Discovery of three rare acremonium-like fungi in the rhizosphere of Gaultheria leucocarpa var. yunnanensis resolves the sister relationship between Paraneoaraneomyces and Subuliphorum (Clavicipitaceae, Hypocreales)
Authors/Creators
- 1. State Key Laboratory of Discovery and Utilization of Functional Components in Traditional Chinese Medicine & School of Pharmaceutical Sciences, Guizhou Medical University, Guiyang, China|The High Efficacy Application of Natural Medicinal Resources Engineering Center of Guizhou Province, Guizhou Medical University, Guiyang, China
- 2. College of Biological Science and Food Engineering, Southwest Forestry University, Kunming, China
- 3. State Key Laboratory of Discovery and Utilization of Functional Components in Traditional Chinese Medicine & School of Pharmaceutical Sciences, Guizhou Medical University, Guiyang, China
Description
Rhizosphere soils represent an underexplored reservoir of fungal diversity. In this study, three rare acremonium-like fungi were isolated from the rhizosphere of Gaultheria leucocarpa var. yunnanensis in Guizhou, China. Using a polyphasic taxonomic approach that integrates morphological observations with six-locus phylogenetic analyses (ITS, SSU, LSU, tef-1α, rpb1, and rpb2), the isolates were determined to represent two novel species and one new habitat record. Paraneoaraneomyces guizhouensis and Subuliphorum cylindrosporum are proposed as new species, while the rare species Subuliphorum camptosporum is reported from the plant rhizosphere for the first time. Phylogenetic analyses provide strong support for resolving Paraneoaraneomyces and Subuliphorum as distinct sister genera, a relationship that was previously unresolved. Together with Neoaraneomyces, these genera form a well-defined lineage within Clavicipitaceae. This study expands the known diversity and ecological range of these rare genera, clarifies their phylogenetic placement within Clavicipitaceae, and highlights the importance of rhizosphere sampling in uncovering hidden fungal diversity.
Files
MC_article_192083.pdf
Files
(3.4 MB)
| Name | Size | Download all |
|---|---|---|
|
md5:434b84cf107aba6f77ddd6e00980fe0b
|
3.1 MB | Preview Download |
|
md5:2b578059cd94e1e8c02ce17a552ab6a8
|
317.7 kB | Preview Download |
Linked records
Additional details
References
- Bischoff JF, Rehner SA, Humber RA (2006) Metarhizium frigidum sp. nov.: A cryptic species of M. anisopliae and a member of the M. flavoviride complex. Mycologia 98: 737–745. https://doi.org/10.1080/15572536.2006.11832645
- Castlebury LA, Rossman AY, Sung GH, Hyten AS, Spatafora JW (2004) Multigene phylogeny reveals new lineage for Stachybotrys chartarum, the indoor air fungus. Mycological Research 108(8): 864–872. https://doi.org/10.1017/s0953756204000607
- Chaverri P, Bischoff JF, Liu M, Hodge KT (2005) A new species of Hypocrella, H. macrostroma, and its phylogenetic relationships to other species with large stromata. Mycological Research 109(11): 1268–1275. https://doi.org/10.1017/s0953756205003904
- Chaverri P, Liu M, Hodge KT (2008) A monograph of the entomopathogenic genera Hypocrella, Moelleriella, and Samuelsia gen. nov. (Ascomycota, Hypocreales, Clavicipitaceae), and their aschersonia-like anamorphs in the Neotropics. Studies in Mycology 60: 1–66. https://doi.org/10.3114/sim.2008.60.01
