Modern agriculture favours the selection and spread of novel plant diseases. Furthermore, crop genetic resistance against pathogens is often rendered ineffective within a few years of its commercial deployment. Leptosphaeria maculans, the cause of phoma stem canker of oilseed rape, develops gene-for-gene interactions with its host plant, and has a high evolutionary potential to render ineffective novel sources of resistance in crops. Here, we established a four-year field experiment to monitor the evolution of populations confronted with the newly released Rlm7 resistance and to investigate the nature of the mutations responsible for virulence against Rlm7. A total of 2551 fungal isolates were collected from experimental crops of a Rlm7 cultivar or a cultivar without Rlm7. All isolates were phenotyped for virulence and a subset was genotyped with neutral genetic markers. Virulent isolates were investigated for molecular events at the AvrLm4-7 locus. Whilst virulent isolates were not found in neighbouring crops, their frequency had reached 36% in the experimental field after four years. An extreme diversity of independent molecular events leading to virulence was identified in populations, with large-scale Repeat Induced Point mutations or complete deletion of AvrLm4-7 being the most frequent. Our data suggest that increased mutability of fungal genes involved in the interactions with plants is directly related to their genomic environment and reproductive system. Thus, rapid allelic diversification of avirulence genes can be generated in L. maculans populations in a single field provided that large population sizes and sexual reproduction are favoured by agricultural practices.
Plant disease resistance often relies on simple “gene-for-gene” systems and, in the pathogen, a mutation in a single “avirulence” gene matching the plant resistance gene is sufficient to render the resistance ineffective. In agricultural systems, breeding for resistance is challenged by both the high evolutionary potential of the pathogen and the large scale of crop production; together, these factors encourage “breakdown” of novel sources of resistance soon after their deployment. Here, we established a four-year field experiment to evaluate the mechanisms and speed with which a fungal pathogen of oilseed rape, Leptosphaeria maculans renders ineffective the novel resistance gene Rlm7. The pathogen showed a very high evolutionary potential; the proportion of isolates in the population that were virulent against Rlm7 increased from 0 to 36% in four years. The experiment demonstrated that an extremely diverse range of molecular events leading to virulence, from more or less extensive nucleotide mutations or deletions to complete gene deletion, can occur in a single field. These results suggest that the genomic environment of the avirulence gene and the reproductive regime of the pathogen promote mutability at a single locus to produce virulence. Cropping practices that promote large pathogen populations and encourage sexual reproduction therefore favour rapid adaptation of the pathogen to the novel resistance.