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

Abstract

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.

Fungal colonization patterns in necrotic rootstocks and stem bases of dieback‐affected Fraxinus excelsior L.

“…Allelic diversity was low with a maximum of two observed alleles per marker. This bi‐allelic pattern has already been found and described in more detailed population genetic studies of H. fraxineus (Burokiene et al, ; Gross, Hosoya, & Queloz, ; Schoebel, Botella, Lygis, & Rigling, ). It points to a strong founder effect due to the limited initial number of two‐parent genotypes upon the introduction of H. fraxineus in Europe (McMullan et al, ).…”

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

“…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 .…”

“…The high heterogeneity in VC types implies that even if a deleterious virus were present, it could not spread rapidly and widely between fungal mycelia within a subpopulation. The high but variable frequency of HfMV1 is in accordance with the virus being transmitted and spread mainly via the ascospores (Schoebel et al ., ).…”

“…In continental Europe, the prevalence of the ssRNA virus HfMV1 was highly variable between different countries, ranging from 0% in Belgium and Slovenia to 91% in Switzerland (Schoebel et al ., ). Comparable virus frequencies were found at the different locations in the UK, ranging from 20% at LWD‐E to 100% at PND‐M.…”

Ash dieback epidemic in Europe: How can molecular technologies help?

“…Microsatellite markers [19], sequencing of parasitic mycoviruses [20], and genome sequencing [21] have been used to understand the population structure and genetic diversity of the invading H . fraxineus using isolates of the pathogen from Europe and Japan.…”