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

Plant resistances impose strong selective pressure on plant pathogen populations through the deployment of resistance genes, which leads to the emergence of new virulences. The pathogen adaptation also involves other parasitic fitness traits, especially aggressiveness components. A previous study on Puccinia triticina, the causal agent of wheat leaf rust, revealed that the distribution frequency of virulences in the French pathogen population cannot be fully explained by the major resistance genes deployed in the landscape. From 2012 to 2015, two dominant pathotypes (distinguished by their combination of virulences) were equally frequent despite the theoretical advantage conferred to one pathotype (166 317 0) by its virulence to Lr3, frequent in the cultivated landscape, whereas the other (106 314 0) is avirulent to this gene. To explain this apparent contradiction, we assessed three components of aggressiveness -- infection efficiency, latency period and sporulation capacity -- for 23 isolates representative of the most frequent genotype within each pathotype (106 314 0-G2 and 166 317 0-G1, identified by their combination of microsatellite markers). We tested these isolates on seedlings of Michigan Amber, a naive wheat cultivar that has never been grown in the landscape, Apache, a neutral cultivar with no selection effect on the landscape-pathotype pattern, and several cultivars that were frequently grown. We found that 106 314 0-G2 was more aggressive than 166 317 0-G1, with a consistency for the three components of aggressiveness. Our results show that aggressiveness plays a significant role in driving evolution in pathogen populations by acting as a selective advantage, even offsetting the disadvantage of lacking virulence towards a major Lr gene. Higher aggressiveness represents a competitive advantage that is likely even more pronounced when exhibited at the landscape scale as the expression of its multiple components is amplified by the polycyclic nature of epidemics.