The Relationship between Fungal Diversity and Invasibility of a Foliar Niche—The Case of Ash Dieback

European ash (<i>Fraxinus excelsior</i>) is threatened by the invasive ascomycete <i>Hymenoscyphus fraxineus</i> originating from Asia. Ash leaf tissues serve as a route for shoot infection but also as a sporulation substrate for this pathogen. Knowledge of the leaf niche par...

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Published in:Journal of Fungi
Main Authors: Ahto Agan, Rein Drenkhan, Kalev Adamson, Leho Tedersoo, Halvor Solheim, Isabella Børja, Iryna Matsiakh, Volkmar Timmermann, Nina Elisabeth Nagy, Ari Mikko Hietala
Format: Article
Language:English
Published: MDPI AG 2020-08-01
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Online Access:https://www.mdpi.com/2309-608X/6/3/150
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author Ahto Agan
Rein Drenkhan
Kalev Adamson
Leho Tedersoo
Halvor Solheim
Isabella Børja
Iryna Matsiakh
Volkmar Timmermann
Nina Elisabeth Nagy
Ari Mikko Hietala
author_facet Ahto Agan
Rein Drenkhan
Kalev Adamson
Leho Tedersoo
Halvor Solheim
Isabella Børja
Iryna Matsiakh
Volkmar Timmermann
Nina Elisabeth Nagy
Ari Mikko Hietala
author_sort Ahto Agan
collection DOAJ
container_title Journal of Fungi
description European ash (<i>Fraxinus excelsior</i>) is threatened by the invasive ascomycete <i>Hymenoscyphus fraxineus</i> originating from Asia. Ash leaf tissues serve as a route for shoot infection but also as a sporulation substrate for this pathogen. Knowledge of the leaf niche partitioning by indigenous fungi and <i>H. fraxineus</i> is needed to understand the fungal community receptiveness to the invasion. We subjected DNA extracted from unwashed and washed leaflets of healthy and diseased European ash to PacBio sequencing of the fungal <i>ITS1-5.8S-ITS2</i> rDNA region. Leaflets from co-inhabiting rowan trees (<i>Sorbus aucuparia</i>) served as a reference. The overlap in leaflet mycobiomes between ash and rowan was remarkably high, but unlike in rowan, in ash leaflets the sequence read proportion, and the qPCR-based DNA amount estimates of <i>H. fraxineus</i> increased vigorously towards autumn, concomitant with a significant decline in overall fungal richness. The niche of ash and rowan leaves was dominated by epiphytic propagules (<i>Vishniacozyma</i> yeasts, the dimorphic fungus <i>Aureobasidion pullulans</i> and the dematiaceous hyphomycete <i>Cladosporium ramotenellum</i> and <i>H. fraxineus</i>), and endophytic thalli of biotrophs (<i>Phyllactinia</i> and <i>Taphrina species</i>), the indigenous necrotroph <i>Venturia fraxini</i> and <i>H. fraxineus</i>. Mycobiome comparison between healthy and symptomatic European ash leaflets revealed no significant differences in relative abundance of <i>H. fraxineus</i>, but <i>A. pullulans</i> was more prevalent in symptomatic trees. The impacts of host specificity, spatiotemporal niche partitioning, species carbon utilization profiles and life cycle traits are discussed to understand the ecological success of <i>H. fraxineus</i> in Europe. Further, the inherent limitations of different experimental approaches in the profiling of foliicolous fungi are addressed.
