Is virulence phenotype evolution driven exclusively by Lr gene deployment in French Puccinia triticina populations?

Abstract

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

“…These results suggest that the replacement of some pathotypes by others, driven by changes in the frequencies of resistance genes in the varietal landscape, may be slowed, to various extents, by increases in the aggressiveness of certain genotypes or ‘lineages’ (defined as genetically related genotypes of the same group of pathotypes, i.e. with the same close ancestor), consistent with the recent analysis by Fontyn et al . (2022).…”

“…These results suggest that the replacement of some pathotypes by others, driven by changes in the frequencies of resistance genes in the varietal landscape, may be slowed, to various extents, by increases in the aggressiveness of certain genotypes or 'lineages' (defined as genetically related genotypes of the same group of pathotypes, i.e. with the same close ancestor), consistent with the recent analysis by Fontyn et al (2022). It is even possible, as for pathotype 166 317 0, for the pathotype to gain a 'second life' -for a period of three to four yearsdue to an increase in the aggressiveness of a new genotype, as long as it remains adapted (or at least not maladapted) to the resistance genes present in the varieties deployed in the landscape.…”

“…Frequency dynamics of two of the major Puccinia triticina pathotypes, 106 314 0 and 166 317 0, in the French landscape during the 2006-2020 period. Pathotype frequency was determined with data from the national survey (see Fontyn et al ., 2022). …”

“…All surveys in wheat-growing areas to date have provided evidence for continual evolution of P. triticina populations, with rapid changes in pathotype frequencies (Goyeau et al ., 2012; Kosman et al ., 2019; Zhang et al ., 2020; Fontyn et al ., 2022; Kolmer & Fajolu, 2022). These changes can be explained intrinsically by the acquisition of new virulence genes, by mutations, somatic exchanges or, more rarely, genetic recombination.…”

A highly multiplexed assay to monitor pathogenicity, fungicide resistance and gene flow in the fungal wheat pathogenZymoseptoria tritici

“…However, the rise of pathogen strains defeating crop resistance is not comprehensively monitored. Notable exceptions include the screening of rust fungi (Park et al 2011; Olivera Firpo et al 2017; Cook et al 2021; Fontyn et al 2022). To reduce damage caused by plant pathogens, a timely and accurate detection of both fungicide resistance mutations and mutations associated with the defeat of crop resistance is essential.…”