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The family Amanitaceae: molecular phylogeny, higher-rank taxonomy and the species in China

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Abstract

Mushrooms in the basidiomycete family Amanitaceae are very important both economically and ecologically. However, the delimitation of the family is still controversial, in part due to limited taxon sampling and in part because of insufficient gene fragment employed for molecular phylogenetic analyses. Furthermore, species diversity in the family is likely to have been largely underestimated, due to morphological similarity between taxa and phenotypic plasticity. In this study, we examined 1190 collections, including 1008 Chinese and 182 external ones, and performed the first comprehensive phylogenetic analyses of Amanitaceae using multi-locus sequence data. To test the monophyly of the Amanitaceae, a concatenated (nrLSU, rpb1, and rpb2) dataset of 200 taxa of the order Agaricales was analyzed. To infer the phylogeny of Amanitaceae, a concatenated nrLSU, tef1-α, rpb2 and β-tubulin dataset (3010 sequences from ca. 890 samples with 2309 newly generated sequences) was used. In this dataset, 252 sequences from the types of 77 species were provided. Our results indicate that Amanitaceae is a monophyletic group, and consists of five genera, namely Amanita, Catatrama, Limacella, Limacellopsis and Myxoderma. It is clear that Catatrama is closely related to Limacella, however, the phylogenetic relationships among these genera remain largely unresolved. Amanita contains 95% of the species in the family, and is here divided into three subgenera and eleven sections (subgen. Amanita, containing: sect. Amanita, sect. Amarrendiae, sect. Caesareae and sect. Vaginatae; subgen. Amanitina, containing: sect. Amidella, sect. Arenariae, sect. Phalloideae, sect. Roanokenses, sect. Strobiliformes and sect. Validae; and subgen. Lepidella, containing sect. Lepidella). Subgen. Lepidella occupies the basal position in the genus. One-hundred and sixty-two species of Amanitaceae known from China are treated in this study, including 50 novel species and 112 known taxa. Amanita gleocystidiosa, A. pyriformis, A. atrofusca, A. subjunquillea var. alba and A. areolata are treated as synonyms of A. sychnopyramis f. subannulata, A. orientigemmata, A. umbrinolutea, A. subjunquillea and A. zangii, respectively. 26 extralimital taxa including a novel species, namely Catatrama indica, were included in our study to allow us to make comparisons between these and the Chinese taxa. DNA sequence data for all the species of Amanitaceae in China and keys for identification of the species are provided.

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Acknowledgements

This paper is in memory of the late Prof. Dr. Franz Oberwinkler. It is also dedicated to the late amanitologist Dr. C. Bas, for his important contributions to the study of Amanitaceae. We are very grateful to Dr. R. E. Tulloss for providing access to many collections of Amanita housed at his private herbarium, important literature and many illuminating discussions. We are greatly indebted to Dr. S. Redhead for his taxonomic and nomenclatural discussions and valuable suggestions on Amanita. We thank Prof. Zuo-Hong Chen, Prof. Yu-Chen Dai, Dr. K. Hosaka, Prof. Gerhard Kost, Dr. S. S. Lee, Dr Fang Li, Prof. Tai-Hui Li, Dr. Flavius Popa, Dr. C. K. Pradeep, Prof. Bau Tolgor, Dr. K. B. Vrinda, Dr. M. Weiß, Prof. Jian-Ping Xu, Prof. Ping Zhang, and the herbaria BO, BPI, CUP, DAOM, F, FH, FRIM, GDGM, H, HKAS, HMAS, HMJAU, HMLD, IFP, K, KPM, L, MB, MEL, MHHNU, PDD, PERTH, RET, SAPA, TBGT, TF, TMI, TNM, TNS, VLAM, and WU for sending materials on loan, for exchange or as gifts. We are grateful to Dr. Xiang-Hua Wang, Dr. Zai-Wei Ge, Dr. Yan-Chun Li, Dr. Hong Luo, Dr. Qi Zhao, Prof. Nian-Kai Zeng, Dr. Bang Feng, Dr. Gang Wu, Dr. Xiao-Fei Shi, Dr. Md. Iqbal Hosen, Dr. Jiao Qin, Dr. Yan-Jia Hao, Dr. Kuan Zhao, Mr. Xiao-Bin Liu, Mr. Pan-Meng Wang, Ms. Xing He, Ms. Xiao-Xia Ding and Ms. Lv-Yun-Jiao Li for providing valuable collections, images and kind help for this study. Thanks are also due to the anonymous reviewers for their valuable suggestions and comments. This work is supported by the Joint Funds of the National Natural Science Foundation of China and Yunnan Provincial Government (U1302263), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31000000), the Biodiversity Conservation Program of the Ministry of Environmental Protection (2016HB2096001006) and the National Natural Science Foundation of China (31600031).

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    1. Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China

      Yang-Yang Cui, Qing Cai, Jian-Wei Liu & Zhu L. Yang

    2. University of Chinese Academy of Sciences, Beijing, 100049, China

      Yang-Yang Cui & Jian-Wei Liu

    3. School of Pharmaceutical Sciences and Yunnan Key Laboratory of Pharmacology for Natural Products, Kunming Medical University, Kunming, 650500, China

      Li-Ping Tang

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    Correspondence to Zhu L. Yang.

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    In memory of our highly respected mentor, Prof. Dr. Franz Oberwinkler (1939–2018). His strong support realized the doctorial study of the senior author (ZLY) in Germany in the 1990s. He brought the senior author to the fantastic fungal world with years of continuous guidance, many constructive discussions and considerable encouragement. He made the senior author understand the spirit of “Good is good, but better carries it”. He taught botany, mycology and the relevant research skills with great enthusiasm, which will be beneficial to many mycologists worldwide, for a long time.

    Yang-Yang Cui and Qing Cai have equally contributed to this work.

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    Cui, YY., Cai, Q., Tang, LP. et al. The family Amanitaceae: molecular phylogeny, higher-rank taxonomy and the species in China. Fungal Diversity 91, 5–230 (2018). https://doi.org/10.1007/s13225-018-0405-9

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