Comparative genomics of Agaricales reveals substrate-driven adaptive radiation and genomic innovations in the subterranean mushroom Agaricus sinodeliciosus | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article Comparative genomics of Agaricales reveals substrate-driven adaptive radiation and genomic innovations in the subterranean mushroom Agaricus sinodeliciosus Hongyun Lu, Shingo Miyauchi, Yingqi Jiang, Ying Shi, Elodie Drula, and 31 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-8432113/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Grassland ecosystems contain approximately 40% of terrestrial organic carbon; however, the genomic mechanisms underlying fungal decomposer adaptation to these environments remain poorly understood. We sequenced 22 new genomes of Agaricales mushroom-forming fungi and compared them with 100 published genomes spanning diverse ecological niches to investigate the genomic innovations associated with substrate specialisation. Our analyses revealed distinct genomic signatures across ecological guilds, with ectomycorrhizal fungi showing a pronounced reduction in plant cell wall-degrading enzymes, whereas grassland saprotrophs exhibited convergent expansion of cellulose-degrading machinery, particularly the CBM1, CBM13, and AA9 families. Notably, several species displayed intermediate genomic profiles that challenge traditional ecological classifications, suggesting more complex evolutionary trajectories along the saprotrophy-symbiosis spectrum than previously recognised. We focused our detailed analysis on Agaricus sinodeliciosus, a wild mushroom endemic to the high-altitude Tibetan Plateau grasslands, which uniquely forms large fruiting bodies underground. Compared to its cultivated relative A. bisporus, A. sinodeliciosus showed substantial genome expansion through transposable element proliferation, a dramatic reduction in plant cell wall-degrading enzymes, and species-specific pathways, including expanded tyrosine metabolism for melanin synthesis and hypoxia-responsive HIF-1 signalling. Transcriptomic analysis revealed that underground fruiting involves the coordinated regulation of hydrophobins, environmental sensors responsive to pH and nutrient availability, and downregulation of cAMP signalling pathways, which typically suppress fruiting body formation. These findings illuminate the genomic basis of fungal niche adaptation and highlight how substrate chemistry and environmental extremes drive the evolutionary innovation of mushroom-forming fungi. Biological sciences/Evolution/Phylogenetics Earth and environmental sciences/Ecology/Microbial ecology comparative genomics Agaricales ecological adaptation grassland fungi subterranean fruiting enzyme evolution Full Text Additional Declarations There is NO Competing Interest. Supplementary Files SupplementaryTables.zip Supplementary Tables AgaricalesSupplementarySMv22Dec25.pdf Supplementary Figures nrreportingsummaryLHY20Jan26.pdf Reporting Summary SupplementaryTables.rar Supplementary Tables from Table S1 to Table S16 Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-8432113","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":583155640,"identity":"4d006d3a-7fa9-44da-bd0e-9ba4114aade5","order_by":0,"name":"Hongyun Lu","email":"","orcid":"","institution":"Zhejiang University","correspondingAuthor":false,"prefix":"","firstName":"Hongyun","middleName":"","lastName":"Lu","suffix":""},{"id":583155641,"identity":"16c4b546-9a52-461d-9aa2-0534c0845881","order_by":1,"name":"Shingo Miyauchi","email":"","orcid":"https://orcid.org/0000-0002-0620-5547","institution":"Max Planck Institute for Plant Breeding 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