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Boixel, A.-L.

Publications and source records attributed to Boixel, A.-L..

5 recordsLinked to original sources

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.

plant biology↗

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

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 x vir, avr x vir, avr x 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 x vir co-inoculations than for avr x vir co-inoculations, with no disease for avr x 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. HighlightsO_LIAvirulent Zymoseptoria tritici strains can reproduce sexually in wheat plants carrying the corresponding resistant gene. C_LIO_LISymptomatic infection of plant tissues is not essential for a strain to reproduce sexually. C_LIO_LIAvirulent strains can be maintained asymptomatically "on" or "in" leaf tissues of plants carrying the corresponding resistant gene for long enough to reproduce sexually. C_LIO_LICrosses of virulent strains with virulent and avirulent strains in a plant host carrying the corresponding resistance gene can produce offspring with similar population sizes. C_LIO_LISeveral possible scenarios for sexual crosses can explain the maintenance of avirulence in Zymoseptoria tritici populations evolving in a wheat canopy, particular in cultivar mixtures. C_LI

microbiology↗

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

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.

microbiology↗

Patterns of thermal adaptation in a worldwide plant pathogen: local diversity and plasticity reveal two-tier dynamics

O_LIPlant pathogen populations inhabit patchy environments with contrasting, variable thermal conditions. We investigated the diversity of thermal responses in populations sampled over contrasting spatiotemporal scales, to improve our understanding of their dynamics of adaptation to local conditions. C_LIO_LISamples of natural populations of the wheat pathogen Zymoseptoria tritici were collected from sites within the Euro-Mediterranean region subject to a broad range of environmental conditions. We tested for local adaptation, by accounting for the diversity of responses at the individual and population levels on the basis of key thermal performance curve parameters and thermotype (groups of individuals with similar thermal responses) composition. C_LIO_LIThe characterisation of phenotypic responses and genotypic structure revealed: (i) a high degree of individual plasticity and variation in sensitivity to temperature conditions across spatiotemporal scales and populations; (ii) geographic adaptation to local mean temperature conditions, with major alterations due to seasonal patterns over the wheat-growing season. C_LIO_LIThe seasonal shifts in functional composition suggest that populations are locally structured by selection, contributing to shape adaptation patterns. Further studies combining selection experiments and modelling are required to determine how functional group selection drives population dynamics and adaptive potential in response to thermal heterogeneity. C_LI

ecology↗

Differential tolerance to changes in moisture regime during early infection stages in the fungal pathogen Zymoseptoria tritici

Foliar plant pathogens require liquid or vapour water for at least part of their development, but their response and their adaptive tolerance to moisture conditions have been much less studied than other meteorological factors to date. We examined the impact on the wheat-Zymoseptoria tritici interaction of altering optimal moisture conditions conducive to infection. We assessed the responses in planta of 48 Z. tritici strains collected in two climatologically distinct locations (Ireland and Israel) to four high moisture regimes differing in the timing and the duration of uninterrupted exposure to saturated relative humidity (100% RH) during the first three days of infection. Individual- and population-level moisture reaction norms expressing how the sporulating area of a lesion change with the RH conditions were established based on visual assessments of lesion development at 14, 17 and 20 days post-inoculation (dpi). Our findings highlighted: (i) a critical time-dependent effect on lesion development of uninterrupted periods of exposure to 100% RH during these earliest infection stages; (ii) a marked interindividual variation in the sensitivity to RH conditions both in terms of strain average moisture response and plasticity; (iii) a higher tolerance - expressed at 14 dpi, not later - of the Israeli population to early interruption of optimal moisture conditions. By indicating that sensitivity to sub-optimal moisture conditions may vary greatly between Z. tritici individuals and populations, this study highlights the evidence of moisture adaptation signature in a plant pathogen. This suggests that understanding such variation will be critical to predict their response to changing climatic conditions.

microbiology↗