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International audience; 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.

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.

Little is known about the impact of host immunity on sexual reproduction in fungal pathogens. In particular, it is unclear whether crossing requires both sexual partners to infect living plant tissues. We addressed this issue in a three-year experiment investigating different scenarios of Zymoseptoria tritici crosses on wheat according to the virulence (‘vir’) or avirulence (‘avr’) of the parents against a qualitative resistance gene. Co-inoculations (‘vir × vir’, ‘avr × vir’, ‘avr × avr’) and single inoculations were performed on a cultivar carrying the resistance gene (Cellule) and a susceptible cultivar (Apache), in the greenhouse. We assessed the intensity of asexual multiplication by scoring disease severity, and the intensity of sexual reproduction by counting the ascospores discharged from wheat residues. As expected, disease severity was more intense on Cellule for ‘vir × vir’ co-inoculations than for ‘avr × vir’ co-inoculations, with no disease for ‘avr × avr’. However, all types of co-inoculation yielded sexual offspring, whether or not the parental strains caused plant symptoms. Parenthood was confirmed by genotyping (SSR markers), and the occurrence of crosses between (co-)inoculated and exogenous strains (other strains from the experiment, or from far away) was determined. We found that symptomatic asexual infection was not required for a strain to participate in sexual reproduction, and that avirulent strains could be maintained asymptomatically “on” or “in” leaf tissues of plants carrying the corresponding resistant gene for long enough to reproduce sexually. In two of the three years, the intensity of sexual reproduction did not differ significantly between the three types of co-inoculation in Cellule, suggesting that crosses involving avirulent strains are not anecdotal. We discuss the possible mechanisms explaining the maintenance of avirulence in Z. tritici populations and supporting the potential efficacy of cultivar mixtures for limiting resistance gene breakdown.HighlightsAvirulent Zymoseptoria tritici strains can reproduce sexually in wheat plants carrying the corresponding resistant gene.Symptomatic infection of plant tissues is not essential for a strain to reproduce sexually.Avirulent strains can be maintained asymptomatically “on” or “in” leaf tissues of plants carrying the corresponding resistant gene for long enough to reproduce sexually.Crosses of virulent strains with virulent and avirulent strains in a plant host carrying the corresponding resistance gene can produce offspring with similar population sizes.Several possible scenarios for sexual crosses can explain the maintenance of avirulence in Zymoseptoria tritici populations evolving in a wheat canopy, particular in cultivar mixtures.

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 (i) the size of the pathogen population relative to the two pure stands, (ii) the size of the virulent subpopulation, and (iii) 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 argued 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.

Background Although the most common path of infection for fire blight, a severe bacterial disease on apple, is via host plant flowers, quantitative trait loci (QTLs) for fire blight resistance to date have exclusively been mapped following shoot inoculation. It is not known whether the same mechanism underlies flower and shoot resistance. Results We report the detection of a fire blight resistance QTL following independent artificial inoculation of flowers and shoots on two F1 segregating populations derived from crossing resistant Malus ×robusta 5 (Mr5) with susceptible ‘Idared’ and ‘Royal Gala’ in experimental orchards in Germany and New Zealand, respectively. QTL mapping of phenotypic datasets from artificial flower inoculation of the ‘Idared’ × Mr5 population with Erwinia amylovora over several years, and of the ‘Royal Gala’ × Mr5 population in a single year, revealed a single major QTL controlling floral fire blight resistance on linkage group 3 (LG3) of Mr5. This QTL corresponds to the QTL on LG3 reported previously for the ‘Idared’ × Mr5 and an ‘M9’ × Mr5 population following shoot inoculation in the glasshouse. Interval mapping of phenotypic data from shoot inoculations of subsets from both flower resistance populations re-confirmed that the resistance QTL is in the same position on LG3 of Mr5 as that for flower inoculation. These results provide strong evidence that fire blight resistance in Mr5 is controlled by a major QTL on LG3, independently of the mode of infection, rootstock and environment. Conclusions This study demonstrates for the first time that resistance to fire blight caused by Erwinia amylovora is independent of the mode of inoculation at least in Malus ×robusta 5.

Whilst minor pests of pear, both sawfly larvae (pear slug) and pear blister mite can at times cause sufficient damage in commercial and particularly in organic pear production for treatment to be required. In the course of breeding new pear cultivars, resistance to both pests was identified in an interspecific pear family raised from a cross between ‘PremP003’ and ‘Moonglow’. The replicated seedling family was subjected to uninhibited insect development for both pests in an insect-proof cage, providing ample infestations for resistance segregation. Using an existing genetic map for the family, one major quantitative trait locus (QTL) for resistance to pear blister mite was located to linkage group 13 (LG13) of ‘PremP003’. For pear slug, we mapped three QTLs for oviposition antixenosis, one each on LG7 and LG9 of ‘Moonglow’ and another on LG10 of ‘PremP003’, and one resistance QTL for leaf damage to LG9 of ‘Moonglow’ at a distance of 8.1 cM below the oviposition QTL. Incorporating these resistances into future cultivars could contribute to a reduction in pesticide use in pear production, especially in combination with the resistances for pear psylla (Cacopsylla pyri) and fire blight (Erwinia amylovora) recently mapped in the same population using marker-assisted selection.