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International audience; The deployment of plant varieties carrying resistance genes (R) exerts strong selection pressure on pathogen populations. Rapidly evolving avirulence genes (Avr) allow pathogens to escape R-mediated plant immunity through a variety of mechanisms, leading to virulence. The poplar rust fungus Melampsora larici-populina is a damaging pathogen of poplars in Europe. It underwent a major adaptive event in 1994, with the breakdown of the poplar RMlp7 resistance gene. Population genomics studies identified a locus in the genome of M. larici-populina that probably corresponds to the candidate avirulence gene AvrMlp7. Here, to further characterize this effector, we used a population genetics approach on a comprehensive set of 281 individuals recovered throughout a 28-year period encompassing the resistance breakdown event. Using two dedicated molecular tools, genotyping at the candidate locus highlighted two different alterations of a predominant allele found mainly before the resistance breakdown: a nonsynonymous mutation and a complete deletion of this locus. This results in six diploid genotypes: three genotypes related to the avirulent phenotype and three related to the virulent phenotype. The temporal survey of the candidate locus revealed that both alterations were found in association during the resistance breakdown event. They pre-existed before the breakdown in a heterozygous state with the predominant allele cited above. Altogether, these results suggest that the association of both alterations at the candidate locus AvrMlp7 drove the poplar rust adaptation to RMlp7-mediated immunity. This study demonstrates for the first time a case of adaptation from standing genetic variation in rust fungi during a qualitative resistance breakdown.

Crop varieties carrying qualitative resistance to targeted pathogens lead to strong selection pressure on parasites, often resulting in resistance breakdown. It is well known that qualitative resistance breakdowns modify pathogen population structure but few studies have analyzed the consequences on their quantitative aggressiveness‐related traits. The aim of this study was to characterize the evolution of these traits following a resistance breakdown in the poplar rust fungus, Melampsora larici‐populina. We based our experiment on three temporal populations sampled just before the breakdown event, immediately after and four years later. First, we quantified phenotypic differences among populations for a set of aggressiveness traits on a universally susceptible cultivar (infection efficiency, latent period, lesion size, mycelium quantity, and sporulation rate) and one morphological trait (mean spore volume). Then, we estimated heritability to establish which traits could be subjected to adaptive evolution and tested for evidence of selection. Our results revealed significant changes in the morphological trait but no variation in aggressiveness traits. By contrast, recent works have demonstrated that quantitative resistance (initially assumed more durable) could be eroded and lead to increased aggressiveness. Hence, this study is one example suggesting that the use of qualitative resistance may be revealed to be less detrimental to long‐term sustainable crop production.

Foliar pathogens face heterogeneous environments depending on the maturity of leaves they interact with. In particular, nutrient availability as well as defense levels may vary significantly, with opposing effects on the success of infection. The present study tested which of these factors have a dominant effect on the pathogen's development. Poplar leaf disks of eight maturity levels were inoculated with the poplar rust fungus Melampsora larici-populina using an innovative single-spore inoculation procedure. A set of quantitative fungal traits (infection efficiency, latent period, uredinia size, mycelium quantity, sporulation rate, sporulation capacity, and spore volume) was measured on each infected leaf disk. Uninfected parts of the leaves were analyzed for their nutrient (sugars, total C and N) and defense compounds (phenolics) content. We found that M. larici-populina is more aggressive on more mature leaves as indicated by wider uredinia and a higher sporulation rate. Other traits varied independently from each other without a consistent pattern. None of the pathogen traits correlated with leaf sugar, total C, or total N content. In contrast, phenolic contents (flavonols, hydroxycinnamic acid esters, and salicinoids) were negatively correlated with uredinia size and sporulation rate. The pathogen's fitness appeared to be more constrained by the constitutive plant defense level than limited by nutrient availability, as evident in the decrease in sporulation.

Host–parasite systems provide convincing examples of Red Queen co-evolutionary dynamics. Yet, a key process underscored in Van Valen's theory – that arms race dynamics can result in extinction – has never been documented. One reason for this may be that most sampling designs lack the breadth needed to illuminate the rapid pace of adaptation by pathogen populations. In this study, we used a 25-year temporal sampling to decipher the demographic history of a plant pathogen: the poplar rust fungus, Melampsora larici-populina. A major adaptive event occurred in 1994 with the breakdown of R7 resistance carried by several poplar cultivars widely planted in Western Europe since 1982. The corresponding virulence rapidly spread in M. larici-populina populations and nearly reached fixation in northern France, even on susceptible hosts. Using both temporal records of virulence profiles and temporal population genetic data, our analyses revealed that (i) R7 resistance breakdown resulted in the emergence of a unique and homogeneous genetic group, the so-called cultivated population, which predominated in northern France for about 20 years, (ii) selection for Vir7 individuals brought with it multiple other virulence types via hitchhiking, resulting in an overall increase in the population-wide number of virulence types and (iii) – above all – the emergence of the cultivated population superseded the initial population which predominated at the same place before R7 resistance breakdown. Our temporal analysis illustrates how antagonistic co-evolution can lead to population extinction and replacement, hence providing direct evidence for the escalation process which is at the core of Red Queen dynamics.

