A fungal plant pathogen overcomes conserved broad-spectrum plant disease resistance by rapid gene loss

Powdery mildews like Blumeria graminis rapidly overcome host plant resistance and exhibit host jumps. However, it is unknown what drives rapid evolutionary adaptation of the powdery mildews. Here, we show that the rapid loss of two genes in the barley powdery mildew promotes virulence on resistant barley mlo plants. We found two major genomic deletions causing the loss of BLGH_02703 and the orthologue of the Aspergillus transcription factor Medusa in barley powdery mildew lines selected to be able to infect barley mlo mutant plants. Analogous to Aspergillus, medusa mutants displayed presence of elongated conidiospores, which was independent of the loss of blgh_02703. In conclusion, barley powdery mildew exhibits rapid gene losses enabling adaptation to resistant plant genotypes. This work highlights the dynamic genome evolution of an obligate biotrophic plant pathogen with a transposon-enriched genome and will aid in understanding the co-evolution of tightly associated host-pathogen interactions.