Does the impact of cultivar mixtures on virulence dynamics in Zymoseptoria tritici populations persist after interseason sexual reproduction?

Abstract

This study follows on from a previous study showing that binary mixtures of wheat cultivars affect the evolution of Zymoseptoria tritici populations within a field epidemic from the beginning (t1) to the end (t2) of a growing season. Here, we focused on the impact of interseason sexual reproduction on this evolution. We studied mixtures of susceptible and resistant cultivars (carrying Stb16q, a recently broken-down resistance gene) in proportions of 0.25, 0.5 and 0.75, and their pure stands. We determined the virulence status of 1440 ascospore-derived strains collected from residues of each cultivar by phenotyping on seedlings. Virulence frequencies were lower in mixtures than in pure stands of the resistant cultivar, as at t2, revealing that the impact of mixtures persisted until the beginning of the next epidemic (t3). The frequency of virulence was lower in the offspring population on the susceptible cultivar and, more surprisingly, the frequency of avirulence on the resistant cultivar increased after sexual reproduction. Our findings highlight two epidemiological processes in mixtures: selection within the local pathogen population between t1 and t2 driven by asexual cross-contamination between cultivars (previous study) and sexual crosses between avirulent and virulent strains between t2 and t3 driven by changes in the probabilities of physical encounters (this study). Mixtures therefore appear to be a promising strategy for the deployment of qualitative resistances, not only to limit the intensity of Septoria tritici blotch epidemics, but also to reduce the erosion of resistances by managing evolution of the pathogen population at a pluriannual scale.

How large and diverse are field populations of fungal plant pathogens? The case of Zymoseptoria tritici

“…A recent field experiment suggested that a mixture can maintain the efficacy of the resistance encoded by Stb16q through a decrease in the frequency of virulent strains infecting the susceptible cultivar and an increase in the frequency of avirulent strains occurring on the cultivar carrying Stb16q in the mixtures compared to pure stands. The observed changes resulted (i) on the one hand from virulence selection/counter‐selection driven by exchanges of splash‐dispersed asexual spores between cultivars depending on their respective proportions in the mixture (Orellana‐Torrejon, Vidal, Boixel, et al, 2022), and (ii) on the other hand from sexual reproduction between virulent strains and avirulent strains that land on the cultivar carrying Stb16q and then recombine with virulent strains without the need to infect host tissues (Orellana‐Torrejon, Vidal, Saint‐Jean, & Suffert, 2022). This mechanism that explains the persistence (or even a slight increase) of avirulent strains in mixtures was experimentally established by Orellana‐Torrejon, Vidal, Gazeau, et al (2022), who showed that symptomatic asexual infection is not required for a strain to engage in sexual reproduction [a similar finding was also reported for the Stb6‐AvrStb6 interaction (Kema et al, 2018)].…”

Multiple scenarios for sexual crosses in the fungal pathogen Zymoseptoria tritici on wheat residues: Potential consequences for virulence gene transmission

“…For instance, the use of cultivar mixtures would increase the exposure of plants carrying a resistance gene to the corresponding avirulent strains, due to the presence of neighbouring susceptible plants on which these strains would be then able to multiply asexually. Orellana-Torrejon et al (2022a, 2022b highlighted a consequence of this phenomenon in the field: the frequency of avirulent Z. tritici strains was higher after sexual reproduction on the residues of a resistant wheat cultivar grown in a mixture than after sexual reproduction on the residues of a pure stand, providing experimental evidence of an "overtransmission" of avirulence to the next epidemic season. Cultivar mixtures, therefore, appear to be a promising way to exploit the epidemiological consequences of avirulent strains crossing on resistant cultivars for limiting the breakdown of resistance genes.…”

How large and diverse are field populations of fungal plant pathogens? The case of Zymoseptoria tritici

“…However, cultivar mixtures can still effectively control STB and limit the loss in effective- Torrejon et al, 2022b). This mechanism that explains the persistence (or even a slight increase) of avirulent strains in mixtures was experimentally established by Orellana-Torrejon et al (2022c), who showed that symptomatic asexual infection is not required for a strain to engage in sexual reproduction [a similar finding was also reported for the Stb6-AvrStb6 interaction (Kema et al, 2018)].…”

“…A recent field experiment suggested that a mixture can maintain the efficacy of the resistance encoded by Stb16q through a decrease in the frequency of virulent strains infecting the susceptible cultivar and an increase in the frequency of avirulent strains occurring on the cultivar carrying Stb16q in the mixtures compared to pure stands. The observed changes resulted (i) on the one hand from virulence selection/counter-selection driven by exchanges of splash-dispersed asexual spores between cultivars depending on their respective proportions in the mixture (Orellana-Torrejon et al, 2022a), and (ii) on the other hand from sexual reproduction between virulent strains and avirulent strains that land on the cultivar carrying Stb16q and then recombine with virulent strains without the need to infect host tissues (Orellana-Torrejon et al, 2022b). This mechanism that explains the persistence (or even a slight increase) of avirulent strains in mixtures was experimentally established by Orellana-Torrejon et al (2022c), who showed that symptomatic asexual infection is not required for a strain to engage in sexual reproduction [a similar finding was also reported for the Stb6-AvrStb6 interaction (Kema et al, 2018)].…”