Abstract
The Clitocybaceae is a recently established family. Currently, the infrafamilial divisions and relationships within the family are vague due to limited sampling and genes employed for phylogenetic analysis. Some mushrooms of the family contain the neurotoxic muscarine, which has caused many severe and even deadly poisonings worldwide. However, the taxonomic distribution and evolution of the toxin within the family is largely unknown. In this study, phylogenetic analyses based on nucleotide sequences of ITS and of six molecular loci (ITS, LSU, TEF1, RPB1, RPB2 and ATP6), plus a phylogenomic analysis based on 485 single-copy orthologous genes, were performed to reconstruct the framework of Clitocybaceae. BEAST analysis was used to estimate the divergence times within the family. Additionally, biochemical analysis for muscarine was conducted of 32 representative species. Based on these analyses, an updated classification of Clitocybaceae into six genera (Clitocybe, Collybia, Dendrocollybia, Lepista, Pseudolyophyllum, and Singerocybe) is proposed. The genus Collybia is emended to accommodate four subgenera (Collybia, Crassicybe, Leucocalocybe, and Macrosporocybe). Seventeen new Chinese species and 15 new combinations are proposed. Keys to the genera of Clitocybaceae and the subgenera of Collybia, as well as to the known species of Clitocybe and Collybia subgen. Collybia in China, are presented. In addition, muscarine was detected in 18 species, and these muscarine-containing species formed a major monophyletic clade within Collybia subgen. Collybia. Finally, our phylogenetic, phylogenomic, chemotaxonomic and molecular dating results indicate that the Clitocybaceae is a natural group estimated to have arisen some 60 million years ago, and in this family, muscarine has evolved only once circa 20 million years ago without later losses.
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Data availability
The DNA sequences obtained in this study have been submitted to GenBank.
References
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Acknowledgements
The authors are very grateful to Drs. Bang Feng, Gang Wu, Jiao Qin, Li-Ping Tang, Kuan Zhao, Pan-Meng Wang, Qi Zhao, Qing Cai, Yan-Jia Hao, Zai-Wei Ge, PhD students Hua Qu, Jian-Wei Liu, Liu-Kun Jia, Mei-Xiang Li, Sheng-Wen Zhou, Si-Peng Jian, Xiao-Xia Ding, and master students Jian-Yun Wu, Tian-Xiu Xu, Xin Xu, Ya-Jun Hou, Yun-Rui Ma, for providing specimens, images and help. They thank Dr. Xiang-Hua Wang for generously providing many specimens and offering insightful suggestions. They also thank the reviewers for their constructive comments, valuable suggestions, and meticulous linguistic corrections.
Funding
This study was supported by Yunnan Xingdian Talents Support Plan—Science and Technology Leading Talents Program (202305AB350004), Yunnan Ten-Thousand-Talents Plan—Yunling Scholar Project (YNWR-YLXZ-2018-011) and Postdoctoral Directional Training Foundation of Yunnan Province.
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Z-MH conceived, designed and complete the experiments under the guidance of ZLY. Z-MH wrote the manuscript and ZLY revised it. Z-HC investigated two cases of mushroom poisoning and identified two specimens of Collybia collected from the scene. TB collected and identified four very critical specimens of Collybia. Z-MH and G-SW did the genome assemble and phylogenomic analysis.
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He, ZM., Chen, ZH., Bau, T. et al. Systematic arrangement within the family Clitocybaceae (Tricholomatineae, Agaricales): phylogenetic and phylogenomic evidence, morphological data and muscarine-producing innovation. Fungal Diversity 123, 1–47 (2023). https://doi.org/10.1007/s13225-023-00527-2
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DOI: https://doi.org/10.1007/s13225-023-00527-2