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  5. Ecological genomics of saprotrophy to biotrophy transitions in the genus Clitopilus (Fr. ex Rabenh.) P. Kumm. (Agaricales, Entolomataceae).

Ecological genomics of saprotrophy to biotrophy transitions in the genus Clitopilus (Fr. ex Rabenh.) P. Kumm. (Agaricales, Entolomataceae).

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Resource type
Journal article
Creator (person)
Zhang, Yuwei
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Wang, Yuchen
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Druzhinina, Irina S.
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Vasco, Fachada
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Zhong, Donglian
Peng, Long
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Yao, Jiajia
Yuan, Zhilin
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Martin, Francis M.
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Date published
January 27, 2026
Abstract
Transitions between saprotrophic and biotrophic lifestyles represent pivotal evolutionary events in fungal ecology; however, the genomic and physiological mechanisms underlying such shifts remain poorly understood. The agaric genus Clitopilus (Basidiomycota, Entolomataceae) offers a valuable model system, with most species being soil saprotrophs. Clitopilus cf. baronii Consiglio & Setti exhibits genomic signatures suggesting incipient biotrophic capacity. Here, we investigated the genomic and eco-physiological properties of seven strains representing five Clitopilus species to identify traits associated with lifestyle transitions. ITS-based phylogeny combined with ecological metadata revealed potential facultative biotrophy in multiple taxa from the section Scyphoides. Physiological profiling showed that all strains utilized mannitol and sucrose poorly, preferred organic nitrogen compounds, and produced variable amounts of indole-3-acetic acid (IAA) in vitro in a strictly tryptophan-dependent manner. Enzymatic assays revealed substantial variations in the nitrogen and phosphorus acquisition capabilities among the strains. Comparative genomics of high-quality assemblies identified a pleuromutilin biosynthetic gene cluster (BGC) across all strains, although synteny analysis revealed considerable structural variation and putative gene loss, indicating that genomic plasticity potentially affects antibiotic production. Principal component analysis of carbohydrate-active enzymes (CAZymes) across 25 fungal genomes partitioned Clitopilus strains into two distinct groups: one resembling saprotrophic white-rot basidiomycetes, the other matching biotrophic ectomycorrhizal and endophytic taxa. This first comprehensive genomic analysis of Clitopilus revealed that nutritional specialization, phytohormone production, and CAZyme repertoire remodeling collectively signal an ongoing evolutionary transition from saprotrophy to plant-associated lifestyles in multiple lineages. These findings provide a rare genomic window into the early stages of symbiosis evolution, offering insights into how free-living fungi acquire the molecular toolkit for mutualistic partnerships.
Project(s)
Priority 4: Accelerated Taxonomy
Funder
Funder nameAwards
National Key Research and Development Program of China, China
(2022YFD2201900)
National Natural Science Foundation of China, China
(32471839)
Royal Botanic Gardens, Kew, United Kingdom
Start-up funds.
Journal title
IMA Fungus
Volume
17
Article number
e179417
Publisher
Pensoft Publishers
Place of publication
Sofia, Bulgaria
ISSN
2210-6340
eISSN
2210-6359
Date accepted
December 30, 2025
Official URL
https://doi.org/10.3897/imafungus.17.179417
Related URL
https://imafungus.pensoft.net/article/179417/
Rights statement
In Copyright
Licence
https://creativecommons.org/licenses/by/4.0/
DOI
10.3897/imafungus.17.179417
Keywords
IAA
Pleuromutilin
Nitrogen acquisition
Ecophysiology
Clitopilus
CAZymes
Additional information
IF = 6.2 (2024)
Managed by the British Library and supported by the AHRC

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