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Species diversity of fungal pathogens on cultivated mushrooms: a case study on morels (Morchella, Pezizales)

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Abstract

Mushrooms are important organisms because of their human nutritional and medicinal value. With the expansion of the cultivation of edible mushrooms, fungal diseases have become a major problem in limiting their production. Numerous fungi can cause mushroom deformation or rots. In this publication we report on fungal diseases found during Morchella cultivation in China, with emphasis on morphology and phylogeny to characterise species. The key findings include 1) establishment of a new family Albomorchellophilaceae in Hypocreales, and a novel monotypic genus Albomorchellophila with the type species A. morchellae. Divergence time estimates indicate that Albomorchellophilaceae diverged from its sister family Calcarisporiaceae at ca. 105 (92–120) MYA; 2) the phylogeny and morphology of the family Pseudodiploosporeaceae (Hypocreales) is revised. The family contains a single genus Pseudodiploospora. Intraspecific genetic analyses of Pseudodiploospora longispora reveals significant base differences within strains, especially in the regions of protein-coding genes RPB 2 and TEF; 3) four fungicolous taxa, i.e., Cylindrodendrum alicantinum, Hypomyces aurantius, Hypomyces rosellus, and Trichothecium roseum, are reported as putative pathogens on cultivated morels for the first time. In addition, the previously reported pathogens of morels, Clonostachys rosea, Clonostachys solani, Hypomyces odoratus, and Pseudodiploospora longispora are also detailed in their symptoms and morphology; 4) the phylogeny and morphology of “Zelopaecilomyces” previously placed within Pseudodiploosporeaceae are re-assessed. “Zelopaecilomyces” is proved to be introduced through a chimerism of gene fragments sourced from two distinct organisms. Consequently, it is recommended that “Zelopaecilomyces” should not be recognised due to the mixed up molecular data in phylogeny and a lack of support from morphological evidence. Furthermore, this study discusses the voucher specimen Paecilomyces penicillatus (CBS 448.69), which may contain two mixed taxa, i.e., Pseudodiploospora longispora and a member of Penicillium. Publications on pathogenic fungi of cultivated mushrooms is sporadically, which leads to a lack of understanding of causal agents. As a follow up to the diseases of morel cultivation, we also review the fungal diseases of cultivated mushrooms reported over the last four decades. More than 130 pathogens affect the growth and development of the main cultivated mushrooms. The taxonomic diversity of these pathogens is high, distributed in 58 genera, 40 families, 20 orders, 12 classes and six phyla. The host infected are from Ascomycota to Basidiomycota, mainly being reported from Agaricus bisporus, Cordyceps militaris, Morchella spp., and Pleurotus spp. This study not only enriches our current knowledge on the diversity of pathogens of cultivated mushrooms, especially morels, but also recognizes the importance of some taxa as potential pathogens. Taxonomic investigation and accurate identification are initial and key steps to understanding pathogen-mushroom interactions, and will result in better disease management strategies in the mushroom industry.

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Data availability

All sequences have been deposited at GenBank database (Tables S1 and S2).

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Acknowledgements

This study is supported by the Second Tibetan Plateau Scientific Expedition and Research (STEP) Program (Grant No. 2019QZKK0503), Major science and technology projects and key R&D plans/programs, Yunnan Province (202202AE090001), Natural Science Foundation of Guizhou Province (Grant No. Qian Ke Zhong Yin Di [2021]4031, Qian Ke He Zhi Cheng [2021] Generally 200), the open research project of “Cross-Cooperative Team” of the Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences (Grant No. 292019312511043), the Biodiversity Survey and Assessment Project of the Ministry of Ecology and Environment, PR China (2019HJ2096001006), the National Research Council of Thailand (NRCT) grant “Total fungal diversity in a given forest area with implications towards species numbers, chemical diversity and biotechnology” (Grant No. N42A650547), Natural Science Foundation of China (No. 32072645). Guizhou Provincial Science and Technology Projects ZK [2023] general 087. Feng-Ming Yu thanks Dr. Xiang-Hua Wang (Kunming Institute of Botany, Chinese Academy of Sciences) for providing valuable guidance for this paper.

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Authors and Affiliations

  1. Key Laboratory for Plant Diversity and Biogeography of East Asia, Yunnan Key Laboratory of Fungal Diversity and Green Development, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, Yunnan, People’s Republic of China

    Feng-Ming Yu, Cui-Jin-Yi Li, Shu-Xin Bao, Hong Ba, De-Qun Zhou, Kevin D. Hyde & Qi Zhao

  2. Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai, 57100, Thailand

    Feng-Ming Yu, Ruvishika S. Jayawardena, Thatsanee Luangharn, Cui-Jin-Yi Li, Shu-Xin Bao & Kevin D. Hyde

  3. School of Science, Mae Fah Luang University, Chiang Rai, 57100, Thailand

    Feng-Ming Yu, Ruvishika S. Jayawardena, Cui-Jin-Yi Li, Shu-Xin Bao & Kevin D. Hyde

  4. Department of Plant Pathology, Agriculture College, Guizhou University, Guiyang, 550025, People’s Republic of China

    Xiang-Yu Zeng

  5. Institute of Fanjing Mountain National Park, Tongren University, Tongren, 554300, People’s Republic of China

    De-Qun Zhou

  6. Biotechnology and Germplasm Resources Institute, Yunnan Academy of Agricultural Science, Kunming, 650205, People’s Republic of China

    Song-Ming Tang

  7. Innovative Institute for Plant Health, Zhongkai University of Agriculture and Engineering, Haizhu District, Guangzhou, 510225, People’s Republic of China

    Kevin D. Hyde

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  1. Feng-Ming Yu
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  7. Hong Ba
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Contributions

F-MY is responsible for culture isolations, identifications and descriptions, data analyses, drafting and editing the manuscript; F-MY, C-J-YL and QZ are responsible for sampling; KDH and QZ for funding acquisition; RSJ, TL, Xiang-Yu Zeng, C-J-YL, S-XB, HB, D-QZ, S-MT, KDH and QZ conceiving this study, and improving the manuscript; RSJ, TL, X-YZ, KDH and QZ contributed to the data analyses.

Corresponding authors

Correspondence to Kevin D. Hyde or Qi Zhao.

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Yu, FM., Jayawardena, R.S., Luangharn, T. et al. Species diversity of fungal pathogens on cultivated mushrooms: a case study on morels (Morchella, Pezizales). Fungal Diversity 125, 157–220 (2024). https://doi.org/10.1007/s13225-023-00531-6

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