Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of French wheat leaf rust populations

Abstract

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.

Can higher aggressiveness effectively compensate for a virulence deficiency in plant pathogen? A case study ofPuccinia triticina’s fitness evolution in a diversified varietal landscape

“…Different genotypes were identified within each pathotype from these markers leading to the distinction of several pathogenotypes, i.e. different pathotype × genotype combinations (Fontyn et al, 2023). Indeed, identical genotypes may differ in one or several virulences, and, conversely, that different genotypes can have the same virulence profile while potentially expressing differences in their aggressiveness.…”

“…Several compatible pathotypes, other than the two aforementioned, virulent against the Lr genes carried by the most widely grown cultivars, were present in the landscape but never reached substantial frequencies. Focusing on the comparative dynamics of these two dominant pathotypes (Figure 3 in Fontyn et al, 2023) highlighted three periods: (i) until 2011, the frequency of the pathotype 106 314 0 remained higher than the frequency of 166 317 0; (ii) then, from 2012 to 2015, the two pathotypes were at similar frequencies; and (iii) from 2016, 106 314 0 strongly decreased and finally disappeared, while 166 317 0 became dominant. Considering the Lr genes present in the French varietal landscape from 2011 to 2015 (Fontyn et al, 2022), the four most frequent Lr13, Lr37, Lr14a and Lr10 were overcome by both pathotypes 106 314 0 and 166 317 0.…”

“…Additionally, Azzimonti et al (2013) found that P. triticina isolates can adapt to quantitative resistance, as evidenced by their specificity towards resistance QTLs in wheat. Despite these evidences, the impact of aggressiveness components in agronomic context at a large spatiotemporal scale has not been previously established for leaf rust, until Fontyn et al (2023) compared the aggressiveness of 'old' and 'new' P. triticina pathotypes. Fontyn et al (2023) reported that two isolates of the same pathotype are not necessarily of identical genotype, as defined by microsatellite markers, and therefore do not necessarily belong to the same clonal lineage, while identical genotypes may differ in one or several virulences.…”

“…Despite these evidences, the impact of aggressiveness components in agronomic context at a large spatiotemporal scale has not been previously established for leaf rust, until Fontyn et al (2023) compared the aggressiveness of 'old' and 'new' P. triticina pathotypes. Fontyn et al (2023) reported that two isolates of the same pathotype are not necessarily of identical genotype, as defined by microsatellite markers, and therefore do not necessarily belong to the same clonal lineage, while identical genotypes may differ in one or several virulences. The authors proposed to use the term 'pathogenotype' to identify isolates based on a unique pathotype × genotype association and found that the 'new' pathogenotypes (106 314 0-G2 and 166 317 0-G2), within each of the aforementioned predominant pathotype 106 314 0 and 166 317 0, exhibited higher levels of aggressiveness compared to the 'old' ones (106 314 0-G1 and 166 317 0-G1).…”

“…Assessments of three aggressiveness components were conducted for 23 representative isolates on two cultivars considered 'neutral' and 'naïve', as defined by Fontyn et al (2023), meaning that they have no selection effect on the cultivated landscape-pathotype pattern, and on five of the most commonly grown cultivars from 2006 to 2016, which includes cultivars grown before and during the studied period.…”