Seven new species of the Rhodocybe– Clitopilus clade (Entolomataceae, Agaricales) from Northeast China
Authors/Creators
- 1. College of Mycology, Jilin Agricultural University, Changchun, China|Ministry of Agriculture and Rural Affairs, Jilin Agricultural University, Changchun, China
Description
The Rhodocybe–Clitopilus clade of Entolomataceae exhibits high diversity in Northeast China, yet taxonomic studies on this group remain limited. Based on a field investigation conducted in this region (Jilin and Heilongjiang provinces), combined with morphological characteristics and multigene phylogenetic analyses (ITS, nrLSU, rpb2, and tef1-α), seven new species within four genera are proposed: Clitopilus fraxinicola, Lulesia variabilicolor, Rhodocybe jilinensis, R. galericulata, R. eburneolutea, R. subnuciolens, and Rhodophana hongshiensis. Phylogenetic analyses support the independent taxonomic status of these species within their respective genera. Detailed morphological descriptions, color photographs of basidiomata, and illustrations of microstructures are provided. Additionally, a dichotomous key to the known species of the Rhodocybe–Clitopilus clade in Northeast China is presented.
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- Abarenkov K, Nilsson RH, Larsson K-H, Taylor AFS, May TW, Frøslev TG, Pawlowska J, Lindahl B, Põldmaa K, Truong C, Vu D, Hosoya T, Niskanen T, Piirmann T, Ivanov F, Zirk A, Peterson M, Cheeke TE, Ishigami Y, Jansson AT, Jeppesen TS, Kristiansson E, Mikryukov V, Miller JT, Oono R, Ossandon FJ, Paupério J, Saar I, Schigel D, Suija A, Tedersoo L, Kõljalg U (2024) The UNITE database for molecular identification and taxonomic communication of fungi and other eukaryotes: Sequences, taxa and classifications reconsidered. Nucleic Acids Research 52(D1): D791–D797. https://doi.org/10.1093/nar/gkad1039
- Agerer R (1997) Entoloma sinuatum (Bull.:Fr.) Kummer + Salix spec. Descriptions of Ectomycorrhizae 2: 13–18.
- Altschul SF, Madden TL, Schäffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research 25(17): 3389–3402. https://doi.org/10.1093/nar/25.17.3389
- Angelini C, Contu M (2012) Lulesia densifolia (Basidiomycota, Agaricomycetes) rinvenuta nella Repubblica Dominicana (Caraibi). Bollettino dell'Associazione Micologica ed Ecologica Romana 86(2): 20–24.
- Antibus RK, Croxdale JG, Miller OK, Linkins AE (1981) Ectomycorrhizal fungi of Salix rotundifolia III. Resynthesized mycorrhizal complexes and their surface phosphatase activities. Canadian Journal of Botany 59(12): 2458–2465. https://doi.org/10.1139/b81-297
- Asif M, Saba M, Akram W, Maula F, Ullah F, Batool M, Ullah M, Krisai-Greilhuber I, Raza M (2025) Integrative taxonomy and multigene phylogeny uncover three novel taxa of the genus Clitopilus from southern Punjab, Pakistan. Mycological Progress 24(1): 1–28. https://doi.org/10.1007/s11557-025-02047-6
- Bailey AM, Alberti F, Kilaru S, Collins CM, de Mattos-Shipley K, Hartley AJ, Hayes P, Griffin A, Lazarus CM, Cox RJ, Willis CL, O'Dwyer K, Spence DW, Foster GD (2016) Identification and manipulation of the pleuromutilin gene cluster from Clitopilus passeckerianus for increased rapid antibiotic production. Scientific Reports 6: е25202. https://doi.org/10.1038/srep25202
- Baroni TJ (1981) A revision of the genus Rhodocybe Maire (Agaricales). Beihefte zur Nova Hedwigia 67: 1–194.