- Chen WH, Liang JD, Ren XX, Zhao JH, Han YF, Liang ZQ (2022) Phylogenetic, ecological and morphological characteristics reveal two new spider-associated genera in Clavicipitaceae. MycoKeys 91: 49–66. https://doi.org/10.3897/mycokeys.91.86812
- Chen H, Bibi S, Tao L, Shen X, Zhao J, Sun Y, Li Q, Tang D, Wang Y (2025) Papiliomyces sinensis (Clavicipitaceae) and Paraisaria pseudoarcta (Ophiocordycipitaceae), two new species parasitizing Lepidopteran insects from southwestern China. MycoKeys 117: 353–374. https://doi.org/10.3897/mycokeys.117.150376
- Christopher LS, Carolyn AY, Neil M, Nicholas K, Pierre-Yves D, Pan J, Simona F, Jennifer SW, Jolanta J, Jerzy WJ, Murray PC, Farman ML (2014) Chapter Ten – Genomes of Plant-Associated Clavicipitaceae. Advances in Botanical Research 70: 291–327. https://doi.org/10.1016/b978-0-12-397940-7.00010-0
- Crous PW, Wingfield MJ, Schumacher RK, Summerell BA, Giraldo A, Gené J, Guarro J, Wanasinghe DN, Hyde KD, Camporesi E, Gareth Jones EB, Thambugala KM, Malysheva EF, Malysheva VF, Acharya K, Álvarez J, Alvarado P, Assefa A, Barnes CW, Bartlett JS, Blanchette RA, Burgess TI, Carlavilla JR, Coetzee MP, Damm U, Decock CA, den Breeÿen A, de Vries B, Dutta AK, Holdom DG, Rooney-Latham S, Manjón JL, Marincowitz S, Mirabolfathy M, Moreno G, Nakashima C, Papizadeh M, Shahzadeh Fazeli SA, Amoozegar MA, Romberg MK, Shivas RG, Stalpers JA, Stielow B, Stukely MJ, Swart WJ, Tan YP, van der Bank M, Wood AR, Zhang Y, Groenewald JZ (2014) Fungal Planet description sheets: 281–319. Persoonia 33: 212–289. https://doi.org/10.3767/003158514X685680
- Currie CR, Bot ANM, Boomsma JJ (2003) Experimental evidence of a tripartite mutualism: bacteria protect ant fungus gardens from specialized parasites. Oikos 101: 91–102. https://doi.org/10.1034/j.1600-0706.2003.12036.x
- Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9(8): 772. https://doi.org/10.1038/nmeth.2109
- Ding MM, Li YP, Bai Y, Gai PZ, Wang J, Jiang ZZ (2024) Albacillium hingganense gen. sp. nov. (Clavicipitaceae) from forest litters in Northeast China. Phytotaxa 650: 157–168. https://doi.org/10.11646/phytotaxa.650.2.3
- Gams W (1971) Cephalosporium-artige Schimmelpilze (Hyphomycetes). G. Fischer Publishing, Stuttgart, Germany.
- Gao S, Meng W, Zhang L, Yue Q, Zheng X, Xu L (2021) Parametarhizium (Clavicipitaceae) gen. nov. with two new species as a potential biocontrol agent isolated from forest litters in Northeast China. Frontiers in Microbiology 12: e627744. https://doi.org/10.3389/fmicb.2021.627744
- Hernández-Restrepo M, Groenewald JZ, Crous PW (2016) Taxonomic and phylogenetic re-evaluation of Microdochium, Monographella and Idriella. Persoonia 36: 57–82. https://doi.org/10.3767/003158516X688676
- Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2017) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35(2): 518–522. https://doi.org/10.1093/molbev/msx281
- Hopple JS (1994) Phylogenetic investigations in the genus Coprinus based on morphological and molecular characters. Ph.D. Dissertation, Duke University, Durham, NC, USA
- Hou LW, Giraldo A, Groenewald JZ, Rämä T, Summerbell RC, Huang GZ, Cai L, Crous PW (2023) Redisposition of acremonium-like fungi in Hypocreales. Studies in Mycology 105(1): 23–203. https://doi.org/10.3114/sim.2023.105.02
