{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T22:34:38Z","timestamp":1788474878877,"version":"build-2803163510"},"reference-count":58,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2026,2,10]],"date-time":"2026-02-10T00:00:00Z","timestamp":1770681600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32500047"],"award-info":[{"award-number":["32500047"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Young Doctor Fund Project of Education Department of Gansu Province","award":["2024QB-016"],"award-info":[{"award-number":["2024QB-016"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JoF"],"abstract":"<jats:p>Oudemansiella raphanipes is a prized edible mushroom renowned for its \u201cthree-high, one-low\u201d nutritional profile (high protein, fiber, vitamins; low fat). However, the stage-specific molecular dynamics governing its development and their potential link to its superior nutrition remain unknown, hindering targeted genetic improvement. This study aimed to decipher the first comprehensive transcriptomic atlas across its five key developmental stages and to explore potential molecular signatures linked to its distinctive nutrition. We first confirmed the superior nutritional profile of O. raphanipes via comparative analysis with nine commercial mushrooms. RNA sequencing (RNA-seq) was performed on samples from five defined developmental stages (spores, mycelia, primordia, closed-cap and open-cap fruiting bodies), followed by de novo transcriptome assembly, functional annotation, and differential expression analysis. Results revealed extensive transcriptional reprogramming, with the most dramatic changes occurring at the spore-to-mycelium transition (19,827 differentially expressed genes). Stage-specific pathway enrichment highlighted regulators of germination (e.g., ribosome, transmembrane transport), primordium formation (e.g., glycerophospholipid metabolism, GTPase signaling), fruiting body development (e.g., starch\/sucrose metabolism, terpenoid synthesis), and maturation (e.g., glycolysis, fatty acid biosynthesis, transcription factors MADS-box\/bZIP). We identified 588 stage-exclusive genes in spores and 515 constitutively upregulated genes linked to energy metabolism and proteostasis. Crucially, integrating nutritional phenotypes with stage-resolved transcriptomics revealed that sustained transcriptional programs in mature fruiting bodies are associated with its nutritional excellence; e.g., upregulation of ribosomal\/amino acid metabolic pathways aligns with high protein content, while active fatty acid degradation correlates with low fat levels. Our study provides the first multi-stage transcriptomic blueprint for O. raphanipes development, revealing stage-specific regulators and proposing molecular associations for its nutritional traits. This resource offers a foundational basis and candidate genetic targets for future breeding strategies aimed at enhancing agronomic and nutritional traits in this prized fungus.<\/jats:p>","DOI":"10.3390\/jof12020124","type":"journal-article","created":{"date-parts":[[2026,2,10]],"date-time":"2026-02-10T11:16:38Z","timestamp":1770722198000},"page":"124","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Unveiling Transcriptional Dynamics Across Five Developmental Stages of the Edible Mushroom Oudemansiella raphanipes"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7391-2615","authenticated-orcid":false,"given":"Yanjun","family":"Ma","sequence":"first","affiliation":[{"name":"College of Life Sciences, Northwest Normal University, Lanzhou 730070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lanlan","family":"Yu","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Northwest Normal University, Lanzhou 730070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-6902-2585","authenticated-orcid":false,"given":"Jinming","family":"Zhang","sequence":"additional","affiliation":[{"name":"Institute of Vegetable Research, Gansu Academy of Agricultural Sciences, Lanzhou 730070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yongxiang","family":"Dang","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Northwest Normal University, Lanzhou 730070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1515-0557","authenticated-orcid":false,"given":"Xuetai","family":"Zhu","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Northwest Normal University, Lanzhou 730070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,2,10]]},"reference":[{"key":"ref_1","first-page":"317","article-title":"Quantification of the umami taste of edible fungi using electronic tongue","volume":"32","author":"Bing","year":"2016","journal-title":"Mod. Food Sci. Technol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"106069","DOI":"10.1016\/j.jfca.2024.106069","article-title":"Evaluation of the umami in edible fungi and study on umami extraction of Agaricus bisporus","volume":"128","author":"Xue","year":"2024","journal-title":"J. Food Compos. Anal."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"e12437","DOI":"10.1111\/jfpe.12437","article-title":"Effects of processing and storage preservation technologies on nutritional quality and biological activities of edible fungi: A review","volume":"40","author":"Xue","year":"2016","journal-title":"J. Food Process Eng."