Department of Fungal Forest and Crop Plant Diseases, Division of Plant Health and Biotechnology, Norwegian Institute of Bioeconomy Research, Pb. 115, NO-1431 As, Norway
Dr. Ari M. Hietala
Department of Fungal Forest and Crop Plant Diseases, Division of Plant Health and Biotechnology, Norwegian Institute of Bioeconomy Research, Pb. 115, NO-1431 As, Norway
European ash (Fraxinus excelsior) is threatened by the invasive ascomycete Hymenoscyphus fraxineus 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 H. fraxineus 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 ITS1-5.8S-ITS2 rDNA region. Leaflets from co-inhabiting rowan trees (Sorbus aucuparia) 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 H. fraxineus 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 (Vishniacozyma yeasts, the dimorphic fungus Aureobasidion pullulans and the dematiaceous hyphomycete Cladosporium ramotenellum and H. fraxineus), and endophytic thalli of biotrophs (Phyllactinia and Taphrina species), the indigenous necrotroph Venturia fraxini and H. fraxineus. Mycobiome comparison between healthy and symptomatic European ash leaflets revealed no significant differences in relative abundance of H. fraxineus, but A. pullulans 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 H. fraxineus in Europe. Further, the inherent limitations of different experimental approaches in the profiling of foliicolous fungi are addressed.
The relationship between the ecological success of needle pathogens of forest trees and species richness of co-inhabiting endophytic fungi is poorly understood. One of the most dangerous foliar pathogens of pine is Dothistroma septosporum, which is a widely spread threat to northern European forests. We sampled two Pinus sylvestris sites in Estonia and two in Norway in order to analyse the relations between the abundance of D. septosporum and overall fungal richness, specific fungal species composition, time of season, needle age and position in the canopy. In both countries, the overall species richness of fungi was highest in autumn, showing a trend of increase with needle age. The overall species richness in the second-year needles in Estonia and third-year needles in Norway was similar, suggesting that a critical colonization threshold for needle shed in P. sylvestris is breached earlier in Estonia than in Norway. The fungal species richness in P. sylvestris needles was largely affected by Lophodermium conigenum. Especially in older needles, the relative abundance of L. conigenum was significantly higher in spring compared to summer or autumn. The timing of recruitment and colonization mechanisms of different foliage endophytes are shortly discussed.
Globally, billions of tons of carbon sequestered in trees are annually recycled back to the atmosphere through wood decomposition by microbes. In Norway, every fifth Norway spruce shows at final harvest infection by pathogenic white-rot fungi in the genera Heterobasidion and Armillaria. As these fungi can mineralize all components of wood, we predicted that they have a significant carbon footprint. Gas samples taken from infected stems were analyzed for CO2 and CH4 concentrations, and wood samples from different parts of the decay columns were incubated under hypoxic (4% O2) and anoxic laboratory conditions. In spring and summer the stem concentrations of CO2 were generally two times higher in trees with heartwood decay than in healthy trees. For most of the healthy trees and trees with heartwood decay, mean stem concentrations of CH4 were comparable to ambient air, and only some Armillaria infected trees showed moderately elevated CH4. Consistently, low CH4 production potentials were recorded in the laboratory experiment. Up-scaling of CO2 efflux due to wood decay in living trees suggests that the balance between carbon sequestration and emission may be substantially influenced in stands with high frequency of advanced root and stem heartwood decay.
Dieback of European ash, caused by the ascomycete Hymenoscyphus fraxineus originating from Asia, has rapidly spread across Europe, and is threatening this keystone tree at a continental scale. High propagule pressure is characteristic to invasive species. Consistently, the enormous production of windborne ascospores by H. fraxineus in an ash forest with epidemic level of disease obviously facilitates its invasiveness and long distance spread. To understand the rate of build-up of propagule pressure by this pathogen following its local introduction, during 2011–2017 we monitored its sporulation at a newly infested ash stand in south-western Norway characterized with mild winters and cool summers. We also monitored the propagule pressure by Hymenoscyphus albidus, a non-pathogenic native species that competes for the same sporulation niche with H. fraxineus. During the monitoring period, crown condition of ash trees had impaired, and 20% of the dominant trees were severely damaged in 2017. H. fraxineus showed an exponential increase in spore production between 2012 and 2015, followed by drastic decline in 2016 and 2017. During 2011–2013, the two Hymenoscyphus species showed similar sporulation level, but thereafter spores of H. albidus were no longer detected. The data suggest that following local introduction, the population of H. fraxineus reaches rapidly an exponential growth stage if the local weather conditions are favorable for ascomata maturation across years. In the North Atlantic climate, summer temperatures critically influence the pathogen infection pressure, warm summers allowing the population to grow according to its biotic potential, whereas cold summers can cause a drastic decline in propagule pressure.
Some common ash trees (Fraxinus excelsior) show tolerance towards shoot dieback caused by the invasive ascomycete Hymenoscyphus fraxineus. Leaf petioles are considered to serve as a pathogen colonization route to the shoots. We compared four common ash clones with variation in disease tolerance, and included the native host, Manchurian ash (Fraxinus mandshurica), as a reference. Tissue colonization, following rachis inoculation by H. fraxineus, was monitored by histochemical observations and a quantitative polymerase chain reaction (qPCR) assay specific to H. fraxineus. Axial spread of the pathogen towards the petiole base occurred primarily within the phloem and parenchyma, tissues rich in starch in healthy petioles. In inoculated petioles, a high content of phenolics surrounded the hyphae, presumably a host defense response. There was a relationship between field performance and susceptibility to leaf infection in three of the four studied common ash clones, i.e., good field performance was associated with a low petiole colonization level and vice versa. Low susceptibility to leaf infection may counteract leaf-to-shoot spread of the pathogen in common ash, but the limited number of clones studied warrants caution and a larger study. The Manchurian ash clone had the highest petiole colonization level, which may suggest that this native host has evolved additional mechanisms to avoid shoot infection.