- Baroni TJ, Gates GM (2006) New species and records of Rhodocybe (Entolomataceae, Agaricales) from Tasmania. Australian Systematic Botany 19(4): 343–358. https://doi.org/10.1071/sb06002
- Baroni TJ, Horak E (1994) Entolomataceae in North America III: New taxa, new combinations and notes on species of Rhodocybe. Mycologia 86(1): 138–145. https://doi.org/10.1080/00275514.1994.12026385
- Baroni TJ, Matheny PB (2011) A re-evaluation of gasteroid and cyphelloid species of Entolomataceae from eastern North America. Harvard Papers in Botany 16(2): 293–310. https://doi.org/10.3100/0.25.016.0205
- Baroni TJ, Angelini C, Bergemann SE, Lodge DJ, Lacey L, Curtis TA, Cantrell SA (2020) Rhodocybe–Clitopilus clade (Entolomataceae, Basidiomycota) in the Dominican Republic: New taxa and first reports of Clitocella, Clitopilus, and Rhodocybe for Hispaniola. Mycological Progress 19(10): 1083–1099. https://doi.org/10.1007/s11557-020-01619-y
- Bas C, Kuyper TW, Noordeloos ME, Vellinga EC (1988) Flora Agaricina Neerlandica (Vol. 1). A.A. Balkema, Rotterdam, 182 pp.
- Bau T (2018) Mushroom Taxonomy. Science Press, Beijing, 303 pp.
- Co-David D, Langeveld D, Noordeloos ME (2009) Molecular phylogeny and spore evolution of Entolomataceae. Persoonia 23: 147–176. https://doi.org/10.3767/003158509X480944
- Contu M (2006) Rhodocybe brunnea spec. nov. (Basidiomycota, Entolomataceae), a new species of the section Rhodocybe from Sardinia. Micologia e Vegetazione Mediterranea 21(1): 87–96.
- Cooper JA (2014) New species and combinations of some New Zealand agarics belonging to Clitopilus, Lyophyllum, Gerhardtia, Clitocybe, Hydnangium, Mycena, Rhodocollybia and Gerronema. Mycosphere 5(2): 263–288. https://doi.org/10.5943/mycosphere/5/2/2
- Deng WQ, Li TH, Shen YH (2013) A new species of Clitopilus from southwestern China. Mycotaxon 122: 443–447. https://doi.org/10.5248/122.443
- Dima B, Papp V, Szabó E, Brandrud TE, Noordeloos ME, Kovács GM (2018) Revealing the phylogenetic relationship in the Rhodophana nitellina complex. Poster. https://www.researchgate.net/publication/328603192
- Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Molecular Ecology 2(2): 113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
- Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology 59(3): 307–321. https://doi.org/10.1093/sysbio/syq010
- Henkel TW, Largent DL, Aime MC, Baroni TJ (2010) The Entolomataceae of the Pakaraima Mountains of Guyana III: New species of Rhodocybe. Mycoscience 51(1): 23–27. https://doi.org/10.1007/s10267-009-0008-0
- Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35(2): 518–522. https://doi.org/10.1093/molbev/msx281
- Horak E (1979) Fungi agaricini Novazelandiae VII. Rhodocybe Maire. New Zealand Journal of Botany 17(3): 275–281. https://doi.org/10.1080/0028825X.1979.10426901
- Izhar A, Khan Z, Asif M, Bashir H, Rani AK, Niazi AR, Khalid AN (2023) Clitopilus cretoalbus sp. nov. (Entolomataceae, Agaricales), a new species from Pakistan. European Journal of Taxonomy 861: 168–184. https://doi.org/10.5852/ejt.2023.861.2075
- Jian SP (2020a) The Application of DNA Barcoding Technology in Species Identification of Clitopilus, Clitocella and Clitopilopsis. Master Thesis, Yunnan University, Kunming, China.
