The origin and diversification of the Entorrhizales: deep evolutionary roots but recent speciation with a phylogenetic and phenotypic split between associates of the Cyperaceae and Juncaceae

Fungi belonging to the Entorrhizales (Entorrhizomycota) comprise biotrophic pathogens associated with roots of the Cyperaceae and Juncaceae plant species. They are nearly globally distributed but rarely studied due to a hidden lifestyle without causing visible effects on host plants. Therefore, the evolutionary origin and phylogenetic relationships of the group are still poorly understood and it is not known whether species diversification was the result of co-evolution with their hosts or the result of host jumps. To infer hypotheses about the evolutionary history of the Entorrhizales, divergence times were estimated and plant-fungal tanglegrams calculated. Relaxed molecular clock analyses suggest that the Entorrhizomycota originated around the Neoproterozoic-Palaeozoic and diverged during the Late Cretaceous-Paleogene into the extant orders Entorrhizales and Talbotiomycetales. The split of the major lineages within the Entorrhizales took place in the Eocene, somewhat later than the divergence of the host families Cyperaceae and Juncaceae. Topology- and distance-based co-phylogenetic analyses of the fungi and their hosts revealed a large number of co-speciation and lineage sorting events in early fungal speciation, which resulted in a phylogenetic split corresponding to species infecting Cyperaceae or Juncaceae. Given that this split is congruent with spore differences, Entorrhiza s. str. is emended for species infecting hosts in the Cyperaceae, and a new genus Juncorrhiza is described for species restricted to hosts in the Juncaceae. Additionally, three new species are described: Entorrhiza fuirenae, Juncorrhiza maritima and J. oxycarpi.