Taming the beast: a revised classification of Cortinariaceae based on genomic data

Kare Liimatainen,Tuula Niskanen,Lisa Pokorny,Jan T. Kim,Paul M. Kirk,Bryn Dentinger

doi:10.1007/s13225-022-00499-9

Abstract

Family Cortinariaceae currently includes only one genus, Cortinarius, which is the largest Agaricales genus, with thousands of species worldwide. The species are important ectomycorrhizal fungi and form associations with many vascular plant genera from tropicals to arctic regions. Genus Cortinarius contains a lot of morphological variation, and its complexity has led many taxonomists to specialize in particular on infrageneric groups. The previous attempts to divide Cortinarius have been shown to be unnatural and the phylogenetic studies done to date have not been able to resolve the higher-level classification of the group above section level. Genomic approaches have revolutionized our view on fungal relationships and provide a way to tackle difficult groups. We used both targeted capture sequencing and shallow whole genome sequencing to produce data and to perform phylogenomic analyses of 75 single-copy genes from 19 species. In addition, a wider 5-locus analysis of 245 species, from the Northern and Southern Hemispheres, was also done. Based on our results, a classification of the family Cortinariaceae into ten genera—Cortinarius, Phlegmacium, Thaxterogaster, Calonarius, Aureonarius, Cystinarius, Volvanarius, Hygronarius, Mystinarius, and Austrocortinarius—is proposed. Seven genera, 10 subgenera, and four sections are described as new to science and five subgenera are introduced as new combinations in a new rank. In addition, 41 section names and 514 species names are combined in new genera and four lecto- and epitypes designated. The position of Stephanopus in suborder Agaricineae remains to be studied. Targeted capture sequencing is used for the first time in fungal taxonomy in Basidiomycetes. It provides a cost-efficient way to produce -omics data in species-rich groups. The -omics data was produced from fungarium specimens up to 21 years old, demonstrating the value of museum specimens in the study of the fungal tree of life. This study is the first family revision in Agaricales based on genomics data and hopefully many others will soon follow.

Highlights

Genomic-level data have revolutionized our views on fungal relationships and helped us create better phylogenies for previously unresolved lineages (e.g., Chang et al 2021; Li et al 2021)
In phylogenomics studies of fungi, in depth or shallow whole genome sequencing (WGS) have been an affordable option to generate High-throughput sequencing (HTS) data, with the vast majority of the fungal genomic studies to date having relied on this approach
The average fragment size in the specimens that were used for WGS ranged from 680 to 745 bp, and from 660 to 880 bp for the specimens used for the targeted capture sequencing

Summary

Introduction

Genomic-level data have revolutionized our views on fungal relationships and helped us create better phylogenies for previously unresolved lineages (e.g., Chang et al 2021; Li et al 2021). These data have been used to tackle macroevolutionary events, e.g., mushroom morphological evolution (Varga et al 2019, Sánchez-García et al 2020) or the evolution of symbiotic traits (Miyauchi et al 2020). In phylogenomics studies of fungi, in depth or shallow whole genome sequencing (WGS) have been an affordable option to generate HTS data, with the vast majority of the fungal genomic studies to date having relied on this approach. Enrichment methods have been widely used to study the systematics of plants and animals (e.g., Johnson et al 2019; Faircloth 2017) and they have recently been applied in fungal systematics to study lichen-forming Ascomycota families Lobariaceae (Widhelm et al 2019) and Parmeliaceae (Grewe et al 2020), as well as the Peltigeralean backbone (Widhelm et al 2021)

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