- Jian SP, Bau T, Zhu XT, Deng WQ, Yang ZL, Zhao ZW (2020b) Clitopilus, Clitocella, and Clitopilopsis in China. Mycologia 112(2): 371–399. https://doi.org/10.1080/00275514.2019.1703089
- Jian SP, Wang XH, Deng WQ, Yang ZL (2023) Clitopilus in southern China: Two new species and comments on C. subscyphoides. Mycological Progress 22(5): 1–35. https://doi.org/10.1007/s11557-023-01885-6
- Jian SP, Chen X, Yang TW, Xu XJ, Gao F, Fang YW, Liu J, Zhang CX (2025) Biotrophic and saprophytic fungi from the Rhodocybe–Clitopilus clade (Entolomataceae): Two new species and one new record in subtropical China. MycoKeys 116: 227–247. https://doi.org/10.3897/mycokeys.116.148775
- Kalyaanamoorthy S, Minh BQ, Wong TK, von Haeseler A, Jermiin LS (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14(6): 587–589. https://doi.org/10.1038/nmeth.4285
- Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20(4): 1160–1166. https://doi.org/10.1093/bib/bbx108
- Khan Z, Khalid AN (2024) Molecular phylogeny and morphology reveal a new species of genus Rhodocybe sensu stricto Maire (Entolomataceae; Agaricales) from Pakistan. Cryptogamie, Mycologie 45(10): 127–137. https://doi.org/10.5252/cryptogamie-mycologie2024v45a10
- Kluting KL, Baroni TJ, Bergemann SE (2014) Toward a stable classification of genera within the Entolomataceae: A phylogenetic re-evaluation of the Rhodocybe–Clitopilus clade. Mycologia 106(6): 1127–1142. https://doi.org/10.3852/13-270
- Koch RA, Herr JR (2021) Transcriptomics reveals the putative mycoparasitic strategy of the mushroom Entoloma abortivum on species of the mushroom genus Armillaria. mSystems 6(5): e00544-21. https://doi.org/10.1128/msystems.00544-21
- Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7): 1870–1874. https://doi.org/10.1093/molbev/msw054
- Loree MAJ, Lumme I, Niemi M, Tormala T (1989) Inoculation of willows (Salix spp.) with ectomycorrhizal fungi on mined boreal peatland. Plant and Soil 116(2): 229–238. https://doi.org/10.1007/bf02214552
- Matheny PB (2005) Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales). Molecular Phylogenetics and Evolution 35(1): 1–20. https://doi.org/10.1016/j.ympev.2004.11.014
- Matheny PB, Wang Z, Binder M, Curtis JM, Lim YW, Nilsson RH, Hughes KW, Hofstetter V, Ammirati JF, Schoch CL, Langer E, Langer G, McLaughlin DJ, Wilson AW, Frøslev T, Ge ZW, Kerrigan RW, Slot JC, Yang ZL, Baroni TJ, Fischer M, Hosaka K, Matsuura K, Seidl MT, Vauras J, Hibbett DS (2007) Contributions of rpb2 and tef1 to the phylogeny of mushrooms and allies (Basidiomycota, Fungi). Molecular Phylogenetics and Evolution 43(2): 430–451. https://doi.org/10.1016/j.ympev.2006.08.024
- Mao N, Lv JC, Xu YY, Zhao TY, Fan L (2022) Two new Clitocella species from North China revealed by phylogenetic analyses and morphological characters. MycoKeys 88: 151–170. https://doi.org/10.3897/mycokeys.88.80068
- Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R (2020) IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37(5): 1530–1534. https://doi.org/10.1093/molbev/msaa015
- Moreno G, Contu M, Ortega A, Platas G, Peláez F (2007) Molecular phylogenetic studies show Omphalina giovanellae represents a new section of Clitopilus (Agaricomycetes). Mycological Research 111(12): 1399–1405. https://doi.org/10.1016/j.mycres.2007.09.009
- Murrill WA (1913) The Agaricaceae of the Pacific Coast—IV. New species of Clitocybe and Melanoleuca. Mycologia 5(4): 206–223. https://doi.org/10.1080/00275514.1913.12018520
- Nation JL (1983) A new method using hexamethyldisilazane for preparation of soft insect tissues for scanning electron microscopy. Stain Technology 58(6): 347–351. https://doi.org/10.3109/10520298309066811
- Noordeloos ME (1984) Notulae ad floram agaricinam neerlandicam–IV–V Clitopilus and Leucopaxillus. Persoonia 12(2): 155–167.
- Noordeloos ME, Gates GM, Sachs AW (2012) The Entolomataceae of Tasmania. Springer, New York, 400 pp. https://doi.org/10.1007/978-94-007-4679-4
- Papetti C (2014) Agaricus nitellinus var. minor, una piccola Rhodocybe di Fries dimenticata. Rivista di Micologia 57(4): 301–314.
- Papetti C (2024) Rhodophana almae-lunae una nuova specie del gruppo di Rhodophana nitellina. Rivista di Micologia 66(3): 195–208.