- Hu YJ, Lan Q, Su BJ, Chen ZF, Liang D (2022) Structurally diverse abietane-type Diterpenoids from the aerial parts of Gaultheria leucocarpa var. yunnanensis. Phytochemistry 201: 113255. https://doi.org/10.1016/j.phytochem.2022.113255
- Hu YJ, Lan Q, Su BJ, Wang Y, Liang D (2024) Three new phenolic glycosides and a new lignan glycoside from Gaultheria leucocarpa var. yunnanensis. Fitoterapia 172: 105740. https://doi.org/10.1016/j.fitote.2023.105740
- Huang H, Wang M, Zhang L, Yue HM, Gong WF, Cai L (2015) Pochonia cordycepisociata, a new species associated with Chinese cordyceps in Tibet, China. Phytotaxa 208(4): 278–286. https://doi.org/10.11646/phytotaxa.208.4.3
- Jeewon R, Hyde KD (2016) Establishing species boundaries and new taxa among fungi: recommendations to resolve taxonomic ambiguities. Mycosphere 7(11): 1669–1677. https://doi.org/10.5943/mycosphere/7/11/4
- Johnson D, Sung GH, Hywel-Jones NL, Luangsa-ard JJ, Bischoff JF, Kepler RM, Spatafora JW (2009) Systematics and evolution of the genus Torrubiella (Hypocreales, Ascomycota). Mycological Research 113(3): 279–89. https://doi.org/10.1016/j.mycres.2008.09.008
- Kalyaanamoorthy S, Minh BQ, Wong TKF, 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
- Kepler RM, Sung GH, Ban S, Nakagiri A, Chen MJ, Huang B, Li Z, Spatafora JW (2012a) New teleomorph combinations in the entomopathogenic genus Metacordyceps. Mycologia 104(1): 182–197. https://doi.org/10.3852/11-070
- Kepler RM, Sung GH, Harada Y, Tanaka K, Tanaka E, Hosoya T, Bischoff JF, Spatafora JW (2012b) Host jumping onto close relatives and across kingdoms by Tyrannicordyceps (Clavicipitaceae) gen. nov. and Ustilaginoidea (Clavicipitaceae). American Journal of Botany 99(3): 552–561. https://doi.org/10.3732/ajb.1100124
- Kepler RM, Humber RA, Bischoff JF, Rehner SA (2014) Clarification of generic and species boundaries for Metarhizium and related fungi through multigene phylogenetics. Mycologia 106(4): 811–829. https://doi.org/10.3852/13-319
- Lawrey JD, Etayo J, Dal-Forno M, Driscoll KE, Diederich P (2015) Molecular data support establishment of a new genus for the lichenicolous species Neobarya usneae (Hypocreales). The Bryologist 118(1): 83–92. https://doi.org/10.1639/0007-2745-118.1.083
- Lin L, Lin Y, Keyhani NO, Pu H, Yang J, Xiong C, Shang J, Mao Y, Yang L, Zheng M, Zhu M, Mu T, Li Y, Liang H, Fan L, Ma X, Ma H, Xiong W, Qiu J, Guan X (2025) New entomopathogenic species in the Clavicipitaceae family (Hypocreales, Ascomycota) from the subtropical forests of Fujian, China. Front Microbiology 3(16): 1532341. https://doi.org/10.3389/fmicb.2025.1532341
- Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: Evidence from an RNA polymerse II subunit. Molecular Biology and Evolution 16(12): 1799–1808. https://doi.org/10.1093/oxfordjournals.molbev.a026092
- Luangsa-ard JJ, Mongkolsamrit S, Thanakitpipattana D, Khonsanit A, Tasanathai K, Noisripoom W, Humber RA (2017) Clavicipitaceous entomopathogens: New species in Metarhizium and a new genus Nigelia. Mycological Progress 16(4): 369–391. https://doi.org/10.1007/s11557-017-1277-1
- Marcelino JAP, Gouli S, Giordano R, Gouli VV, Parker BL, Skinner M (2009) Fungi associated with a natural epizootic in Fiorinia externa Ferris (Hemiptera: Diaspididae) Journal of Applied Entomology 133(2): 82–89. https://doi.org/10.1111/j.1439-0418.2008.01301.x
- 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
