A multigene phylogeny toward a new phylogenetic classification of Leotiomycetes

Abstract

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.

Broad geographical and ecological diversity from similar genomic toolkits in the ascomycete genusTetracladium

“…The family level phylogenetic relationships resolved in this study are in line with the results from previous studies (85-87). Within the Leotiomycetes, all clades identified by Johnston and colleagues (88) and were represented here, are recovered. The family containing Tetracladium , Vandijckellaceae (88, 89), was included in an analysis based on 15 concatenated sequences (88).…”

“…Within the Leotiomycetes, all clades identified by Johnston and colleagues (88) and were represented here, are recovered. The family containing Tetracladium , Vandijckellaceae (88, 89), was included in an analysis based on 15 concatenated sequences (88). The tree herein differs from that result in the branching order of the Vandijckellaceae and helotioid taxa.…”

The Asian‐Melanesian bambusicolous genus Myriodiscus is related to the genus Tympanis, the North American‐European tree pathogen

“…Myriodiscus is supported in the clade with Tympanis, but also related to Collophorina as a sister clade (Figure 2, clade J). Although our phylogeny did not yield good support in the backbone of the tree (relationships at order level in Leotiomycetes) since we used only two genes, the 15-gene phylogeny of Johnston et al (2019) shows the same relationships found here with high support for the internal nodes of the tree and will place Tympanidaceae as a family in Leotiales (Johnston et al, 2019) rather than Phacidiales (Baral, 2016;Wijayawardene et al, , 2018. Sanoamuang et al (2013) did not realize that Collophorina is a polyphyletic genus (Damm, Fourie, & Crous, 2010).…”

Brassicaceous roots as an unexpected diversity hot-spot of helotialean endophytes

“…Species of the genus Cadophora (Ploettnerulaceae, Helotiales, Leotiomycetes) are frequently associated with living plant roots and classified as so-called dark septate endophytes (DSEs), a polyphyletic group of non-pathogenic, root-colonizing fungi characterized by melanized hyphae conspicuous when observing roots under the microscope (Jumpponen 2001;Sieber 2002;Addy et al 2005). Cadophora has close phylogenetic affinities with other helotialean lineages with well-known root-associated habits, such as Leptodontidium, Acephala, or Phialocephala (with its teleomorph in Mollisia)-constituting the 'mollisioid clade' sensu Johnston et al (2019)-and more distantly with mycorrhizal fungi in the Hyaloscyphaceae (Johnston et al 2019). Whereas Cadophora species are also common as plant pathogens and colonizing substrata other than roots, such as wood or soil (Lagerberg et al 1927;Bills 2004, p. 2;Gramaje et al 2011;Crous et al 2017), several lines of evidence suggest a degree of adaptation in the genus toward a symbiotic association with plant roots or, leastwise, the possession of a genomic toolbox favoring the evolution of such a lifestyle.…”