Tales from the crypt: genome mining from fungarium specimens improves resolution of the mushroom tree of life

Abstract

The enormity of the breadth and depth of specimens held within the world's biological collections offers unparalleled opportunities to capture genomic data from across the entire range of known biological diversity. Such a task would take many lifetimes to complete if we could rely only on fresh samples. High‐throughput sequencing provides a technical solution to the long‐term problems of recalcitrant and degraded DNA typical of museum specimens, suggesting that we may be on the verge of a major collections‐based revolution. Although the potential is great, the feasibility of using preserved collections for large‐scale, taxonomically comprehensive phylogenomic studies remains unknown. In the present study, we demonstrate the continued relevance of fungarium collections in the genomic era by analyzing a genomic dataset composed of 39 genomes representing 26 family‐level clades, including 14 newly generated draft genomes derived from short‐read shotgun sequencing of preserved specimens, frozen and freeze‐dried material, representing most of the known families of Agaricales. We predicted homologues of 210 putative single copy genes in the newly generated draft genome assemblies, of which 208 were used for phylogenetic reconstruction. Our analyses resulted in a robust and, for the first time, fully supported phylogeny of the Agaricales, enabling the recognition of seven suborders and providing a resource for testing hypotheses of the evolution of mushrooms. Our analysis of optimal combinations of ranked genes using an information theory‐based method provides guidance on gene selection for future studies, enabling efficient application of high‐throughput sequencing techniques toward unlocking the potential of collections‐based research in the genomic era.

Fungal DNA barcoding

“…For example, nextgeneration sequencing technologies have shown to be very useful in fungal evolutionary studies, including analyzing the genomes of herbarium samples. In a recent study, Dentinger et al (2015) obtained 14 whole-genome sequences from herbarium mushroom specimens and compiled a dataset of over 200 genes for 35 taxa representing most of the known families of mushrooms in the order Agaricales. Their analysis revealed seven suborders and established robust relationships among the suborders and families.…”

The cacao pathogen Moniliophthora roreri (Marasmiaceae) possesses biallelic A and B mating loci but reproduces clonally

“…Theobroma cacao L. is the source of chocolate and its production in Latin America is severely affected by two major diseases: frosty pod rot caused by Moniliophthora roreri and witches' broom disease, caused by the C-biotype of M. perniciosa (Phillips-Mora and Wilkinson, 2007), which together form a clade within the mushroom-forming family Marasmiaceae in the Marasmiineae, Agaricales (Aime and PhillipsMora, 2005;Dentinger et al, 2015). Moniliophthora roreri is believed to originate from Colombia and before the 1950s, it was confined to Colombia, Ecuador and western Venezuela .…”

Taxonomical and chorological notes 2

“…Scale bar indicates 0.1 expected changes per site per branch. Hohenbuehelia Schulzer (anamorphic synonym: Nematoctonus Drechsler) is a cosmopolitan saprotrophic and nematode-destroying genus in the family Pleurotaceae Kühner belonging to the suborder Pleurotineae Aime, Dentinger et Gaya (Dentiger et al 2016) in Agaricales Underw. Th e genus is morphologically characterised by crepidotoid to pleurotoid, rarely omphalinoid basidiocarp and the gelatinous zone beneath the pileipellis, and metuloid pseudocystidia (Koziak et al 2007, Thorn andBarron 1986).…”