- Mongkolsamrit S, Luangsa-ard JJ, Hywel-Jones NL (2011) Samuelsia mundiveteris sp. nov. from Thailand. Mycologia 103(4): 921–927. https://doi.org/10.3852/11-049
- Mongkolsamrit S, Khonsanit A, Thanakitpipattana D, Tasanathai K, Noisripoom W, Lamlertthon S, Himaman W, Houbraken J, Samson RA, Luangsa-ard JJ (2020) Revisiting Metarhizium and the description of new species from Thailand. Studies in Mycology 95: 171–251. https://doi.org/10.1016/j.simyco.2020.04.001
- Mongkolsamrit S, Noisripoom W, Thanakitpipattana D, Khonsanit A, Lamlertthon S, Luangsa-ard JJ (2021) New species in Aciculosporium, Shimizuomyces and a new genus Morakotia associated with plants in Clavicipitaceae from Thailand. Fungal Systematics and Evolution 8: 27–37. https://doi.org/10.3114/fuse.2021.08.03
- Nonaka K, Omura S, Masuma R, Kaifuchi S, Masuma R (2013) Three new Pochonia taxa (Clavicipitaceae) from soils in Japan. Mycologia 105(5): 1202–1218. https://doi.org/10.3852/12-132
- Píchová K, Pažoutová S, Kostovčík M, Chudíčková M, Stodůlková E, Novák P, Flieger M, van der Linde E, Kolařík M (2018) Evolutionary history of ergot with a new infrageneric classification (Hypocreales: Clavicipitaceae: Claviceps). Molecular Phylogenetics and Evolution 123: 73–87. https://doi.org/10.1016/j.ympev.2018.02.013
- Rehner SA, Buckley EA (2005) Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97(1): 84–98. https://doi.org/10.3852/mycologia.97.1.84
- Rehner SA, Samuels GJ (1995) Molecular systematics of the Hypocreales: A teleomorph gene phylogeny and the status of their anamorphs. Canadian Journal of Botany 73(S1): 816–823. https://doi.org/10.1139/b95-327
- 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
- Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: Plant-dependent enrichment and seasonal shifts revealed. Applied and Environmental Microbiology 67(10): 4742–4751. https://doi.org/10.1128/AEM.67.10.4742-4751.2001
- Spatafora JW, Sung GH, Sung JM, Hywel‐Jones NL, White Jr JF (2007) Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Molecular Ecology 16(8): 1701–1711. https://doi.org/10.1111/j.1365-294X.2007.03225.x
- Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology 57: 758–771. https://doi.org/10.1080/10635150802429642
- Sung GH, Spatafora JW, Zare R, Gams W (2001) A revision of Verticillium sect. Prostrata. II. Phylogenetic analyses of SSU and LSU nuclear rDNA sequences from ana morphs and teleomorphs of the Clavicipitaceae. Nova Hedwigia 72(3–4): 311–328. https://doi.org/10.1127/nova.hedwigia/72/2001/311
- Sung GH, Hywel-Jones NL, Sung JM, Luangsa-ard JJ, Shrestha B, Spatafora JW (2007a) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Studies in Mycology 57: 5–59. https://doi.org/10.3114/sim.2007.57.01
- Sung GH, Sung JM, HywelJones NL, Spatafora JW (2007b) A multigene phylogeny of Clavicipitaceae (Ascomycota, Fungi): Identification of localized incongruence using a combinational bootstrap approach. Molecular Phylogenetics and Evolution 44(3): 1204–1223. https://doi.org/10.1016/j.ympev.2007.03.011
- Tanaka E, Tanaka C, Gafur A, Tsuda M (2002) Heteroepichloë, gen. nov. (Clavicipitaceae; Ascomycotina) on bamboo plants in East Asia. Mycoscience 43: 87–93. https://doi.org/10.1007/s102670200014
