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Research Article
Morphological characteristics and phylogenetic analyses revealed two new species from China and a new record from Jilin Province of Agaricales
expand article infoDi Zhang‡§, Jun-Jie Peng‡, Jia-Jun Wang‡, A. K. Hasith Priyashnatha|, Jin-Peng Liao, Hua-Xing Luo#, Shi-Chen Huang§, Ji-Ze Xu‡
‡ JiLin Agricultural Science and Technology University, Jilin, China
§ Yanbian University, Yanbian, China
| Chiang Mai University, Chiang Mai, Thailand
¶ Management Bureau of Tianbaoyan National Nature Reserve in Yong'an, Yongan, China
# Yong'an Zhisheng Chemical Union Co., Ltd, Yongan, China

Corresponding author: Shi-Chen Huang ( schuang@ybu.edu.cn )

Corresponding author: Ji-Ze Xu ( xujize@163.com )

Academic editor: Ajay Kumar Gautam
© 2024 Di Zhang, Jun-Jie Peng, Jia-Jun Wang, A. K. Hasith Priyashnatha, Jin-Peng Liao, Hua-Xing Luo, Shi-Chen Huang, Ji-Ze Xu.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Zhang D, Peng J-J, Wang J-J, Priyashnatha AKH, Liao J-P, Luo H-X, Huang S-C, Xu J-Z (2024) Morphological characteristics and phylogenetic analyses revealed two new species from China and a new record from Jilin Province of Agaricales. MycoKeys 109: 73-90. https://doi.org/10.3897/mycokeys.109.128960
Open Access

Abstract

In this study, we have found two new species—Stropharia subrugosoannulata and Stropharia microaeruginosa. Phylogenetic analyses, based on the internal transcribed spacer regions (ITS) and the nuclear ribosomal RNA gene (nrLSU), suggest that the two new species are distinct and monophyletic. S. subrugosoannulata is distinguished from other species of the genus Stropharia by the pileus covered with greyish-orange squamules in the centre, stipe light brown and surface covered with white triangular squamules. S. microaeruginosa differs from other species in its pileus bluish-grey when young becoming lighter towards margins, later greyish-turquoise lightens towards the edges and surface radially striate when young, lamellae adnate to subdecurrent, stipe with white squamules at the base, acanthocytes absent. The new record species from Jilin Province, Clitolyophyllum umbilicatum was also confirmed, based on morphological and molecular study. Here, we have given full descriptions of each species, colour images, illustrations and two phylogenetic trees that show the placement and relationship of the two new species and the new record are provided.

Key words

Clitolyophyllum, morphological characteristics, new species, phylogenetic analyses, Stropharia

Introduction

Stropharia (Fr.) Quél. is the type genus of the family Strophariaceae Singer & A.H. Sm. Species of Stropharia are characterised mainly by pileus with viscid to dry, slightly hygrophanous or not, glabrous to floccose to squamous surface, a central, cylindrical, viscid or dry stipe often with a distinct annulus or annular zone, lamellae are dark purple, purplish-grey, or brownish-grey and the base of the stipe has white rhizoids (Murrill 1918, 1922; Hawksworth et al. 1983). Many species in this genus are well-known medicinal fungi, such as Stropharia rugosoannulata Farl. ex Murrill Stropharia cubensis Earle and others (Dai et al. 2012).

Fries (1821) had recognised three clades within Agaricus and placed Stropharia in Tribus Psalliota. In order to accommodate a number of morphologically distinct species within Agaricus, Fries (1849) established subgenus Stropharia. Singer and Smith (1946) were raised to the genus level of subgenus Stropharia in 1946. The 7th and 8th editions of the Dictionary of the Fungi also adopts the classification of Singer et al. (Hawksworth et al. 1983, 1995). However, Smith (1979) changed his view and later on, together with Kühner (1980) and Holland (1984), placed the subgenera of Stropharia and others within Psilocybe. Noordeloos (1995, 1999) also supports this viewpoint. The 9th and 10th editions of the Dictionary of the Fungi categorise Stropharia in Psilocybe (Kirk et al. 2001, 2008). In contrast, molecular studies have supported it as an independent genus (Moncalvo et al. 2002; Matheny et al. 2006; Tian and Matheny 2021).

