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International audience; The intense and unidirectional selection pressure caused by the massive deployment of resistant plants can result in rapid adaptation of pathogen populations1. Such rapid evolution was documented for the poplar rust fungus. In 1994, poplar rust populations suddenly overcame the RMlp7 qualitative resistance carried by several poplar cultivars planted widely in Western Europe2,3. This recent event of adaptation from standing genetic variation caused a selective sweep on the rust genome4. We study a 25-year temporal sampling of poplar rust populations to decipher the demographic and evolutionary history of this pathogen while overcoming its host genetic resistance. Using resurrection ecology, we examine phenotypic and genetic variations throughout this adaptive event. Our analyses reveal that a unique and homogeneous genetic group overcame RMlp7 resistance and replaced the ancestral genetic group within five years. We then use forward simulations to 1) understand the interplay between demography and genetic evolution underpinning the rapid evolution of poplar rust populations, and 2) disentangle the polymorphism signatures of selection from that of stochastic processes due to demographic changes. We show high stochasticity in evolutionary trajectories with the notable effect of evolutionary rescue scenarios on polymorphism signatures. Finally, we integrate our simulator in an Approximate Bayesian approach (ABC) to infer the demographic and selection parameters from temporal genetic data. Our statistical framework coupling modelling with temporal data is powerful to understand recent events of rapid adaptation.1 Saubin et al. DOI:10.24072/pcjournal.102 Louet et al. DOI:10.1111/mec.162943 Persoons et al. DOI:10.1111/mec.13980 4 Persoons et al. DOI:10.1093/gbe/evab279

Cropping genetically resistant plants allows to control pathogen populations while substantially reducing chemical inputs. However, resistances are often quickly defeated by pathogens. In this context, how can sustainable crop protection be achieved? This question has shaped the debate about the durability of genetic resistances in agriculture for decades, and, despite active research efforts, has not been satisfactorily answered yet. Here we demonstrate from a bibliography analysis that the research field of resistance durability evolved into two non-overlapping directions: (i) the subfield of 'epidemiology and evolution', which aims to forecast and explain pathogen population dynamics; (ii) the subfield of 'molecular interactions', which studies the molecular processes involved in the overcoming of resistance and in the dialogue between plants and pathogens. After reviewing briefly these two subfields and the gap between the corresponding research communities, we propose strategies to merge these approaches into one by using the concepts of population genetics. Ultimately, such new eco-evolutionary studies could be used to determine the best strategy for the deployment of genetically resistant cultivars by integrating, from gene to landscape, all relevant and contextual biological knowledge into sound theoretical models.

Plant effector biology is a research area that describes how plant-associated organisms modulate host structures and functions to promote colonization by using small molecules (effectors). In this article, we analyzed the 249 most highly-cited publications focused on plant pathogen effectors (aka Highly Influential studies on plant Pathogen Effectors; thereafter HIPEs) published between 2000 and 2020. This analysis identified outstanding countries, organizations, and journals that contributed HIPEs, as well as the evolution of research trends, model molecules, and model organisms over the last two decades. We notably show an increasing proportion of studies focused on effectors of biotrophic and hemibiotrophic fungi upon time. Our snapshot of the top tier plant effector biology papers will help readers gain a comprehensive and analytical understanding of this research area.

Molecular plant immunity is a dynamic research field that broadly addresses how plants interact with their associated organisms and defend themselves against pests and pathogens. Here, we aimed at providing readers with a snapshot of top-tiers molecular plant immunity research, by identifying and analyzing the 170 most highly-cited publications (aka Highly-Influential Publications in Plant Immunity; hereafter HIPPYs) published in this field between 2000 and 2019. Our analysis draws a broad analytical knowledge of the most influential scientific advances in the field, as well as the research community that made them. We notably show that HIPPYs are shared by a small, structured, and connected research community. The HIPPYs address coherent research questions using a handful of key model objects (i.e. organisms or molecules), and report findings and concepts that collectively shape our integrated understanding on the molecular interactions between plants and their associated organisms. Our 'HIP in' method is easily transposable to other large research areas, and may help early-career researchers to gain a broader knowledge of their field of interest.

International audience

International audience; Melampsora larici-populina is a partially asexual basidiomycete fungus responsible for poplar rust, with its sexual stage on larch (Larix sp.) and its asexual stage on poplar (Populus sp.). Resistant 7 poplar cultivars were widely planted in northern France until a major resistance breakdown which occurred in 1994. This selective event lead to a rapid and complete shift in the pathogen population. Two independent mutations are responsible for the virulent recessive allele: a SNP and a deletion. Here we study the dynamics of virulence allele fixation both theoretically and empirically, by modeling virulence fixation in different evolutionary scenarios, and by tracing back the polymorphism evolution at the candidate locus before, during and after the resistance breakdown. The modeling part highlighted the interplay between the life cycle (host alternation or not) and the extent of resistance deployment on the probability and dynamics of fixation. Fluorescence ratio methods allowed us to successfully characterize genotypes of reference strains. This method will be applied to nearly 300 isolates collected from 1988 to 2016. By linking our model results and the observed polymorphism evolution in the studied populations, we will investigate whether the combined presence of the deletion and the mutation conferring virulence may have led to such a rapid and complete replacement of the pathogen population.