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.

The recent availability of genome-wide sequencing techniques has allowed systematic screening for molecular signatures of adaptation, including in non-model organisms. Host-pathogen interactions constitute good models due to the strong selective pressures that they entail. We focused on an adaptive event which affected the poplar rust fungus Melampsora larici-populina when it overcame a resistance gene borne by its host, cultivated poplar. Based on 76 virulent and avirulent isolates framing narrowly the estimated date of the adaptive event, we examined the molecular signatures of selection. Using an array of genome scan methods based on different features of nucleotide diversity, we detected a single locus exhibiting a consistent pattern suggestive of a selective sweep in virulent individuals (excess of differentiation between virulent and avirulent samples, linkage disequilibrium, genotype-phenotype statistical association and long-range haplotypes). Our study pinpoints a single gene and further a single amino acid replacement which may have allowed the adaptive event. Although our samples are nearly contemporary to the selective sweep, it does not seem to have affected genome diversity further than the immediate vicinity of the causal locus, which can be explained by a soft selective sweep (where selection acts on standing variation) and by the impact of recombination in mitigating the impact of selection. Therefore, it seems that properties of the life cycle of M. larici-populina, which entails both high genetic diversity and outbreeding, has facilitated its adaptation.

Growing genetically resistant plants allows pathogen populations to be controlled and reduces the use of chemicals. However, pathogens can quickly overcome such resistance. In this context, how can we achieve sustainable crop protection? This crucial question has remained largely unanswered despite decades of intense debate and research effort. In this study, we used a bibliographic analysis to show that the research field of resistance durability has evolved into three subfields: (i) ‘plant breeding’ (generating new genetic material), (ii) ‘molecular interactions’ (exploring the molecular dialogue governing plant–pathogen interactions) and (iii) ‘epidemiology and evolution’ (explaining and forecasting of pathogen population dynamics resulting from selection pressure(s) exerted by resistant plants). We argue that this triple split of the field impedes integrated research progress and ultimately compromises the sustainable management of genetic resistance. After identifying a gap among the three subfields, we argue that the theoretical framework of population genetics could bridge this gap. Indeed, population genetics formally explains the evolution of all heritable traits, and allows genetic changes to be tracked along with variation in population dynamics. This provides an integrated view of pathogen adaptation, notably via evolutionary–epidemiological feedbacks. In this Opinion Note, we detail examples illustrating how such a framework can better inform best practice for developing and managing genetically resistant cultivars.

Melampsora larici-populina is an obligate biotrophic plant pathogen responsible for the poplar rust disease. This fungus belongs to the taxonomical order Pucciniales and exhibits a complex heteroecious and macrocyclic life cycle, i.e. it has the capacity to infect two unrelated host plants, larch and poplar, and to form five distinct spore types through the year. The M. larici-populina genome has been sequenced and annotated in 2011 and since, different transcriptomic analyses were conducted at different stages with oligoarrays and later on with RNA-Seq covering most of its life cycle. Here, we collected published transcriptome data for the poplar rust fungus, transposed them for the version 2 of the genome now available at the Joint Genome Institute Mycocosm website and performed normalization of different oligoarray datasets on one hand, and of RNA-Seq on the other hand. We report a comprehensive normalized dataset for this fungus, made available for the community, which allows life cycle transcriptomics analysis.

Growing genetically resistant plants allows pathogen populations to be controlled and reduces the use of pesticides. However, pathogens can quickly overcome such resistance. In this context, how can we achieve sustainable crop protection? This crucial question has remained largely unanswered despite decades of intense debate and research effort. In this study, we used a bibliographic analysis to show that the research field of resistance durability has evolved into three subfields: (i) 'plant breeding' (generating new genetic material), (ii) 'molecular interactions' (exploring the molecular dialogue governing plant-pathogen interactions) and (iii) 'epidemiology and evolution' (explaining and forecasting of pathogen population dynamics resulting from selection pressure(s) exerted by resistant plants). We argue that this triple split of the field impedes integrated research progress and ultimately compromises the sustainable management of genetic resistance. After identifying a gap among the three subfields, we argue that the theoretical framework of population genetics could bridge this gap. Indeed, population genetics formally explains the evolution of all heritable traits, and allows genetic changes to be tracked along with variation in population dynamics. This provides an integrated view of pathogen adaptation, in particular via evolutionary-epidemiological feedbacks. In this Opinion Note, we detail examples illustrating how such a framework can better inform best practices for developing and managing genetically resistant cultivars.

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 snap-shot of influential molecular plant immunity research, by identifying and analyzing 170 highly-cited publications (aka Highly-Influential Publications in molecular Plant Immunity; hereafter HIPPYs) published in this field between 2000 and 2019. Our analysis draws a broad analytical knowledge of 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 contribute to 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.

Zymoseptoria tritici is the fungal pathogen responsible for Septoria tritici blotch on wheat. Disease outcome in this pathosystem is partly determined by isolate-specific resistance, where wheat resistance genes recognize specific fungal factors triggering an immune response. Despite the large number of known wheat resistance genes, fungal molecular determinants involved in such cultivar-specific resistance remain largely unknown. We identified the avirulence factor AvrStb9 using association mapping and functional validation approaches. Pathotyping AvrStb9 transgenic strains on Stb9 cultivars, near isogenic lines and wheat mapping populations, showed that AvrStb9 interacts with Stb9 resistance gene, triggering an immune response. AvrStb9 encodes an unusually large avirulence gene with a predicted secretion signal and a protease domain. It belongs to a S41 protease family conserved across different filamentous fungi in the Ascomycota class and may constitute a core effector. AvrStb9 is also conserved among a global Z. tritici population and carries multiple amino acid substitutions caused by strong positive diversifying selection. These results demonstrate the contribution of an ‘atypical’ conserved effector protein to fungal avirulence and the role of sequence diversification in the escape of host recognition, adding to our understanding of host-pathogen interactions and the evolutionary processes underlying pathogen adaptation.

Background: The recent availability of genome-wide sequencing techniques has allowed systematic screening for molecular signatures of adaptation, including in non-model organisms. Host-pathogen interactions constitute good models due to the strong selective pressures that they entail. We focused on an adaptive event which affected the poplar rust fungus Melampsora larici-populina when it overcame a resistance gene borne by its host, cultivated poplar. Based on 76 virulent and avirulent isolates framing narrowly the estimated date of the adaptive event, we examined the molecular signatures of selection. Results: Using an array of genome scan methods, we detected a single locus exhibiting a consistent pattern suggestive of a selective sweep in virulent individuals (excess of differentiation between virulent and avirulent samples, linkage disequilibrium, genotype-phenotype statistical association and long-range haplotypes). Our study pinpoints a single gene and further a single amino acid replacement which may have allowed the adaptive event. Although the selective sweep occurred only four years earlier, it does not seem to have affected genome diversity further than the immediate vicinity of the causal locus. Conclusions: Our results suggest that M. larici-populina underwent a soft selective sweep and possibly a prominent effect of outbreeding and recombination, which we speculate have increased the efficiency of selection.