Evolution of morphological but not aggressiveness‐related traits following a major resistance breakdown in the poplar rust fungus, Melampsora larici‐populina

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 analysed 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

Association of two co-occurring mutations at the AvrMlp7 avirulence locus in poplar rust during the breakdown of RMlp7 resistance gene

International audienceThe deployment of plant varieties carrying resistance (R) genes exerts strong selection pressures towards pathogen populations. Several studiesreported the rapid evolution of avirulence (Avr) genes to escape R-mediated plant immunity and identified a variety of mechanisms leading tovirulence. The poplar rust fungus Melampsora larici-populina is the most damaging pathogen of poplars. A major adaptive event occurred in1994 with the breakdown of RMlp7 resistance gene in poplar in Europe. Population genomics studies identified a locus in the genome of M.larici-populina, which likely corresponds to the AvrMlp7 candidate avirulence gene. We used a population genetics approach combined withdedicated qPCR assays on a comprehensive set of 281 isolates, covering 27 years (encompassing the resistance breakdown event), to validate thecandidate locus and to assess its polymorphism. We found two mechanisms, a point mutation and a deletion, that allowed the pathogen to escapeRMlp7-mediated resistance. Six diploid genotypes were thus characterized at the candidate locus (three avirulent and three virulent). In addition,a temporal analysis revealed that the two virulence alleles pre-existed (harbored as avirulent heterozygous genotypes) since the early samplingsand were found in association (as virulent genotypes) at the time of the resistance breakdown. Our study documented that, in a diploid pathogen,combining virulence determinisms is adaptive

Association of two co-occurring mutations at the AvrMlp7 avirulence locus in poplar rust during the breakdown of RMlp7 resistance gene: [Poster]

International audienceThe deployment of plant varieties carrying resistance (R) genes exerts strong selection pressures towards pathogen populations. Several studies reported the rapid evolution of avirulence (Avr) genes to escape R-mediated plant immunity and identified a variety of mechanisms leading to virulence. The poplar rust fungus Melampsora larici-populina is the most damaging pathogen of poplars. A major adaptive event occurred in 1994 with the breakdown of RMlp7 resistance gene in poplar in Europe. Population genomics studies identified a locus in the genome of M. larici-populina, which likely corresponds to the AvrMlp7 candidate avirulence gene. We used a population genetics approach combined with dedicated qPCR assays on a comprehensive set of 281 isolates, covering 27 years (encompassing the resistance breakdown event), to validate the candidate locus and to assess its polymorphism. We found two mechanisms, a point mutation and a deletion, that allowed the pathogen to escape RMlp7-mediated resistance. Six diploid genotypes were thus characterized at the candidate locus (three avirulent and three virulent). In addition, a temporal analysis revealed that the two virulence alleles pre-existed (harbored as avirulent heterozygous genotypes) since the early samplings and were found in association (as virulent genotypes) at the time of the resistance breakdown. Our study documented that, in a diploid pathogen, combining virulence determinisms is adaptive

A point mutation and large deletion at the candidate avirulence locus AvrMlp7 in the poplar rust fungus correlate with poplar RMlp7 resistance breakdown

International audienceThe 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

Association of two co-occurring mutations at the AvrMlp7 avirulence locus in poplar rust during the breakdown of RMlp7 resistance gene: [Poster]

International audienceThe deployment of plant varieties carrying resistance (R) genes exerts strong selection pressures towards pathogen populations. Several studies reported the rapid evolution of avirulence (Avr) genes to escape R-mediated plant immunity and identified a variety of mechanisms leading to virulence. The poplar rust fungus Melampsora larici-populina is the most damaging pathogen of poplars. A major adaptive event occurred in 1994 with the breakdown of RMlp7 resistance gene in poplar in Europe. Population genomics studies identified a locus in the genome of M. larici-populina, which likely corresponds to the AvrMlp7 candidate avirulence gene. We used a population genetics approach combined with dedicated qPCR assays on a comprehensive set of 281 isolates, covering 27 years (encompassing the resistance breakdown event), to validate the candidate locus and to assess its polymorphism. We found two mechanisms, a point mutation and a deletion, that allowed the pathogen to escape RMlp7-mediated resistance. Six diploid genotypes were thus characterized at the candidate locus (three avirulent and three virulent). In addition, a temporal analysis revealed that the two virulence alleles pre-existed (harbored as avirulent heterozygous genotypes) since the early samplings and were found in association (as virulent genotypes) at the time of the resistance breakdown. Our study documented that, in a diploid pathogen, combining virulence determinisms is adaptive