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1016\/j.tifs.2019.12.018","article-title":"Advances in umami taste and aroma of edible mushrooms","volume":"96","author":"Sun","year":"2019","journal-title":"Trends Food Sci. Technol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1016\/S0254-6272(15)30089-3","article-title":"Antioxidant and immunomodulatory activities of a polysaccharide from Flammulina velutipes","volume":"34","author":"Wu","year":"2014","journal-title":"J. Tradit. Chin. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"6563","DOI":"10.1007\/s11033-022-07496-w","article-title":"Investigation of HER-3 gene expression under the influence of carbohydrate biopolymers extract of shiitake and reishi in MCF-7 cell line","volume":"49","author":"Larypoor","year":"2022","journal-title":"Mol. Biol. Rep."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"102608","DOI":"10.1016\/j.fbio.2023.102608","article-title":"Structural characterization and antioxidant activity of a glycoprotein isolated from shiitake mushrooms","volume":"53","author":"Gao","year":"2023","journal-title":"Food Biosci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.jff.2010.11.004","article-title":"Lipid lowering effects of oyster mushroom (Pleurotus ostreatus) in humans","volume":"3","author":"Schneider","year":"2010","journal-title":"J. Funct. Foods"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"49","DOI":"10.4103\/jrms.JRMS_513_20","article-title":"The effects of hot air-dried white button mushroom powder on glycemic indices, lipid profile, inflammatory biomarkers and total antioxidant capacity in patients with type-2 diabetes mellitus: A randomized controlled trial","volume":"27","author":"Hadiseh","year":"2022","journal-title":"J. Res. Med. Sci."},{"key":"ref_10","first-page":"67","article-title":"Research progress on nutritional value, functional properties and application of edible mushrooms in meat processing","volume":"39","author":"Sun","year":"2025","journal-title":"Meat Res."},{"key":"ref_11","first-page":"1","article-title":"Comparison of gene expression patterns in the mycelium and primordia of Flammulina velutipes, strain 1123","volume":"21","author":"Liu","year":"2014","journal-title":"Acta Edulis Fungi"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1760","DOI":"10.1016\/j.ijbiomac.2018.09.209","article-title":"Extraction, preliminary characterization and in vitro antioxidant activity of polysaccharides from Oudemansiella radicatamushroom","volume":"120","author":"Wang","year":"2018","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_13","first-page":"1","article-title":"A new systematic arrangement of the genus Oudemansiellas. str. (Physalacriaceae, Agaricales)","volume":"28","author":"Kost","year":"2009","journal-title":"Mycosystema"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1016\/j.sjbs.2015.07.001","article-title":"Evaluation of edible mushroom Oudemansiella canarii cultivation on different lignocellulosic substrates","volume":"23","author":"Xu","year":"2016","journal-title":"Saudi J. Biol. Sci."},{"key":"ref_15","first-page":"133","article-title":"Optimization of Oudemansiella raphanipes liquid fermentation medium","volume":"53","author":"Liu","year":"2024","journal-title":"J. Henan Agri Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1169","DOI":"10.7150\/jca.89873","article-title":"Glucan from Oudemansiella raphanipes suppresses breast cancer proliferation and metastasis by regulating macrophage polarization and the WNT\/\u03b2-catenin signaling pathway","volume":"15","author":"Alitongbieke","year":"2024","journal-title":"J. Cancer"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Zhu, L.P., Gao, X., Zhang, M.H., Hu, C.H., Yang, W.J., Guo, L.Z., Yang, S., Yu, H.L., and Yu, H. (2023). Whole genome sequence of an edible mushroom Oudemansiella raphanipes (Changgengu). J. Fungi, 9.","DOI":"10.3390\/jof9020266"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"105445","DOI":"10.1016\/j.jprot.2025.105445","article-title":"Comparative secretome analysis of Oudemansiella raphanipes grown on different agricultural residues","volume":"317","author":"Zhu","year":"2025","journal-title":"Proteomics"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"6173","DOI":"10.1021\/jf301198b","article-title":"Comparative proteomic analysis of mushroom cell wall proteins among the different developmental stages of Pleurotus tuber-regium","volume":"60","author":"Chen","year":"2012","journal-title":"J. Agric. Food Chem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"00532-19","DOI":"10.1128\/AEM.00532-19","article-title":"Chitinases play a key role in stipe cell wall extension in the mushroom Coprinopsis cinerea","volume":"85","author":"Zhou","year":"2019","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e03626-21","DOI":"10.1128\/mbio.03626-21","article-title":"Molecular mechanism by which the GATA transcription factor CcNsdD2 regulates the developmental fate of Coprinopsis cinerea under dark or light conditions","volume":"13","author":"Liu","year":"2022","journal-title":"MBio"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"6179","DOI":"10.1007\/s00253-023-12726-7","article-title":"Transcription factors: Switches for regulating growth and development in macrofungi","volume":"107","author":"Sun","year":"2023","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Zhou, Y., Chen, L.F., Fan, X.Z., and Bian, Y.B. (2014). De novo assembly of Auricularia polytricha transcriptome using Illumina sequencing for gene discovery and SSR marker identification. