein families that recognize the same AVR protein. We anticipate that this likely is a consequence of a geographically separated dynamic co-evolution of R gene families of Solanum with an important effector gene of P. infestans. Author summaryPotato is the largest non-grain staple crop and essential for food security world-wide. However, potato plants are continuously threatened by the notorious oomycete pathogen Phytophthora infestans that causes late blight. This devastating disease has led to the Irish famine more then 150 years ago, and is still a major threat for potato. Resistance against P. infestans can be found in wild relatives of potato, which carry resistance genes that belong to the nucleotide binding site-leucine-rich repeat (NLR) class. Known NLR proteins typically recognize a matching effector from Phytophthora, which leads to a hypersensitive resistance response (HR). For example, R2 from Mexican Solanum species recognizes AVR2 from P. infestans. So far, these R genes exclusively match to one Avr gene. Here, we identified a new class of NLR proteins that are different from R2, but also recognize the same effector AVR2. This new family of NLR occurs in South American Solanum species, and we anticipate that it is likely a product of a geographically separated co-evolution with AVR2. This is the first report of two unrelated R protein families that recognize the same AVR protein.