The different subspecies of Phytophthora alni, P. alni subsp. alni (Paa), P. alni subsp. uniformis (Pau), and P. alni subsp. multiformis (Pam), are recent and widespread pathogens of alder in Europe. They are believed to be a group of emergent heteroploid hybrids between two phylogenetically close Phytophthora species. Nuclear and mitochondrial DNA analyses were performed, using a broad collection of P. alni and two closely related species, P. cambivora and P. fragariae. Paa possesses three different alleles for each of the nuclear genes we studied, two of which are present in Pam as well, whereas the third matches the single allele present in Pau. Moreover, Paa displays common mtDNA patterns with both Pam and Pau. A combination of the data suggests that Paa may have been generated on several occasions by hybridization between Pam and Pau, or their respective ancestors. Pau might have P. cambivora as a species ancestor, whereas Pam seems to have either been generated itself by an ancient reticulation or by autopolyploidization.
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 phenotyped for their virulence profile (ability to infect or not the most deployed resistant cultivar 'Beaupré'), 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 'Beaupré'. 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.
The advent of molecular epidemiology has greatly improved our ability to identify the population sources and track the pathogen movement. Yet the wide spatial and temporal scales usually considered are useful only to infer historical migration pathways. In this study, Bayesian genetic assignments and a landscape epidemiology approach were combined to unravel genetic origin and annual spread during a single epidemic of a plant pathogen: the poplar rust fungus Melampsora larici-populina. The study focused on a particular area-the Durance River valley-which enabled inoculum sources to be identified and channelled spread of the epidemic along a one-dimensional corridor. Spatio-temporal monitoring of disease showed that the epidemic began in the upstream part of the valley and spread out downstream. Using genetic assignment tests, individuals collected at the end of the epidemic were sorted into two genetic groups; very few hybrids were detected, although individuals from both groups coexisted locally downstream in the valley. The epidemic originated from two genetically distinct inoculum sources. Individuals of each group then dispersed southwards along the Durance River and became mixed in poplar riparian stands. These two genetic groups were found previously at a wider spatial scale and proved to result from distinct evolutionary histories on either wild or cultivated poplars. This study showed that the two groups can mix during an epidemic but do not hybridize because they then reproduce asexually. In general, the methods employed here could be useful for elucidating the genetic origin and retracing the colonization history and migration pathways of recent epidemics.
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