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0091740"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"9266","DOI":"10.1038\/s41598-017-08049-z","article-title":"Comparative transcriptome analysis identified candidate genes related to Bailinggu mushroom formation and genetic markers for genetic analyses and breeding","volume":"7","author":"Fu","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"8983","DOI":"10.1038\/s41598-018-27318-z","article-title":"Comparative transcriptome analysis of dikaryotic mycelia and mature fruiting bodies in the edible mushroom Lentinula edodes","volume":"8","author":"Song","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1007\/s10068-020-00732-8","article-title":"Comparative analysis of transcriptomes revealed the molecular mechanism of development of Tricholoma matsutake at different stages of fruiting bodies","volume":"29","author":"Tang","year":"2020","journal-title":"Food Sci. Biotechnol."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Cai, M.J., Liang, X.W., Liu, Y.C., Hu, H.P., Xie, Y.Z., Chen, S.D., Gao, X., Li, X.M., Xiao, C., and Chen, D.L. (2021). Transcriptional dynamics of genes purportedly involved in the control of meiosis, carbohydrate, and secondary metabolism during sporulation in Ganoderma lucidum. Genes, 12.","DOI":"10.3390\/genes12040504"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2315","DOI":"10.1007\/s00203-021-02225-6","article-title":"Deep sequencing of the Sanghuangporus vaninii transcriptome reveals dynamic landscapes of candidate genes involved in the biosynthesis of active compounds","volume":"203","author":"Zhou","year":"2019","journal-title":"Arch. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Liu, Z.C., Tong, X.Y., Liu, R.P., and Zuo, L. (2022). Metabolome and transcriptome profiling reveal that four terpenoid hormones dominate the growth and development of Sanghuangporus baumii. J. Fungi, 8.","DOI":"10.22541\/au.164362292.22373963\/v1"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"406","DOI":"10.1007\/s12257-022-0207-5","article-title":"Dissecting metabolic regulation in mycelial growth and fruiting body developmental stages of Cordyceps militaris through integrative transcriptome analysis","volume":"28","author":"Thananusak","year":"2023","journal-title":"Biotechnol. Bioprocess Eng."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Deng, K.J., Lan, X.H., Chen, Y., Wang, T., Li, M.K., Xu, Y.Y., Cao, X.L., Xie, G.B., and Xie, L.Y. (2022). Integration of transcriptomics and metabolomics for understanding the different vegetative growth in Morchella sextelata. Front. Genet., 12.","DOI":"10.3389\/fgene.2021.829379"},{"key":"ref_32","first-page":"27","article-title":"Comparative study on several determination of protein content in grey tree polysaccharide","volume":"22","author":"Wang","year":"2003","journal-title":"Edible Fungi China"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"8821315","DOI":"10.1155\/2020\/8821315","article-title":"Analysis of Nutritional Composition in 23 Kinds of Edible Fungi","volume":"2020","author":"Yu","year":"2020","journal-title":"J. Food Qual."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"9714930","DOI":"10.1155\/2019\/9714930","article-title":"Quality Evaluation of Thirteen Geographical Populations of Lycium chinense Using Quantitative Analysis of Nutrients and Bioactive Components","volume":"2019","author":"Yang","year":"2019","journal-title":"J. Food Qual."},{"key":"ref_35","first-page":"177","article-title":"Nutritional Composition, Gamma-aminobutyric Acid Content and Anti-fatigue Activity of Germinated Brown Rice Bran","volume":"40","author":"Wang","year":"2019","journal-title":"Food Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1231","DOI":"10.1016\/S0891-5849(98)00315-3","article-title":"Antioxidant activity applying an improved ABTS radical cation decolorization assay","volume":"26","author":"Re","year":"1999","journal-title":"Free Radic. Biol. Med."