Fungi in the class Leotiomycetes are ecologically diverse, including mycorrhizas, endophytes of roots and leaves, plant pathogens, aquatic and aero-aquatic hyphomycetes, mammalian pathogens, and saprobes. These fungi are commonly detected in cultures from diseased tissue and from environmental DNA extracts. The identification of specimens from such character-poor samples increasingly relies on DNA sequencing. However, the current classification of Leotiomycetes is still largely based on morphologically defined taxa, especially at higher taxonomic levels. Consequently, the formal Leotiomycetes classification is frequently poorly congruent with the relationships suggested by DNA sequencing studies. Previous class-wide phylogenies of Leotiomycetes have been based on ribosomal DNA markers, with most of the published multi-gene studies being focussed on particular genera or families. In this paper we collate data available from specimens representing both sexual and asexual morphs from across the genetic breadth of the class, with a focus on generic type species, to present a phylogeny based on up to 15 concatenated genes across 279 specimens. Included in the dataset are genes that were extracted from 72 of the genomes available for the class, including 10 new genomes released with this study. To test the statistical support for the deepest branches in the phylogeny, an additional phylogeny based on 3156 genes from 51 selected genomes is also presented. To fill some of the taxonomic gaps in the 15-gene phylogeny, we further present an ITS gene tree, particularly targeting ex-type specimens of generic type species. A small number of novel taxa are proposed: Marthamycetales ord. nov., and Drepanopezizaceae and Mniaeciaceae fams. nov. The formal taxonomic changes are limited in part because of the ad hoc nature of taxon and specimen selection, based purely on the availability of data. The phylogeny constitutes a framework for enabling future taxonomically targeted studies using deliberate specimen selection. Such studies will ideally include designation of epitypes for the type species of those genera for which DNA is not able to be extracted from the original type specimen, and consideration of morphological characters whenever genetically defined clades are recognized as formal taxa within a classification.

Under the rules for the naming of fungi with pleomorphic life-cycles adopted in July 2011, the nomenclaturally correct name for the fungus causing the current ash dieback in Europe is determined to be Hymenoscyphus fraxineus, with the basionym Chalara fraxinea, and Hymenoscyphus pseudoalbidus as a taxonomic synonym of H. fraxineus.

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.

A list of all generic names that have been connected with the Orbiliomycetes is provided. Recommendations are made as to which names should be used in accordance with the rules and the different generic concepts. There is a mismatch in the current generic concepts within Orbiliomycetes regarding the two morphs: a narrow concept is used for the asexual morphs, but a broad concept relies on the sexual morphs. As a consequence, many more generic names have been established for the asexual morphs. A number of previous generic concepts are artificial, since they were based on single characters without molecular support. In order to provide solutions for this mismatch, we present three different generic concepts within the Orbiliomycetes. A broad concept recognizes a large genus Orbilia, with which most of the listed names fall into synonymy, but could be maintained as infrageneric names. Due to the lack of data proving phylogenetic relationships, this broad concept, at present, is the most practicable and recommended one. A moderate concept subdivides Orbilia into several genera, with all nematode-trapping fungi merged in Arthrobotrys. A narrow generic concept accepts genera based on differences in trapping organs, but also subdivides the remaining groups of Orbilia into additional genera. Trapping of invertebrates (zoophagy) is not restricted to Arthrobotrys in a broad sense, but occurs also in the more distant basal genera Hyalorbilia and Lecophagus, which mainly prey on rhizopods and rotifers. Whether these predatory capabilities trace back to a common ancestor is not clear. The following new combinations are proposed: Hyalorbilia oviparasitica, Hyalorbilia quadridens, Hyalorbilia tenuifusaria, and Orbilia fissilis.