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

Abstract

Hosts and pathogens typically engage in an evolutionary arms race. This also applies to phytopathogenic powdery mildew fungi, which can rapidly overcome plant resistance and perform host jumps. Using experimental evolution, we show that the powdery mildew pathogen Blumeria graminis f.sp. hordei is capable of breaking the agriculturally important broad-spectrum resistance conditioned by barley loss-of-function mlo mutants. Partial mlo virulence is associated with a distinctive pattern of adaptive mutations, including small-sized (8-40 kb) deletions, one of which likely affects spore morphology. The detected mutational spectrum comprises the same loci in at least two independent mlo-virulent isolates, indicating convergent multigenic evolution. This work highlights the dynamic genome evolution of an obligate biotrophic plant pathogen with a transposon-enriched genome.

Long‐term and rapid evolution in powdery mildew fungi

“…Indeed, several mutational events were detected in these isolates, suggesting modulation or loss-of-function of a transcriptional regulator, an E3-ligase-like protein, and a protein of unknown function to contribute to partial virulence on mlo genotypes (Kusch et al, 2021).…”

“…Interestingly, experimental evolution trials demonstrated that B . hordei can rapidly adapt to overcome mlo ‐based resistance (Kusch et al, 2021; Schwarzbach, 1979). In these experiments, less than 15 asexual passages or generations of selection on barley mlo mutant plants were sufficient to obtain and stabilize partially mlo ‐virulent isolates of B . hordei .…”

“…This is remarkable since, in contrast to a break of race‐specific resistance, mlo virulence appears to be multigenic. Indeed, several mutational events were detected in these isolates, suggesting modulation or loss‐of‐function of a transcriptional regulator, an E3‐ligase‐like protein, and a protein of unknown function to contribute to partial virulence on mlo genotypes (Kusch et al, 2021). The fact that few genetic events are sufficient to break down mlo ‐based broad‐spectrum resistance raises the question why this phenotype does not occur more frequently in agricultural settings.…”

“…This conundrum may be explained by the fact that farmers only deploy mlo ‐resistant spring barley but not winter barley varieties (Czembor, 2016; Jørgensen, 1992). Further, so far, all mlo ‐virulent isolates are only capable of partial virulence on mlo ‐resistant barley (Kusch et al, 2021; Schwarzbach, 1979; Yaeno et al, 2021), and this capacity may be an adaptation with a trade‐off affecting overall fitness even on susceptible Mlo wild‐type barley cultivars (Kusch et al, 2021).…”