Phylogenomics, trophic ecology, and systematics of the truffle-forming Morchellaceae

The family Morchellaceae contains four truffle-forming genera: Fischerula, Imaia, Kalapuya, and Leucangium. In North America, some Imaia, Kalapuya, and Leucangium species are highly regarded gourmet edible fungi. In this study, we address longstanding questions about the evolution, systematics, and trophic mode of these fungal genera. We used high-throughput sequencing and a custom genome assembly pipeline to sequence and assemble 41 new genomes of epigeous and hypogeous Morchellaceae genera and outgroup taxa from the sister family Discinaceae. Phylogenomic reconstructions based on high-quality de novo genomes and published reference genomes support a single transition from epigeous to hypogeous habit within the Morchellaceae. These results are corroborated by phylogenetic evidence from LSU, tef1, and rpb2 with a larger dataset of specimens and publicly available sequences. We also provide direct morphological and molecular evidence that one species of Leucangium from North America forms ectomycorrhizas on Pseudotsuga menziesii in a natural habitat. Stable isotope analysis further supports the hypothesis that other species of truffle-forming Morchellaceae also obtain carbon via ectomycorrhizal symbiosis. Phylogenetic and morphological analysis supports the description of two new species and one new combination of Leucangium as well as one new species and one new combination of Imaia from North America. We also discuss additional, undescribed diversity detected in our phylogenetic analyses of these genera derived from fungarium specimens, mycophagous mammal scat samples, and other environmental samples.