Genetic population structure of the invasive ash dieback pathogen Hymenoscyphus fraxineus in its expanding range

Burokienė, Daiva; Prospero, Simone; Jung, Esther; Marčiulynienė, Diana; Moosbrugger, K; Norkutė, Goda; Rigling, Daniel; Lygis, Vaidotas; Schoebel, Corine N.

doi:10.1007/s10530-015-0911-6

Cited by 46 publications

(59 citation statements)

References 58 publications

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“…Collectively, the present observations on VC, SNP markers, mating types and virus frequency point to the UK population being founded by numerous genetic individuals from continental Europe, although H. fraxineus throughout Europe appears to have originated from a single founder population (Gross et al ., ; Burokiene et al ., ; Schoebel et al ., ) followed by long‐distance dispersal by means of sexually produced spores. The results of the present study, demonstrating many unique individuals at each location, do not provide evidence for clonal reproduction and consequently do not indicate a role for substantial dispersal by asexual inoculum as proposed by Fones et al .…”

Section: Discussionmentioning

confidence: 99%

Population structure of the ash dieback pathogen, Hymenoscyphus fraxineus, in relation to its mode of arrival in the UK

et al. 2017

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The ash dieback fungus, Hymenoscyphus fraxineus, a destructive, alien pathogen of common ash (Fraxinus excelsior), has spread across Europe over the past 25 years and was first observed in the UK in 2012. To investigate the relationship of the pathogen's population structure to its mode of arrival, isolates were obtained from locations in England and Wales, either where established natural populations of ash had been infected by wind‐dispersed ascospores or where the fungus had been introduced on imported planting stock. Population structure was determined by tests for vegetative compatibility (VC), mating type and single‐nucleotide polymorphisms (SNPs). VC heterogeneity was high at all locations, with 96% of isolate pairings being incompatible. Frequencies of the MAT1‐1‐1 and MAT1‐2‐1 idiomorphs were approximately equal, consistent with H. fraxineus being an obligate outbreeder. Most SNP variation occurred within study location and there was little genetic differentiation between the two types of location in the UK, or between pathogen populations in the UK and continental Europe. There was modest differentiation between UK subpopulations, consistent with genetic variation between source populations in continental Europe. However, there was no evidence of strong founder effects, indicating that numerous individuals of H. fraxineus initiated infection at each location, regardless of the route of pathogen transmission. The ssRNA virus HfMV1 was present at moderate to high frequencies in all UK subpopulations. The results imply that management of an introduced plant pathogen requires action against its spread at the continental level involving coordinated efforts by European countries.

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Section: Discussionmentioning

confidence: 99%

Population structure of the ash dieback pathogen, Hymenoscyphus fraxineus, in relation to its mode of arrival in the UK

et al. 2017

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“…; Burokiene et al . ). However, only low resolution and the lack of a genetic population structure across the expanding range of the pathogen was detected using a decent set of markers.…”

Section: Introductionmentioning

confidence: 97%

“…; Burokiene et al . ) using microsatellite markers. At most loci, a bi‐allelic structure was detected, and thus, it was suggested that possibly only two individuals had been introduced (Gross et al .…”

Section: Introductionmentioning

confidence: 99%

Population genetic analysis of a parasitic mycovirus to infer the invasion history of its fungal host

et al. 2017

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Hymenoscyphus fraxineus mitovirus 1 (HfMV1) occurs in the fungus Hymenoscyphus fraxineus, an introduced plant pathogen responsible for the devastating ash dieback epidemic in Europe. Here, we explored the prevalence and genetic structure of HfMV1 to elucidate the invasion history of both the virus and the fungal host. A total of 1298 H. fraxineus isolates (181 from Japan and 1117 from Europe) were screened for the presence of this RNA virus and 301 virus-positive isolates subjected to partial sequence analysis of the viral RNA polymerase gene. Our results indicate a high mean prevalence (78.7%) of HfMV1 across European H. fraxineus isolates, which is supported by the observed high transmission rate (average 83.8%) of the mitovirus into sexual spores of its host. In accordance with an expected founder effect in the introduced population in Europe, only 1.1% of the Japanese isolates were tested virus positive. In Europe, HfMV1 shows low nucleotide diversity but a high number of haplotypes, which seem to be subject to strong purifying selection. Phylogenetic and clustering analysis detected two genetically distinct HfMV1 groups, both present throughout Europe. This pattern supports the hypothesis that only two (mitovirus-carrying) H. fraxineus individuals were introduced into Europe as previously suggested from the bi-allelic nature of the fungus. Moreover, our data points to reciprocal mating events between the two introduced individuals, which presumably initiated the ash dieback epidemic in Europe.

