The Ash Dieback Pathogen Resists the Chemical Defences of Its Host Tree, European Ash, by Depleting Them From the Growth Medium

Plant pathogenic fungi are major drivers of disease in forest trees, often causing substantial ecological and economic damage. Ash dieback, caused by the ascomycete Hymenoscyphus fraxineus , has resulted in the widespread decline of Fraxinus excelsior populations throughout Europe. As infection is initiated in leaves containing diverse plant defensive metabolites, the ability of H. fraxineus to cope with host chemistry may determine successful host colonisation. We therefore investigated the responses of H. fraxineus to crude ash leaf extracts and individual defensive compounds. In contrast to the non‐ash associated fungi tested, H. fraxineus was not inhibited by crude methanolic leaf extracts or most plant defence compounds tested. In addition, H. fraxineus depleted ash compounds extensively from the growth medium. Consistent with these findings, untargeted metabolomics revealed extensive alterations of the ash leaf‐based medium by H. fraxineus , with 48% of detected chemical features being significantly reduced following fungal growth. Moreover, the growth of H. fraxineus was promoted by nearly all tested ash metabolites in minimal medium, indicating that these compounds can support fungal growth and may serve as carbon sources. Together, these results suggest that successful colonisation of ash tissues by H. fraxineus depends on its resistance to host defences, facilitated by its ability to deplete defensive compounds from colonised tissue.