Puccinia triticina is a highly damaging wheat pathogen. The efficacy of leaf rust control by genetic resistance is mitigated by the adaptive capacity of the pathogen, expressed as changes in its virulence combinations (pathotypes). An extensive P. triticina population survey has been carried out in France over the last 30 years, describing the evolutionary dynamics of this pathogen in response to cultivar deployment. We analysed the data set for the 2006–2016 period to determine the relationship between the Lr genes in the cultivars and virulence in the pathotypes. Rust populations were dominated by a small number of pathotypes, with variations in most of the virulence frequencies related to the corresponding Lr gene frequencies in the cultivated landscape. Furthermore, the emergence and spread of a new virulence matched the introduction and use of the corresponding Lr gene (Lr28), confirming that the deployment of qualitative resistance genes is an essential driver of evolution in P. triticina populations. However, principal component analysis (PCA) revealed that certain pathotype–cultivar associations cannot be explained solely by the distribution of Lr genes in the landscape. This conclusion is supported by the predominance of a few pathotypes on some cultivars, with the persistence of several other compatible pathotypes at low frequencies. Specific interactions are not, therefore, sufficient to explain the distribution of virulence in rust populations. The hypothesis that quantitative interactions between P. triticina populations and bread wheat cultivars—based on differences in aggressiveness—is also a driver of changes in pathotype frequencies deserves further investigation.

Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of French wheat leaf rust populations , Peer Community Journal, 3: e39.

Plant pathogens are constantly evolving and adapting to their environment, including their host. Virulence alleles emerge, and then increase, and sometimes decrease in frequency within pathogen populations in response to the fluctuating selection pressures imposed by the deployment of resistance genes. In some cases, these strong selection pressures cannot fully explain the evolution observed in pathogen populations. A previous study on the French population of Puccinia triticina, the causal agent of wheat leaf rust, showed that two major pathotypes — groups of isolates with the same combinations of virulences — predominated but then declined over the 2005-2016 period. The relative dynamics of these two pathotypes — 166 317 0 and 106 314 0 — relative to the others present in the population could not be explained solely by the frequency of Lr genes in the landscape. Within these two pathotypes, we identified two main genotypes that emerged in succession. We assessed three components of aggressiveness — infection efficiency, latency period and sporulation capacity — for 44 isolates representative of the four P. triticina pathotype-genotype combinations. We showed, for both pathotypes, that the most recent genotypes were more aggressive than the older ones. Our findings were highly consistent for the various components of aggressiveness for pathotype 166 317 0 grown on Michigan Amber — a 'naive' cultivar never grown in the landscape — or on Apache — a 'neutral' cultivar, with no selection effect on the landscape-pathotype pattern. For pathotype 106 314 0, the most recent genotype was more aggressive on several of the cultivars most frequently grown in the landscape, but not on 'neutral' and 'naive' cultivars, and only in terms of its latency period. We conclude that the quantitative components of aggressiveness can be significant drivers of evolution in pathogen populations. A gain in aggressiveness allowed the maintenance of a declining pathotype, and even further expansion of that pathotype, in the pathogen population, providing evidence that virulence alone is not sufficient, aggressiveness also being required for the adaptation of a pathogen to a changing varietal landscape.