- Tanaka E, Hosoe T, Degawa Y, Kolařík M (2021) Revision of the genus Aciculosporium (Clavicipitaceae) with a description of a new species on wavyleaf basketgrass, and proline-containing cyclic dipeptide production by A. take. Mycoscience 62(3): 166–175. https://doi.org/10.47371/mycosci.2021.01.002
- Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
- Vu D, Groenewald M, de Vries M, Gehrmann T, Stielow B, Eberhardt U, AlHatmi A, Groenewald JZ, Cardinali G, Houbraken J, Boekhout T, Crous PW, Robert V, Verkley GJM (2019) Large-scale generation and analysis of filamentous fungal DNA bar codes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Studies in Mycology 92: 135–154. https://doi.org/10.1016/j.simyco.2018.05.001
- Wang X, Sun Y, Ling L, Ren X, Liu X, Wang Y, Dong Y, Ma J, Song R, Yu A, Wei J, Fan Q, Guo M, Zhao T, Dao R, She G (2021) Gaultheria leucocarpa var. yunnanensis for treating rheumatoid arthritis—an assessment combining machine learning-guided ADME properties prediction, network pharmacology, and pharmacological assessment. Frontiers in Pharmacology 12: 704040. https://doi.org/10.3389/fphar.2021.704040
- Wang X, Dong Y, Song R, Yu A, Wei J, Fan Q, Yao J, Shan D, Zhong X, Lv F, She G (2022) Intestinal metabolism and absorption mechanism of multi-components in Gaultheria leucocarpa var. yunnanensis – an assessment using in situ and in vitro models, comparing gut segments in pathological with physiological conditions. Journal of Ethnopharmacology 286: 114844. https://doi.org/10.1016/j.jep.2021.114844
- Wang Y, Tang DX, Luo R, Wang YB, Thanarut C, Dao VM, Yu H (2023) Phylogeny and systematics of the genus Clonostachys. Frontiers in Microbiology 14: 1117753. https://doi.org/10.3389/fmicb.2023.1117753
- Wang Y, Tang DX, Chen H, Li QR, Loinheuang C, Shen XC (2025) Phylogenetic evidence reveal a close relationship between Amphichorda and Ovicillium in Bionectriaceae (Hypocreales). MycoKeys 117: 337–352. https://doi.org/10.3897/mycokeys.117.151366
- Wen TC, Zha LS, Xiao YP, Wang Q, Kang JC, Hyde KD (2015) Metacordyceps shibinense sp. nov. from larvae of Lepidoptera in Guizhou Province, southwest China. Phytotaxa 226(1): 51–62. https://doi.org/10.11646/phytotaxa.226.1.5
- White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplifcation and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: A guide to methods and applications. Academic 315–322. https://doi.org/10.1016/b978-0-12-372180-8.50042-1
- Xiao YP, Wen TC, Hongsanan S, Jeewon R, Luangsa-ard JJ, Brook S, Wanasinghe DN, Long FY, Hyde KD (2018) Multigene phylogenetics of Polycephalomyces (Ophiocordycipitaceae, Hypocreales), with two new species from Thailand. Scientific Reports 8(1): 18087. https://doi.org/10.1038/s41598-018-36792-4
- Zare R, Gams W, Culham A (2000) A revision of Verticillium sect. Prostrata. I. Phylogenetic studies using ITS sequences Nova Hedwigia 71: 465–480. https://doi.org/10.1127/nova/71/2000/465
- Zhang B, He XL, Ding Y, Du GH (2006) Gaultherin, a natural salicylate derivative from Gaultheria yunnanensis: towards a better non-steroidal anti-inflammatory drug. European Journal of Pharmacology 530: 166–171. https://doi.org/10.1016/j.ejphar.2005.11.030
- Zhang ZY, Feng Y, Tong SQ, Ding CY, Tao G, Han YF (2023) Morphological and phylogenetic characterisation of two new soil-borne fungal taxa belonging to Clavicipitaceae (Hypocreales, Ascomycota). MycoKeys 98: 113–132. https://doi.org/10.3897/mycokeys.98.106240