Annual dynamics of Zymoseptoria tritici populations in wheat cultivar mixtures: A compromise between the efficacy and durability of a recently broken‐down resistance gene?

Abstract

Cultivar mixtures slow polycyclic epidemics but may also affect the evolution of pathogen populations by diversifying the selection pressures exerted by their plant hosts at field scale. We compared the dynamics of natural populations of the fungal pathogen Zymoseptoria tritici in pure stands and in three binary mixtures of wheat cultivars (one susceptible cultivar and one cultivar carrying the recently broken‐down Stb16q gene) over two annual field epidemics. We combined analyses of population “size” based on disease severity, and of population “composition” based on changes in the frequency of virulence against Stb16q in seedling assays with more than 3000 strains. Disease reductions were observed in mixtures late in the epidemic, at the whole‐canopy scale and on both cultivars, suggesting the existence of a reciprocal protective effect. The three cultivar proportions in the mixtures (0.25, 0.5, and 0.75) modulated the decrease in (a) the size of the pathogen population relative to the two pure stands, (b) the size of the virulent subpopulation, and (c) the frequency of virulence relative to the pure stand of the cultivar carrying Stb16q. Our findings suggest that optimal proportions may differ slightly between the three indicators considered. We argue potential trade‐offs that should be taken into account when deploying a resistance gene in cultivar mixtures: between the dual objectives “efficacy” and “durability,” and between the “size” and “frequency” of the virulent subpopulation. Based on current knowledge, it remains unclear whether virulent subpopulation size or frequency has the largest influence on interepidemic virulence transmission.

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

“…The selection pressure exerted on pathogen populations by the deployment of a resistance gene in fields planted with a single cultivar promotes the generalisation of virulent strains (Brown and Tellier, 2011). Virulence is, theoretically, accompanied by a fitness cost (Burdon and Laine, 2019), but it was thought that this advantage for avirulent strains (rarely demonstrated; see, for instance, Orellana-Torrejon et al ., 2022a) was compensated by their inability to persist in pathogen populations over a long period of time. The experimental findings presented here challenge partly this assumption.…”

“…This epiphytic development may be explained by specific experimental conditions in the greenhouse: application of a high concentration of inoculum on the leaf surface and favourable conditions for fungal growth over an extended period of time. This phenomenon could however happen in the field: 3.3% of the strains sampled on Cellule grown in mixture with Apache, from STB lesions, were found to be avirulent against Stb16q (Orellana-Torrejon et al ., 2022a). The success of ‘vir × avr’ crosses (process ② in Figure 6 ) can be also explained by the hypothesis that penetration of the avirulent strain was favoured by a virulent strain that had previously infected the host tissues (Tollenaere et al ., 2016).…”

“…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.…”

“…Each year, we selected eight strains ( Figure 1 and Table S1 ) from a Z. tritici population sampled from single pycnidium on cv. Cellule and Apache in pure-stand field trials in Grignon (France) in July 2017, July 2018, and June 2019 (Orellana-Torrejon et al ., 2022a). The virulence status of these strains with respect to Stb16q was determined by phenotyping on wheat cv.…”

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 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)].…”