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“…This occurrence was previously discussed by Burokiene et al (2015) but may also be disregarded, as H. fraxineus is a strictly outcrossing fungus. This occurrence was previously discussed by Burokiene et al (2015) but may also be disregarded, as H. fraxineus is a strictly outcrossing fungus.…”

Section: Discussionmentioning

confidence: 94%

“…Compared to previous studies aimed at population diversity on a larger scale (Burokiene et al, 2015) or a local scale with a single sampling effort (Nguyen et al, 2016), we were able not only to provide a survey of the genetic diversity of H. fraxineus on a local scale but also to trace particular genotypes from the infected petiole into the shoot, where they caused necrosis the following season. Compared to previous studies aimed at population diversity on a larger scale (Burokiene et al, 2015) or a local scale with a single sampling effort (Nguyen et al, 2016), we were able not only to provide a survey of the genetic diversity of H. fraxineus on a local scale but also to trace particular genotypes from the infected petiole into the shoot, where they caused necrosis the following season.…”

Section: Discussionmentioning

confidence: 98%

Direct evidence of Hymenoscyphus fraxineus infection pathway through the petiole‐shoot junction

et al. 2017

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The symptoms of ash dieback caused by the fungus Hymenoscyphus fraxineus include wilting of the foliage followed by dieback of shoots, twigs and branches. Necroses in shoots are assumed to develop after infection through leaf petioles; however, clear evidence of this infection pathway has not yet been provided. Considering the multiple pathogen genotypes in dead ash petioles, we aimed to obtain a spatial overview of all H. fraxineus genotypes colonizing individual shoots and their corresponding petioles before leaf shedding to acquire precise information about the infection biology of H. fraxineus and its ability to cross the petiole-shoot junction. Individual genotypes of H. fraxineus were characterized by the analysis of microsatellites using DNA extracted directly from petiole segments or cultures isolated from the segments. We detected 150 different multilocus genotypes in 10 analysed shoots and their respective petioles; the highest number of genotypes was eight for a single petiole and three for a single shoot. The genotypes of most shoot lesions were identical to particular genotypes from the proximal segments of petioles, implicating the main pathway of shoot infections. To test whether the amount of colonized substrate or intraspecific competition have an effect on successful infection, genotypes that reached the most proximal end of the petioles were scored for the number of invaded petiole segments and for the number of other H. fraxineus genotypes co-occurring in the segments. However, the extent of colonization of the scored genotypes and intraspecific competition with other H. fraxineus strains did not influence pathogen success in entering the shoot.This study confirms that the majority of ash shoot infections are caused by genotypes of H. fraxineus originating from petioles. Compared to petioles, the frequency of shoot colonization as well as number of H. fraxineus genotypes in shoots was much lower.

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Genetic population structure of the invasive ash dieback pathogen Hymenoscyphus fraxineus in its expanding range

Cited by 46 publications

References 58 publications

Population structure of the ash dieback pathogen, Hymenoscyphus fraxineus, in relation to its mode of arrival in the UK

Population structure of the ash dieback pathogen, Hymenoscyphus fraxineus, in relation to its mode of arrival in the UK

Population genetic analysis of a parasitic mycovirus to infer the invasion history of its fungal host

Direct evidence of Hymenoscyphus fraxineus infection pathway through the petiole‐shoot junction

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