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Topic 1 - Multi-scale host-pathogen adaptation: host specialization and response to qualitative and quantitative resistances

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The use of wheat resistant varieties, one of the most effective methods of protection against fungal pathogens, is often not sustainable in current cropping systems due to their high adaptive capacity at the population level. Our research aims to understand how pathogen populations adapt to the genetic resistance of heterogeneous host populations. We address the following questions: How does the fungus adapt to its host (e.g. bread wheat, durum wheat and triticale) and to its resistances?, How to reintroduce an effective level of functional diversity into crops at plant, plot and regional scales?, How to integrate quantitative resistance into management strategies? What is the impact of the adaptation of pathogen populations on the durability of the resistances?

This first axis justifies a strong investment in understanding the impact of quantitative resistance on the evolution of pathogen life-history traits (fitness and aggressiveness). Since some years our research is carried out simultaneously on both plant and pathogen sides: the sources of resistance are characterized through a combined study of the genetic architecture of the host resistance and of the pathogenicity of the fungus (Zymoseptoria triticiPuccinia triticina).

Most of our activities are still based on long-term survey of pathogen populations in natural conditions and acquisition of phenotypic data (pathotyping and race identification, quantification of aggressiveness traits, resistance gene postulation). This is particularly the case for annual monitoring in P. striiformis and P. triticina, with a summary report sent each year to plant breeding companies and ARVALIS-Institut du Végétal. Our collection of rust isolates, stored at -80°C, constitutes an extremely rich and unique database (core collection of several hundred P. triticina and P. striiformis reference isolates collected annually since the mid-1990s, completed by an historical work collection of thousands isolates). A more recent collection of Z. tritici (worldwide and local subpopulations) is also being constructed. These collections are used in several projects conducted at various scales:

Gene scale

In order to understand how pathogen populations adapt to qualitative and quantitative wheat resistances, we characterize and genetically map resistance genes from the host and pathogenicity genes from the pathogen. This work was performed on P. triticina within Gustavo Azzimonti's PhD thesis and several MSc students. Most of our activities are focused on screening different variety panels of bread and durum wheats, developing new phenotyping methodologies, constructing linkage maps to identify QTL involved in quantitative resistance, and performing GWAS analyses to identify host resistance and pathogen aggressiveness loci. This important experimental work, essential for evaluating the durability of wheat resistance, is developed on Z. tritici for some years now. Consensus linkage maps comprising several thousand SNP markers were built for bread and durum wheat allowing the identification and comparison of robust quantitative resistance QTL to leaf rust and to Septoria leaf blotch. Those QTL are now being fine-mapped to derive diagnostic markers for breeders. GWAS analyses in French Z. tritici populations allowed the identification of several candidate avirulence genes corresponding to known Stb resistance genes. This work, developed in collaboration with ETH Zürich and Université de Neuchâtel allowed to identify and to characterize functionally the first avirulence gene (AvrStb6) in Z. tritici. These research activities continue through a post-doctoral project.

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Field scale
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Our team has investigated for about thirty years the effectiveness of cultivar mixtures to limit the spread of epidemics within a wheat canopy. While the efficacy has been demonstrated for wind-borne diseases (stripe rust), it was less clear for rain-splashed diseases (septoria leaf blotch). This efficacy was explained by biophysical effect (barrier and dilution of the susceptible host resource). The PhD theses of Christophe Gigot, then of Tiphaine Vidal, focused on the interactions between plant architecture, canopy structure and pathogen dispersal in varietal mixtures, in collaboration with EcoSys. Our team now focuses on the impact of cultivar mixtures on host-pathogen interaction and adaptive dynamics rather than on their architectural effect sensu stricto. The hypothesis developed in the Carolina Torrejon’s PhD thesis is that a varietal mixture could modify the transmission rate of virulence between two cropping seasons through the impact of both asexual and sexual reproduction. In parallel, Safa Ben Krima's PhD thesis aims to characterize the adaptation of Z. tritici to Tunisian durum wheat landraces, known to be genetically heterogeneous at an even smaller scale.

Landscape scale

The team has been interested for several years in optimizing the territorial management of wheat varieties to improve the efficiency and the durability of resistance. We based most of our research activities on our large collection of Puccinia sp. isolates, a corpus of phenotyping data (virulence and aggressiveness), the analysis of the distribution of French cultivars, and the postulation of their resistance genes. We connected, at the national level, the frequency of cultivars to the pathotypic composition of pathogen populations. The theoretical influence of strategies of resistance deployment on the intensity of epidemics and on the evolutionary dynamics of the pathogen (virulence and aggressiveness) was established by Julien Papaïx at the landscape scale during his PhD thesis. He characterized the link between environmental spatial heterogeneity and the adaptive dynamics of pathogen populations. Theoretical models showed for instance that epidemic control could be achieved by altering landscape connectivity. The presence of spatial clusters of habitats in the metapopulation was also found to facilitate specialization and to increase both the level of adaptation and the evolutionary speed of the population when dispersal is limited. Since then, studies have been conducted at the landscape scale in interaction with other BIOGER teams, focusing for instance on the management of fungicide sprays in the Maxime Garnault’s PhD thesis. Our objective is now to improve theoretical models and to validate them with experimental data to understand how host heterogeneity and landscape connectivity influence the intensity of wheat rust epidemics (see Axis 4). In her PhD thesis, as part of the H2020 RustWatch project, Cecilia Fontyn now aims to answer the question "Is aggressiveness a significant component of the adaptation of populations of P. triticina to the cultivated landscape?"

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