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

ABSTRACT: 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.

SUBMITTER: Orton ES

PROVIDER: S-EPMC5832303 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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

Orton E S ES Brasier C M CM Bilham L J LJ Bansal A A Webber J F JF Brown J K M JKM

Plant pathology. 20170926 2

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 bee ...[more]

PMID: 29527064

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Project description:Five species of Hymenoscyphus that fruit on black stromatized parts of dead leaves of deciduous trees are presented, giving details on their morphological and ecological characteristics. Several of these species have previously been misplaced in rutstroemiaceous genera because of the presence of a substratal stroma. However, the heteropolar, scutuloid ascospores with an often hook-like lateral protrusion at the rounded apex and the ascus apical ring of the Hymenoscyphus-type represent two reliable morphological characteristics that, together with molecular data, provide clear evidence for their placement in the genus Hymenoscyphus (Helotiaceae). Among the species treated is Hymenoscyphus fraxineus (=Hymenoscyphus pseudoalbidus), the causal agent of the European ash dieback disease. Since 1992 this species started within Europe to replace the rather uncommon Hymenoscyphus albidus, which is likewise confined to leaves of Fraxinus. Hy. fraxineus has been recorded already since 1990 in Eastern Asia (Japan, Korea, northeast of China), where it had been initially misidentified as Lambertella albida (?Hy. albidus). In these regions, it occurs as a harmless saprotroph on Fraxinus mandshurica and Fraxinus rhynchophylla, suggesting that those populations are native while the European ash dieback disease has a recent Eastern Asiatic origin. The distinctly higher genetic diversity found in Japanese Hy. fraxineus in contrast to European Hy. fraxineus supports this view. Genetic similarities between Japanese Hy. fraxineus and European Hy. albidus suggest that also Hy. albidus might be a descendant of Asian Hy. fraxineus, though having invaded Europe much earlier. However, consistent genetic deviation between European and Asian Hy. fraxineus at two nucleotide positions of the ITS region indicates that the European ash disease originates from a region different from the presently known areas in Eastern Asia. Our results underline the importance of detailed morphological studies in combination with molecular work. Hy. fraxineus was described from Europe as a cryptic species that differed from Hy. albidus by molecular data alone. However, the Hy. albidus/Hy. fraxineus species complex represents one of many examples within the ascomycetes in which subtle microscopic differences between closely related species, in this case the presence or absence of croziers at the ascus base, are strictly correlated with molecular characteristics. Two species that closely resemble Hy. albidus and Hy. fraxineus form pseudosclerotia in Aesculus leaves and again differ from each other mainly in the ascus base: Hymenoscyphus aesculi on Aesculus hippocastanum from Europe lacks croziers, whereas Hymenoscyphus honshuanus from Japan on Aesculus turbinata possesses croziers. Other taxa treated here include Hymenoscyphus vacini, a European species growing on stromatized net veins of skeletonized leaves of Acer, and Hymenoscyphus torquatus, a Chinese species on unidentified herbaceous stems. An equivalent stroma-forming North American species on leaves of Fraxinus, Rutstroemia longipes (Rutstroemiaceae), is discussed and compared. A key to the Hymenoscyphus species that form a dark stroma on leaves of Acer, Aesculus, Fraxinus, and Picrasma is provided.

Project description:The invasive ascomycete Hymenoscyphus fraxineus has been threatening Fraxinus excelsior populations throughout Europe for over two decades. Since the infection and first colonization by the pathogen occurs in leaves, leaf-colonizing microorganisms have been discussed as a barrier and as possible biocontrol agents against the disease. To identify fungal groups with health-supporting potential, we compared the fungal microbiota of compound leaves from susceptible and tolerant ash trees in four ash stands with high H. fraxineus exposure. The fungal communities were analyzed both culture-independently by ITS2 amplicon sequencing and by the taxonomic classification of 1,704 isolates using matrix-assisted laser desorption/ionization time of flight mass spectrometry (MALDI-TOF MS) or sequencing of the entire ITS region. The fungal community structure did not show significant differences depending on the health status. However, for several OTUs and a MALDI group, a significantly higher abundance was found in tolerant ash trees. Thus, the yeast Papiliotrema flavescens was significantly increased and accounted for 12.3% of the mycobiome of tolerant ashes (OTU0003), and it had also a distinctly higher abundance among the isolates. The filamentous ascomycete Sarocladium strictum was increased 24-fold among the isolates of tolerant trees, but its abundance was comparably low. An in vitro screening for the growth inhibition of the pathogen via cocultivation resulted in 28 yeast-like isolates and 79 filamentous fungi with antagonistic activity. A statistical cocultivation test on two H. fraxineus strains confirmed six of the yeast-like isolates that suppressed H. fraxineus significantly, from 39-50%, two of them through a fungicidal effect. The highest inhibition rates among the yeasts were found for three isolates belonging to Aureobasidium pullulans and P. flavescens. The cocultivation test of the filamentous isolates revealed higher effects compared to the yeasts. Four isolates showed significant inhibition of both H. fraxineus strains with a rate of 72-100%, and five further isolates inhibited only one H. fraxineus strain significantly. The most effective isolates were members of the genus Cladosporium. During the next step, in planta tests will be necessary to verify the efficacy of the antagonistic isolates and to assess their suitability as biocontrol agents.

Dataset Information

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

Publications

Population structure of the ash dieback pathogen, <i>Hymenoscyphus fraxineus</i>, in relation to its mode of arrival in the UK.

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