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1038\/nbt.1883","article-title":"Trinity: Reconstructing a full-length transcriptome without a genome from RNA-Seq data","volume":"29","author":"Grabherr","year":"2011","journal-title":"Nat. Biotechnol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"Altschul","year":"1990","journal-title":"J. Mol. Biol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"D480","DOI":"10.1093\/nar\/gkm882","article-title":"KEGG for linking genomes to life and the environment","volume":"36","author":"Kanehisa","year":"2008","journal-title":"Nucleic Acids Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1038\/nbt.1621","article-title":"Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation","volume":"28","author":"Trapnell","year":"2010","journal-title":"Nat. Biotechnol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast gapped-read alignment with Bowtie 2","volume":"9","author":"Langmead","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1038\/nmeth.2251","article-title":"Streaming fragment assignment for real-time analysis of sequencing experiments","volume":"10","author":"Roberts","year":"2013","journal-title":"Nat. Methods"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1007\/s11427-007-0046-9","article-title":"Comparison between gene expression of conidia and germinating phase in Trichophyton rubrum","volume":"50","author":"Yang","year":"2007","journal-title":"Sci. China Ser. C Life Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"00463-20","DOI":"10.1128\/msphere.00463-20","article-title":"Integrative analysis of proteome and transcriptome dynamics during Bacillus subtilis spore revival","volume":"5","author":"Swarge","year":"2020","journal-title":"Msphere"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"e147558","DOI":"10.3897\/imafungus.16.147558","article-title":"Multi-omics insights into growth and fruiting body development in the entomopathogenic fungus Cordyceps blackwelliae","volume":"16","author":"Li","year":"2025","journal-title":"IMA Fungus"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Xie, M.Y., Wang, J., Wang, F.X., Wang, J.F., Yan, Y.J., Feng, K., and Chen, B.X. (2025). A review of genomic, transcriptomic, and proteomic applications in edible fungi biology: Current status and future directions. J. Fungi, 11.","DOI":"10.3390\/jof11060422"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1021\/acs.biochem.4c00763","article-title":"Glutamine synthetase: Diverse regulation and functions of an ancient enzyme","volume":"64","author":"Tecson","year":"2025","journal-title":"Biochemistry"},{"key":"ref_49","first-page":"136","article-title":"Analysis of nutritional and nutraceutical properties of wild-grown mushrooms of Nepal","volume":"12","author":"Upadhyaya","year":"2017","journal-title":"EC Microbiol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"103991","DOI":"10.1016\/j.fgb.2025.103991","article-title":"Fungal cell wall biogenesis: Structural complexity, regulation and inhibition","volume":"179","author":"Gow","year":"2025","journal-title":"Fungal Genet. Biol."},{"key":"ref_51","first-page":"775","article-title":"Transcriptome sequencing on six Agaricus bisporus strains at four developmental stages","volume":"34","author":"Shi","year":"2019","journal-title":"J. Agric. Sci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"e00290-20","DOI":"10.1128\/mBio.00290-20","article-title":"The proteasome governs fungal morphogenesis via functional connections with hsp90 and cAMP-protein kinase A signaling","volume":"11","author":"Hossain","year":"2020","journal-title":"MBio"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1259","DOI":"10.1007\/s00253-009-2320-1","article-title":"Light regulation of metabolic pathways in fungi","volume":"85","author":"Schmoll","year":"2010","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Dautt-Castro, M., Rosendo-Vargas, M., and Casas-Flores, S. (2021). The small GTPases in fungal signaling conservation and function. Cells, 10.","DOI":"10.3390\/cells10051039"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"217","DOI":"10.15698\/mic2019.05.677","article-title":"Ser\/Thr protein phosphatases in fungi: Structure, regulation and function","volume":"6","author":"Casamayor","year":"2019","journal-title":"Microb. Cell"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.biocontrol.2013.06.017","article-title":"Advances in fundamental and applied studies in China of fungal biocontrol agents for use against arthropod pests","volume":"68","author":"Wang","year":"2013","journal-title":"Biol. Control"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"e00080-21","DOI":"10.1128\/mSphere.00080-21","article-title":"A conserved machinery underlies the synthesis of a chitosan layer in the Candida chlamydospore cell wall","volume":"6","author":"Bemena","year":"2021","journal-title":"MSphere"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2945","DOI":"10.1534\/g3.117.043331","article-title":"Functional profiling of transcription factor genes in Neurospora crassa","volume":"7","author":"Carrillo","year":"2017","journal-title":"G3"}],"container-title":["Journal of Fungi"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2309-608X\/12\/2\/124\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,2,10]],"date-time":"2026-02-10T11:54:49Z","timestamp":1770724489000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2309-608X\/12\/2\/124"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,2,10]]},"references-count":58,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2026,2]]}},"alternative-id":["jof12020124"],"URL":"https:\/\/doi.org\/10.3390\/jof12020124","relation":{},"ISSN":["2309-608X"],"issn-type":[{"value":"2309-608X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,2,10]]}}}