Doomed by popularity: The broad use of the Pm8 resistance gene in wheat resulted in hypermutation of the AvrPm8 gene in the powdery mildew pathogen

Abstract

The Pm8 resistance gene against the powdery mildew disease has been introgressed from rye into wheat as part of a large 1BL.1RS chromosomal translocation. Due to its high agronomic value, this translocation has seen continuous global use since the 1960′s on large growth areas, even after Pm8 resistance was overcome. This allows studying the effect of long and widespread resistance gene use on a pathogen population. Using genome wide association studies in a global population of wheat mildew isolates, we identified the avirulence effector AvrPm8 specifically recognized by Pm8. Haplovariant mining in the global population revealed 17 virulent haplotypes of the AvrPm8 gene that grouped into two categories. The first one from geographically diverse regions comprised two single amino acid polymorphisms at the same position in the AvrPm8 protein, which we confirmed to be crucial for recognition by Pm8. The second category consisted of numerous destructive mutations to the AvrPm8 open reading frame. Most individual gain-of-virulence mutations were found in geographically restricted regions, indicating they occurred recently as a consequence of the frequent Pm8 use. We conclude that both standing genetic variation as well as locally occurring new mutations contributed to the global breakdown of the Pm8 resistance gene introgression.

Long‐term and rapid evolution in powdery mildew fungi

“…Isolate‐specific resistance in barley cultivars Sultan ( Mla12 ), Wing ( Mla7 + Mlk ), Triumph ( Ml ( Ab ) + Mla7 ), Kym ( Mla9 + Mlk ), and Pipkin ( Mla13 ) were each found to break down within 2–3 years of agricultural usage (Brown, 1994). Similarly, the powdery mildew resistance gene PM8 became ineffective in many regions of the world shortly after its introgression from rye to wheat (Kunz et al, 2022). This phenotypic change has been attributed to the occurrence of individual, geographically restricted virulent B . hordei clones (“founder events”).…”

A diverse panel of 755 bread wheat accessions harbors untapped genetic diversity in landraces and reveals novel genetic regions conferring powdery mildew resistance

“…Currently, for the 27 genes represented in the differential set of Pm lines, only eight of the corresponding avirulence genes are molecularly known (43)(44)(45)(46)(47)(48)(49). Avirulence gene sequence comparison in our ten powdery mildew isolates revealed the presence of recognized haplotypes of seven of the cloned Avrs.…”

“…The response of differential lines based on the presence of specific Pm genes facilitated the prediction of cognate Avr genes in the corresponding isolates. To test the accuracy of this prediction, we compared the suggested presence of seven cloned Avrs, AvrPm1a (44,45), AvrPm2 (46), AvrPm3a/f (47), AvrPm3b/c (48), AvrPm3d (48), AvrPm8 (49) and AvrPm17 (43) to their presence and haplotype in the genomes of the ten isolates (S1 Table ). In the following we show this for the representative case of Pm2a and AvrPm2a (46).…”