Pathogen populations differ in the amount of genetic diversity they contain. Populations carrying higher genetic diversity are thought to have a greater evolutionary potential than populations carrying less diversity. We used published studies to estimate the range of values associated with two critical components of genetic diversity, the number of unique pathogen genotypes and the number of spores produced during an epidemic, for the septoria tritici blotch pathogen Zymoseptoria tritici. We found that wheat fields experiencing typical levels of infection are likely to carry between 3.1 and 14.0 million pathogen genotypes per hectare and produce at least 2.1–9.9 trillion pycnidiospores per hectare. Given the experimentally derived mutation rate of 3 × 10−10 substitutions per site per cell division, we estimate that between 27 and 126 million pathogen spores carrying adaptive mutations to counteract fungicides and resistant cultivars will be produced per hectare during a growing season. This suggests that most of the adaptive mutations that have been observed in Z. tritici populations can emerge through local selection from standing genetic variation that already exists within each field. The consequences of these findings for disease management strategies are discussed.

Successful host colonization by plant pathogens requires the circumvention of host defense responses, frequently through sequence modifications in secreted pathogen proteins known as avirulence factors (Avrs). Although Avr sequences are often polymorphic, the contribution of these polymorphisms to virulence diversity in natural pathogen populations remains largely unexplored.We used molecular genetic tools to determine how natural sequence polymorphisms of the avirulence factor Avr3D1 in the wheat pathogen Zymoseptoria tritici contributed to adaptive changes in virulence.We showed that there is a continuous distribution in the magnitude of resistance triggered by different Avr3D1 isoforms and demonstrated that natural variation in an Avr gene can lead to a quantitative resistance phenotype. We further showed that homologues of Avr3D1 in two nonpathogenic sister species of Z. tritici are recognized by some wheat cultivars, suggesting that Avr-R gene-for-gene interactions can contribute to nonhost resistance.We suggest that the mechanisms underlying host range, qualitative resistance, and quantitative resistance are not exclusive.

Natural infections frequently involve several coinfecting pathogen strains. These mixed infections can affect the extent of the infection, the transmission success of the pathogen and the eventual epidemic outcome. To date, few studies have investigated how mixed infections affect transmission between hosts. Zymoseptoria tritici is a highly diverse wheat pathogen in which multiple strains often coexist in the same lesion. Here we demonstrate that the most competitive strains often exclude their competitors during serial passages of mixed infections. The outcome of the competition depended on both the host genotype and the genotypes of the competing pathogen strains. Differences in virulence among the strains were not associated with competitive advantages during transmission, while differences in reproductive potential had a strong effect on strain competitive ability. Overall, our findings suggest that host specialization is determined mainly by the ability to successfully transmit offspring to new hosts during mixed infections.

Plants interact with a plethora of pathogenic microorganisms in nature. Pathogen-plant interaction experiments focus mainly on single-strain infections, typically ignoring the complexity of multi-strain infections even though mixed infections are common and critical for the infection outcome. The wheat pathogenZymoseptoria triticiforms highly diverse fungal populations in which several pathogen strains often colonize the same leaf. Despite the importance of mixed infections, the mechanisms governing interactions between a mixture of pathogen strains within a plant host remain largely unexplored. Here we demonstrate that avirulent pathogen strains benefit from being in mixed infections with virulent strains. We show that virulent strains suppress the wheat immune response, allowing the avirulent strain to colonize the apoplast and to reproduce. Our experiments indicate that virulent strains in mixed infections can challenge the plant immune system both locally and systemically, providing a mechanistic explanation for the persistence of avirulent pathogen strains in fields planted to resistant host plants.

Pathogen populations differ in the amount of genetic diversity they contain. Populations carrying higher genetic diversity are thought to have a greater evolutionary potential than populations carrying less diversity. We used published studies to estimate the range of val-ues associated with two critical components of genetic diversity, the number of unique pathogen genotypes and the number of spores produced during an epidemic, for the septo-ria tritici blotch pathogen Zymoseptoria tritici. We found that wheat fields experiencing typi-cal levels of infection are likely to carry between 3.2 and 14.9 million pathogen genotypes per hectare and produce at least 2.3 to 10.5 trillion pycnidiospores per hectare. Given the experimentally derived mutation rate of 3 x 10-10 substitutions per site per cell division, we estimate that between 28 and 130 million pathogen spores carrying adaptive mutations to counteract fungicides and resistant cultivars will be produced per hectare during a growing season. This suggests that most of the adaptive mutations that have been observed in Z. tritici populations can emerge through local selection from standing genetic variation that already exists within each field. The consequences of these findings for disease management strategies are discussed.