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

Hosts and pathogens typically engage in a coevolutionary arms race. This also applies to phytopathogenic powdery mildew fungi, which can rapidly overcome plant resistance and perform host jumps.<br /> Using experimental evolution, we show that the powdery mildew pathogen Blumeria hordei is capable of breaking the agriculturally important broad-spectrum resistance conditioned by barley loss-of-function mlo mutants.<br /> Partial mlo virulence of evolved B. hordei isolates is correlated with a distinctive pattern of adaptive mutations, including small-sized (c. 8-40 kb) deletions, of which one is linked to the de novo insertion of a transposable element. Occurrence of the mutations is associated with a transcriptional induction of effector protein-encoding genes that is absent in mlo-avirulent isolates on mlo mutant plants. The detected mutational spectrum comprises the same loci in at least two independently isolated mlo-virulent isolates, indicating convergent multigenic evolution. The mutational events emerged in part early (within the first five asexual generations) during experimental evolution, likely generating a founder population in which incipient mlo virulence was later stabilized by additional events.<br /> This work highlights the rapid dynamic genome evolution of an obligate biotrophic plant pathogen with a transposon-enriched genome.