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spelling doaj-art-e1c30ea0e38a4e25ae69a7621bebd00d2025-08-20T01:11:07ZengMDPI AGJournal of Fungi2309-608X2020-08-016315010.3390/jof6030150The Relationship between Fungal Diversity and Invasibility of a Foliar Niche—The Case of Ash DiebackAhto Agan0Rein Drenkhan1Kalev Adamson2Leho Tedersoo3Halvor Solheim4Isabella Børja5Iryna Matsiakh6Volkmar Timmermann7Nina Elisabeth Nagy8Ari Mikko Hietala9Natural History Museum and Institute of Ecology and Earth Sciences, University of Tartu, 50411 Tartu, EstoniaInstitute of Forestry and Rural Engineering, Estonian University of Life Sciences, 51006 Tartu, EstoniaInstitute of Forestry and Rural Engineering, Estonian University of Life Sciences, 51006 Tartu, EstoniaNatural History Museum and Institute of Ecology and Earth Sciences, University of Tartu, 50411 Tartu, EstoniaNorwegian Institute of Bioeconomy Research, p.b. 115, 1431 Ås, NorwayNorwegian Institute of Bioeconomy Research, p.b. 115, 1431 Ås, NorwayInstitute of Forestry and Park Gardening, Ukrainian National Forestry University, 79057 Lviv, UkraineNorwegian Institute of Bioeconomy Research, p.b. 115, 1431 Ås, NorwayNorwegian Institute of Bioeconomy Research, p.b. 115, 1431 Ås, NorwayNorwegian Institute of Bioeconomy Research, p.b. 2609, 7734 Steinkjer, NorwayEuropean ash (<i>Fraxinus excelsior</i>) is threatened by the invasive ascomycete <i>Hymenoscyphus fraxineus</i> originating from Asia. Ash leaf tissues serve as a route for shoot infection but also as a sporulation substrate for this pathogen. Knowledge of the leaf niche partitioning by indigenous fungi and <i>H. fraxineus</i> is needed to understand the fungal community receptiveness to the invasion. We subjected DNA extracted from unwashed and washed leaflets of healthy and diseased European ash to PacBio sequencing of the fungal <i>ITS1-5.8S-ITS2</i> rDNA region. Leaflets from co-inhabiting rowan trees (<i>Sorbus aucuparia</i>) served as a reference. The overlap in leaflet mycobiomes between ash and rowan was remarkably high, but unlike in rowan, in ash leaflets the sequence read proportion, and the qPCR-based DNA amount estimates of <i>H. fraxineus</i> increased vigorously towards autumn, concomitant with a significant decline in overall fungal richness. The niche of ash and rowan leaves was dominated by epiphytic propagules (<i>Vishniacozyma</i> yeasts, the dimorphic fungus <i>Aureobasidion pullulans</i> and the dematiaceous hyphomycete <i>Cladosporium ramotenellum</i> and <i>H. fraxineus</i>), and endophytic thalli of biotrophs (<i>Phyllactinia</i> and <i>Taphrina species</i>), the indigenous necrotroph <i>Venturia fraxini</i> and <i>H. fraxineus</i>. Mycobiome comparison between healthy and symptomatic European ash leaflets revealed no significant differences in relative abundance of <i>H. fraxineus</i>, but <i>A. pullulans</i> was more prevalent in symptomatic trees. The impacts of host specificity, spatiotemporal niche partitioning, species carbon utilization profiles and life cycle traits are discussed to understand the ecological success of <i>H. fraxineus</i> in Europe. Further, the inherent limitations of different experimental approaches in the profiling of foliicolous fungi are addressed.https://www.mdpi.com/2309-608X/6/3/150<i>Hymenoscyphus fraxineus</i><i>Venturia fraxini</i>mycobiomeepiphytic and endophytic fungiqPCRPacBio
spellingShingle Ahto Agan
Rein Drenkhan
Kalev Adamson
Leho Tedersoo
Halvor Solheim
Isabella Børja
Iryna Matsiakh
Volkmar Timmermann
Nina Elisabeth Nagy
Ari Mikko Hietala
The Relationship between Fungal Diversity and Invasibility of a Foliar Niche—The Case of Ash Dieback
<i>Hymenoscyphus fraxineus</i>
<i>Venturia fraxini</i>
mycobiome
epiphytic and endophytic fungi
qPCR
PacBio
title The Relationship between Fungal Diversity and Invasibility of a Foliar Niche—The Case of Ash Dieback
title_full The Relationship between Fungal Diversity and Invasibility of a Foliar Niche—The Case of Ash Dieback
title_fullStr The Relationship between Fungal Diversity and Invasibility of a Foliar Niche—The Case of Ash Dieback
title_full_unstemmed The Relationship between Fungal Diversity and Invasibility of a Foliar Niche—The Case of Ash Dieback
title_short The Relationship between Fungal Diversity and Invasibility of a Foliar Niche—The Case of Ash Dieback
title_sort relationship between fungal diversity and invasibility of a foliar niche the case of ash dieback
topic <i>Hymenoscyphus fraxineus</i>
<i>Venturia fraxini</i>
mycobiome
epiphytic and endophytic fungi
qPCR
PacBio
url https://www.mdpi.com/2309-608X/6/3/150
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