Friend or foe? Hymenoscyphus fraxineus causes ash dieback in Europe, but does not harm the trees in its original habitat

In 1992, strange symptoms of disease on a large number of ashes were reported from Poland. These consisted of areas of dead tissue on branches and stems, wilting and drying twigs, and prematurely shed leaves, and often resulted in the death of the tree. Soon, similar findings were reported from the Baltic States. During the following 20 years, the phenomenon spread across the entire geographic range of European ash, from Ireland in the west to Russia in the east, and from Sweden in the north to Italy in the south. The impact has varied from country to country, but in general more than  90 % of all trees were attacked and more than 60 %  killed. The remainder appear to be partly resistant or tolerant to the disease. This mass death of ash is commonly known as the European ash dieback.

Very small original population

The culprit of this vast drama is an Ascomycete fungus that over the years has been given several names, but since 2014 is known as Hymenoscyphus fraxineus. Population studies of the fungus has shown that the genetic differences between different parts of Europe are very small, which indicates that there is no population structure. In other words, the entire European population originates from a small number of individuals, a so-called genetic bottle neck. This is not uncommon for new serious epidemics, and is caused by a minor immigration of the pathogen from a different location. The host in the new location has no adapted defence against the disease, and the small original population can swiftly spread over a large area.

In the case of H. fraxineus, evidence points towards East Asia as the origin of the fungus. The East Asian broadleaf forest is populated by ash species such as Fraxinus mandshurica, Manchurian ash, but no outbreaks of Asian ash dieback has been reported. Yet, the fungus is present, and must thus play a different ecological part in its original habitat than it does after being introduced to Europe. This mystery is investigated in an article in Nature Scientific Reports, written by researchers from the Department of Forest Mycology and Plant Pathology and the Southern Swedish Forest Reserach Centre at the Swedish University of Agricultural Sciences.

The symptoms of European ash dieback. Photo: Food and Environment Research Agency - FERA.

Harmless in its natural environment

Michelle Cleary is the first author of the study. “One of our hypotheses was that H. fraxineus is not a pathogen in its natural environment, but an endophyte, dwelling in the leaves of the ash, neither harming nor helping the host in any tangible way. When the leaves are shed, the fungus switches to a saprophytic, decaying, growth stage and completes its sexual cycle. This would be a competitive advantage over other saprophytes, since the fungus would already be seated when the food is served, so to speak.”

To investigate this, Michelle Cleary studied leaves in healthy Manchurian ash without symptoms of disease in eastern Russia and used DNA-methods to detect the presence of H. fraxineus.

“We found H. fraxineus in 33 % of all healthy Manchurian ash trees”, Michelle says. “This is the first time the fungus is detected in ash trees completely free of symptoms, which strongly suggests that, in its original habitat, it has the capacity to live within the host as a non-pathogenic endophyte, or alternatively as a silent, mild pathogen. The European situation has however shown that this balance is probably unstable, and might tilt towards parasitism through the lack of adapted defences on a host with which it never co-evolved. But even on Manchurian ash planted in Europe, parasitism may be already happening, for example in hosts weakened by various forms of stress.”

Indeed, the potentially brittle balance of this interaction is highlighted in another study, on Manchurian ash planted in Estonia. These trees showed the very same disease symptoms as their European relatives, which contrasts to observations from Denmark and Sweden, where Manchurian ash growing next to H. fraxineus-infected European ash showed no symptoms at all. It is possible that the Estonian forest was somehow particularly unsuitable for Manchurian ash, which could have stressed the trees and caused the fungus to go from endophyte to pathogen.

“We also compared the Asian H. fraxineus population to the European, and found that the Asian one is much more genetically varied. This obviously supports the idea that the European population went through a bottle neck and sprung from a small, migrated fraction of the Asian population.”

Fungi unique for Manchurian ash

Finally, the scientists used DNA methods to compare the fungal community associated with Manchurian ash to that associated with European. “Not surprisingly, we found large similarities in community composition between the species”, says Professor Jan Stenlid, another author of the study. “Most strikingly however was that the commonest species on Manchurian ash, Mycosphaerella, present on 99 % of those trees, was not found at all on European ash. Mycosphaerella-species play many parts on tree leaves and presently we cannot tell how and if they affect the host health, but since the trees were specifically selected for being free of disease symptoms, they are probably not pathogenic. It is tempting to imagine that the strong presence of endophytic Mycosphaerella-species somehow inhibits other fungi, such as H. fraxineus, from transitioning into pathogens. There are no evidence for such mechanisms, but it would be exciting to investigate further.”

“What the study does show, however, is that H. fraxineus grows in healthy, asymptomatic leaves of Manchurian ash without visibly hurting the host, and that the genetic variation in the Asian fungal population is much larger than in the European”, Jan Stenlid summarizes. “This is very interesting information for the growing understanding of the origin and nature of ash dieback.”