Summary 1. Biological invasions are a major consequence of globalization and pose a significant threat to biodiversity. Because only a small fraction of introduced species become invasive, identification of those species most likely to become invasive after introduction is highly desirable to focus management efforts. The predictive potential of species-specific traits has been much investigated in plants and animals. However, despite the importance of fungi as a biological group and the potentially severe effects of pathogenic fungi on agrosystems and natural ecosystems, the specific identification of traits correlated with the invasion success of fungi has not been attempted previously. 2. We addressed this question by constructing an ad hoc data set including invasive and non-invasive species of forest pathogenic fungi introduced into Europe. Data were analysed with a machine learning method based on classification trees (Random Forest). The performance of the classification rule based on species traits was compared with that of several random decision rules, and the principal trait predictors associated with invasive species were identified. 3. Invasion success was more accurately predicted by the classification rule including biological traits than by random decision rules. The effect of species traits was maintained when confounding variables linked to residence time and habitat availability were included. The selected traits were unlikely to be affected by a phylogenetic bias as invasive and non-invasive species were evenly distributed in fungal clades. 4. The species-level predictors identified as useful for distinguishing between invasive and non-invasive species were traits related to long-distance dispersal, sexual reproduction (in addition to asexual reproduction), spore shape and size, number of cells in spores, optimal temperature for growth and parasitic specialization (host range and infected organs). 5. Synthesis and applications. This study demonstrates that some species-level traits are predictors of invasion success for forest pathogenic fungi in Europe. These traits could be used to refine current pest risk assessment (PRA) schemes. Our results suggest that current schemes, which are mostly based on sequential questionnaires, could be improved by taking into account trait interactions or combinations. More generally, our results confirm the interest of machine learning methods, such as Random Forest, for species classification in ecology.

Wild and cultivated plants represent very different habitats for pathogens, especially when cultivated plants bear qualitative resistance genes. Here, we investigated to what extent the population genetic structure of a plant pathogenic fungus collected on its wild host can be impacted by the deployment of resistant cultivars. We studied one of the main poplar diseases, poplar rust, caused by the fungus Melampsora larici-populina. A thousand and fifty individuals sampled from several locations in France were pheno-typed for their virulence profile (ability to infect or not the most deployed resistant cultivar 'Beaupre'), and a subset of these was genotyped using 25 microsatellite markers. Bayesian assignment tests on genetic data clustered the 476 genotyped individuals into three genetic groups. Group 1 gathered most virulent individuals and displayed evidence for selection and drastic demographic changes resulting from breakdown of the poplar cultivar 'Beaupre'. Group 2 comprised individuals corresponding to ancestral populations of M. larici-populina naturally occurring in the native range. Group 3 displayed the hallmarks of strict asexual reproduction, which has never previously been demonstrated in this species. We discuss how poplar cultivation has influenced the spatial and genetic structure of this plant pathogenic fungus, and has led to the spread of virulence alleles (gene swamping) in M. larici-populina populations evolving on the wild host.

Background Localized scleroderma also called morphea is a skin disorder of undetermined cause. The widely recognized Mayo Clinic Classification identifies 5 main morphea types: plaque, generalized, bullous, linear and deep. Whether each of these distinct types has a particular clinical course or is associated with some patient-related features is still unclear. Methods We report here a retrospective series of patients with localized scleroderma with an attempt to identify features related to the type of lesion involved. The medical records of all patients with a diagnosis of localized scleroderma were reviewed by skilled practitioners. Lesions were classified according to the Mayo Clinic Classification. The relationship between each lesion type and various clinical features was tested by non-parametrical methods. Results The sample of 52 patients included 43 females and 9 males. Median age at onset was 30 y (range 1–76). Frequencies of patients according to morphea types were: plaque morphea 41 (78.8%) (including morphea en plaque 30 (57.7%) and atrophoderma of Pasini–Pierini 11 (21.1%)), linear scleroderma 14 (26.9%). Nine patients (17.3%) had both types of localized scleroderma. Median age at onset was lower in patients with linear scleroderma (8 y (range 3–44)) than in others (36 y (range 1–77)) (p = 0.0003). Head involvement was more common in patients with linear scleroderma (37.5%) than in other subtypes (11.1%) (p = 0.05). Atrophoderma of Pasini–Pierini was never located at the head. Systemic symptoms, antinuclear antibodies and the rheumatic factor were not associated with localized scleroderma types or subtypes. Conclusion These results suggest that morphea types, in adults are not associated with distinct patient features except for age at disease onset (lower) and the localization on the head (more frequent), in patients with lesions of the linear type.