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Phylogeny and species delimitation of Flammulina: taxonomic status of winter mushroom in East Asia and a new European species identified using an integrated approach

Mycological Progress volume 17, pages 1013–1030 (2018)Cite this article

Abstract

The winter mushroom, or Enokitake, is economically important and commercially cultivated on a large scale in East Asia. However, the phylogeny and species delimitation of the winter mushroom genus (Flammulina) have not been fully clarified. In this study, 81 collections of Flammulina from East Asia, Europe, and North America were studied, and their phylogeny and species delimitation were inferred from partial sequences of the ITS, tef1-α, rpb2, and homeodomain1 (HD1) of the mating gene (labeled as HD1-A). Genetic structure analyses based on genomic SSR markers and haplotype network analysis based on HD1-A were also used to delimit several closely related taxa. Twelve phylogenetic species were recognized, which was largely consistent with previous studies. However, our integrated studies indicated that Enokitake is not identical to the European winter mushroom Flammulina velutipes, and thus should be treated as a separate species, namely Flammulina filiformis. All cultivated strains of “F. velutipes” in East Asia, including those from South Korea and Japan with genome sequences labeled as such, are in fact F. filiformis. A new species, Flammulina finlandica, was also unexpectedly discovered in Northern Europe. Morphological descriptions of these two species, color photos of their fresh basidiomata, and line drawings of their microscopic features are presented.

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Acknowledgements

We are grateful to Dr. J. M. Budke and B. E. Wofford (Directors of University of Tennessee Herbarium TENN, Knoxville, USA), and Dr. Walter Till (Curator of University of Vienna Herbarium, WU) for sending us specimens of Flammulina on loan. We are very grateful to Dr. Bao-Kai Cui (Beijing Forestry University), Dr. Ping Zhang (Hunan Normal University), Dr. Xiang-Hua Wang, Dr. Yan-Jia Hao, Dr. Qi Zhao, Dr. Jiao Qin, Dr. Bang Feng, Dr. Qing Cai (Kunming Institute of Botany), and Dr. Han-Cheng Wang (Chongqing Normal University) for providing specimens and/or color images. We really appreciate Dr. Wei Wang (Shandong Agricultural University) for valuable information on mating genes. Dr. Won-Sik Kong (Mushroom Research Division, National Institute of Horticultural and Herbal Science, Rural Development Administration, Eumsung, Republic of Korea) is acknowledged for generously sharing the genome sequencing data of the cultivar KACC42780. Finally, we especially thank Dr. Yan-Jia Hao, Dr. Bang Feng, Dr. Qing Cai, and Dr. Gang Wu for their constructive comments and valuable suggestions. The present research work was supported by the National Basic Research Program of China (973 Program, No. 2014CB138305) and the National Natural Science Foundation of China (No. 31270074).

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Authors and Affiliations

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

    Pan Meng Wang, Xiao Bin Liu & Zhu L. Yang

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

    Pan Meng Wang & Xiao Bin Liu

  3. Institute of Microbiology, Beijing Forestry University, Beijing, 100083, China

    Yu Cheng Dai

  4. Innsbruck, Austria

    Egon Horak

  5. Nanoform Finland Ltd., Helsinki, Finland

    Kari Steffen

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  1. Pan Meng Wang
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  6. Zhu L. Yang
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Correspondence to Zhu L. Yang.

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Section Editor: Marc Stadler

In memory of Prof. Dr. Franz Oberwinkler (5. 1939–3. 2018), for his outstanding mycological studies and inspiring teaching.

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Fig S1

Phylogenetic tree inferred from maximum likelihood analysis based on the ITS alignment. Bootstrap Values (BS > 75%), together with Bayesian Posterior Probabilities (PPs > 0.95) are indicated above the branch (PDF 328 kb)

Fig S2

Phylogenetic tree inferred from maximum likelihood analysis based on the tef1-α alignment. Bootstrap Values (BS > 75%), together with Bayesian Posterior Probabilities (PPs > 0.95) are indicated above the branch (PDF 307 kb)

Fig S3

Phylogenetic tree inferred from maximum likelihood analysis based on the rpb2 alignment. Bootstrap Values (BS > 75%), together with Bayesian Posterior Probabilities (PPs > 0.95) are indicated above the branch (PDF 304 kb)

Fig S4

Estimation of number of populations for K ranging from 1 to 10 by ΔK values (PNG 35 kb)

High Resolution Image (TIF 2624 kb)

Fig S5

Phylogenetic tree inferred from maximum likelihood analysis based on the concatenated ITS-tef1-α-rpb2 alignment. Bootstrap Values (BS > 75%), together with Bayesian Posterior Probabilities (PPs > 0.95) are indicated above the branch (PDF 324 kb)

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Wang, P.M., Liu, X.B., Dai, Y.C. et al. Phylogeny and species delimitation of Flammulina: taxonomic status of winter mushroom in East Asia and a new European species identified using an integrated approach. Mycol Progress 17, 1013–1030 (2018). https://doi.org/10.1007/s11557-018-1409-2

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Keywords

  • Agaricales
  • Physalacriaceae
  • DNA barcoding
  • Edible mushroom
  • New species
  • Genetic structure
  • Mating type gene