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Topic 2 - Adaptive responses of plant pathogens to their abiotic environment: from individual to population scale

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In this second axis our objective is to progress in the understanding of how pathogen populations adapt to abiotic factors (mainly climatic conditions), in addition to the selection pressure exerted by host varieties and fungicides. A challenge is to produce knowledge that helps to understand how pathogen populations are affected by the sharp spatio-temporal variations in climatic conditions occurring over leaf surfaces and in fine how they could adapt to climate change. To this end we develop experimental methods to characterize the phenotypic diversity of wheat pathogen populations (Puccinia striiformis and Zymoseptoria tritici) and their response to temperature variations at different spatiotemporal scales (contrasted climatic areas, local seasonal fluctuations, climate change). By combining experimental and modeling approaches, mixing thermal biology and eco-evolutionary concepts, we also tried to renew the issues of thermal adaptation in plant disease epidemiology, highlighted by the "climate change" challenge. This third strategic axis is strongly structured by the collaborations developed over many years with EcoSys.

We address two main critical questions:

Can thermal adaptation explain the emergence of new Puccinia striiformis races by their thermal competitive advantage? (case of pathogen population driven by clonal reproduction)

Epidemics of stripe rust are recurrent and determined by a rapid succession over time of P. striiformis races, characterized phenotypically by their virulence to cultivated wheat varieties (see Axis 1). A significant part of our activities consist in monitoring this boom-and-bust dynamic at French, European and world scales. We study the thermal adaptation of the new invasive strains (e.g. PstS1, PstS2, Warrior+, Warrior-, Triticale). In the recent past we focused on populations from France, southern Europe and Mediterranean basin within Bochra Bahri’s PhD thesis, from Central Asia within Sajid Ali’s PhD thesis (previous period), and from Middle East with Rola El Amil’s PhD thesis. A recent analysis combining experimental and modelling results, questioned whether thermal aptitude promoted the spread of the different strains, by comparing their infection efficiency and latent period at different temperatures on susceptible wheat varieties. The thermal generalist profile of Warrior isolates was confirmed, with an intermediate capacity to tolerate warming climate, whereas the southern isolates are better adapted to warm conditions, but do not have the virulences necessary to develop on current varieties. This type of research continues within the H2020 RustWatch project, in which our objective is to understand the selective advantage of new invasive P. striiformis strains, which appeared more aggressive and tolerant to high temperatures compared to oldest local strains, specific to the temperate areas (Northern France) and to the Mediterranean basin (Tunisia).

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What is the adaptive potential of Zymoseptoria tritici populations to temperature fluctuations at different spatiotemporal scales? (case of pathogen population driven by sexual reproduction)
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This question followed Frédéric Bernard's PhD thesis, in which the response of Z. tritici to leaf temperature was characterized. A series of experimental results then showed that seasonal temperature fluctuations can drive short-term selection for aggressiveness traits (sporulation capacity, latency period) in Z. tritici. This research was continued with Anne-Lise Boixel's PhD thesis in collaboration with EcoSys. Thermal phenotyping of Z. tritici populations highlighted shifts in thermal adaptive patterns between Euromediterranean populations sampled from contrasted climatic areas and confirmed the presence of local seasonal patterns. The consequences of this interindividual phenotypic variation in thermal responses (plasticity) on both dynamics and adaptive potential of populations was explored by conducting mark-release-recapture experiments in controlled and natural conditions. We are now building a spatially explicit individual-based model simulating temporal changes in the phenotypic composition of a population in response to thermal variations of its environment.