- Peng L, Shan XL, Wang YC, Martin F, Vilgalys R, Yuan ZL (2021) Hybrid genome assembly and gene repertoire of the root endophyte Clitopilus hobsonii QYL-10 (Entolomataceae, Agaricales, Basidiomycetes). Molecular Plant-Microbe Interactions 34(6): 711–714. https://doi.org/10.1094/MPMI-11-20-0328-A
- Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67(5): 901–904. https://doi.org/10.1093/sysbio/syy032
- Rehner SA, Samuels GJ (1994) Taxonomy and phylogeny of Gliocladium analysed from nuclear large subunit ribosomal DNA sequences. Mycological Research 98(6): 625–634. https://doi.org/10.1016/S0953-7562(09)80409-7
- Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029
- Sánchez-García M, Matheny PB (2017) Is the switch to an ectomycorrhizal state an evolutionary key innovation in mushroom-forming fungi? A case study of the Tricholomatineae (Agaricales). Evolution 71: 51–65. https://doi.org/10.1111/evo.13099
- Sayers EW, Cavanaugh M, Frisse L, Pruitt KD, Schneider VA, Underwood BA, Yankie L, Karsch-Mizrachi I (2025) GenBank 2025 update. Nucleic Acids Research 53(D1): D56–D61. https://doi.org/10.1093/nar/gkae1114
- Sesli E, Vizzini A (2017) Two new Rhodocybe species (sect. Rufobrunnea, Entolomataceae) from the East Black Sea coast of Turkey. Turkish Journal of Botany 41(2): 200–210. https://doi.org/10.3906/bot-1607-1
- Shishikura M, Takemura Y, Sotome K, Maegawa N, Nakagiri A, Endo N (2021) Four mycelial strains of Entoloma clypeatum species complex form ectomycorrhiza-like roots with Pyrus betulifolia seedlings in vitro, and one develops fruiting bodies 2 months after inoculation. Mycorrhiza 31(1): 31–42. https://doi.org/10.1007/s00572-020-00994-4
- Singer R (1986) The Agaricales in Modern Taxonomy (4th edn.), Koeltz Scientific Books, Koenigstein, 981 pp.
- Song HB, Bau T (2024) Resolving the polyphyletic origins of Pholiotina s.l. (Bolbitiaceae, Agaricales) based on Chinese materials and reliable foreign sequences. Mycosphere 15(1): 1595–1674. https://doi.org/10.5943/mycosphere/15/1/14
- Sun YL, Bau T (2023) Rhodocybe subasyae, a new species of Rhodocybe sect. Rufobrunnea (Entolomataceae, Agaricales) from northeast China. Mycoscience 64(3): 96–100. https://doi.org/10.47371/mycosci.2023.03.001
- Varga T, Krizsán K, Földi C, Dima B, Sánchez-García M, Sánchez-Ramírez S, Szöllősi GJ, Szarkándi JG, Papp V, Albert L, Andreopoulos W, Angelini C, Antonín V, Barry KW, Bougher NL, Buchanan P, Buyck B, Bense V, Catcheside P, Chovatia M, Cooper J, Dämon W, Desjardin D, Finy P, Geml J, Haridas S, Hughes K, Justo A, Karasiński D, Kautmanova I, Kiss B, Kocsubé S, Kotiranta H, LaButti KM, Lechner BE, Liimatainen K, Lipzen A, Lukács Z, Mihaltcheva S, Morgado LN, Niskanen T, Noordeloos ME, Ohm RA, Ortiz-Santana B, Ovrebo C, Rácz N, Riley R, Savchenko A, Shiryaev A, Soop K, Spirin V, Szebenyi C, Tomšovský M, Tulloss RE, Uehling J, Grigoriev IV, Vágvölgyi C, Papp T, Martin FM, Miettinen O, Hibbett DS, Nagy LG (2019) Megaphylogeny resolves global patterns of mushroom evolution. Nature Ecology & Evolution 3(4): 668–678. https://doi.org/10.1038/s41559-019-0834-1
- Vila J, Contu M, Caballero F, Català S, Ribes MA (2009) Nuevos datos sobre el género Clitopilus (incl. Rhodocybe) en la península Ibérica e Islas Canarias. Bollettino dell'Associazione Micologica ed Ecologica Romana 25(77–78): 3–14.
- Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172(8): 4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
- Vizzini A, Picillo B, Ercole E, Vila J, Contu M (2016) Rhodocybe formosa (Agaricales, Entolomataceae): New collections, molecular data and synonymy, and Rhodocybe griseonigrella comb. nov. Phytotaxa 255(1): 34–46. https://doi.org/10.11646/phytotaxa.255.1.3
- Vizzini A, Alvarado P, Consiglio G, Angelini C, Marchetti M (2023a) Lulesia Singer (1970), an older name for Clitocella Kluting, TJ Baroni & Bergemann (2014, Entolomataceae). Rivista Micologica Romana 39: 3–23. https://doi.org/10.57624/AMER.2023.18
- Vizzini A, Consiglio G, Marchetti M (2023b) Overview of the European species of the genus Clitocella (Entolomataceae, Agaricales) with notes on extralimital taxa. Persoonia 50: 123–157. https://doi.org/10.3767/persoonia.2023.50.04
- Vrinda KB, Pradeep CK, Mathew S, Abraham TK (1999) Agaricales from Western Ghats–VI. Indian Phytopathology 52(2): 198–200. https://doi.org/10.54207/bsmps1000-1997-822r2p
- Wang JR, Bau T (2013) A new species and a new record of the genus Entoloma from China. Mycotaxon 124(1): 165–171. https://doi.org/10.5248/124.165
- White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (Eds) PCR Protocols. Academic Press, San Diego, 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
- Wong TKF, Ly-Trong N, Ren H, Banos H, Roger AJ, Susko E, Bielow C, De Maio N, Goldman N, Hahn MW, Huttley G, Lanfear R, Minh BQ (2025) IQ-TREE 3: Phylogenomic inference software using complex evolutionary models. EcoEvoRxiv. https://doi.org/10.32942/X2P62N
- Wu F, Zhou LW, Yang ZL, Bau T, Li TH, Dai YC (2019) Resource diversity of Chinese macrofungi: Edible, medicinal and poisonous species. Fungal Diversity 98: 1–76. https://doi.org/10.1007/s13225-019-00432-7
- Xiao YQ, Xu YD, Chen ZH, He XH, He ZM (2024) Lulesia umbrinomarginata (Entolomataceae, Agaricales), a newly discovered species from Southern China. Phytotaxa 650(1): 60–72. https://doi.org/10.11646/phytotaxa.650.1.5
- Xu JZ, Jiang Y, Wang TT, Zhang D, Li XB, Hosen MI (2023) Morphological characteristics and phylogenetic analyses revealed four new species of Agaricales from China. Frontiers in Microbiology 14: е1118525. https://doi.org/10.3389/fmicb.2023.1118525
- Yang KL, Lin JY, Li GM, He XH, Yang ZL (2025) New and interesting fungi from Guangzhou City, South China. Phytotaxa 707(1): 1–95. https://doi.org/10.11646/phytotaxa.707.1.1
- Ye QQ (2022) Taxonomy and molecular phylogeny of Entoloma s.l. in Jilin Province. Master Thesis, Jilin Agricultural University, Changchun, China.
- Zhang YW, Wang YC, Druzhinina IS, Vasco F, Zhong DL, Peng L, Yao JJ, Yuan ZL, Martin FM (2026) Ecological genomics of saprotrophy to biotrophy transitions in the genus Clitopilus (Fr. ex Rabenh.) P. Kumm. (Agaricales, Entolomataceae). IMA Fungus 17: e179417. https://doi.org/10.3897/imafungus.17.179417
- Zhao D, Ye T, Gao F, Jakovlić I, La Q, Tong Y, Liu X, Song R, Liu F, Lian Z, Zou H, Li WX, Wang GT, Zeng B, Zhang D (2025) PhyloSuite v2: The development of an all-in-one, efficient and visualization-oriented suite for molecular dating analysis and other advanced features. iMeta: e70095. https://doi.org/10.1002/imt2.70095
- Zhong XR (2019) Phylogenetic and taxonomic studies on Clitopilus and its allied genera resources from China, Master Thesis, South China Agricultural University, Guangzhou, China.