The species of Stropharia have a widespread distribution all over the world. Currently, over 351 records have been listed in Index Fungorum and 185 legal names have been verified (Available online: www.indexfungorum.org, accessed on 3 July 2024). To date, only 13 species and three varieties of Strophaira have been reported from China: Stropharia aeruginosa (Curtis) Quél., Stropharia aeruginosa f. brunneola Hongo, Stropharia aeruginosa var. earthwormia T.X. Meng & Tolgor, Stropharia albonitens (Fr.) Quél., Stropharia chrysocystidia T.X. Meng & Tolgor, Stropharia halophila Pacioni, Stropharia hardii G.F. Atk., Stropharia hornemannii (Fr.) S. Lundell & Nannf., Stropharia jilinensis T. Bau & E. J. Tian, Stropharia lignicola E.J. Tian, Stropharia populicola L. Fan, S. Guo & H. Liu, Stropharia rugosoannulata, Stropharia rugosoannulata f. lutea Hongo, Stropharia scabella (Zeller) E.J. Tian & M. Gordon, Stropharia subsquamulosa Mitchel & A.H. Sm. and Stropharia yunnanensis W.F. Chiu (Bau and Meng 2008; Tian and Bau 2014; Zhao 2020; Liu et al. 2021; Tian et al. 2021).

Clitolyophyllum is a genus within the family Lyophyllaceae; it was discovered in 2016, a Turkish species fruiting on the dead bark of Picea orientalis. It is mainly characterised by fan-shaped, translucent-striate pileus; decurrent lamellae; lateral, cylindrical to flattened stipe; smooth, inamyloid spores; non-siderophilous basidia and irregular pileipellis (Sesli et al. 2016). Until now, it shows an apparently poor species diversity worldwide and currently contains only two species, of these, Clitolyophyllum akcaabatense Sesli, Vizzini & Contu is from Turkey and C. umbilicatum J.Z. Xu & Yu Li is from Gansu Province, China (Sesli et al. 2016; Xu et al. 2021).

In this study, two new species of Stropharia from China and a new record species of Clitolyophyllum from Jilin Province in China are described, based on both morphological and molecular data.

Materials and methods

Collection of specimens

All samples were collected during 2022–2023 from Shangping Village, Tianbaoyan National Nature Reserve, Yong’an City, Fujian Province and Red Pine King Scenic Area, Antu County, Yanbian Korean Autonomous Prefecture, Jilin Province, China. These were dried overnight by using an electric oven at 45 °C. The specimens were preserved in the Herbarium of Mycology of Jilin Agricultural Science and Technology University (HMJU).

Morphological observation

Photographs of fresh basidiocarps were taken with a Canon 80D camera. The colour name and code were recorded according to Kornerup and Wanscher (1978). The micromorphology of the specimens was studied at 40×, 100×, 400×, 600× and 1000× magnifications with the help of an Olympus BX 53 (Tokyo, Japan) optical microscope (measurements were carried out at 1000× oil immersion). Sections of dried specimens were fixed in 3% potassium hydroxide (KOH), 1% Congo red and Melzer’s reagent for observation. Dimensions for basidiospores are given using the notation of the form ‘(a–)b–av–c(–d)’. The range of ‘b–c’ contains a minimum of 90% of the measured values. Extreme values, ‘a’ and ‘d’, are given in parentheses, while ‘av’ is the average value. Factor Q is the ratio of spore length to width, Qm is the average of factor Q.

DNA extraction, PCR, sequencing and phylogenetic analyses

Total genomic DNA was extracted using an M5 Fungal Genomic DNA Kit (Mei5 Biotechnology Co., Ltd., Beijing, China) according to the manufacturers’ instructions. For polymerase chain reaction (PCR) amplification, primers ITS1 and ITS4 were used for the ITS region (White et al. 1990) and primer LR0R was paired with LR5 and LR7 to obtain the nrLSU sequences (Vilgalys and Hester 1990). The reactions were performed with the following procedure: initial denaturation at 94 °C for 5 min (ITS) or 4 min (nrLSU), 30 cycles at 94 °C for 30 s (ITS) or 40 s (nrLSU), 52 °C (nrLSU) or 53 °C (ITS) for 30 s or 45 s (nrLSU) and 72 °C for 30 s (ITS) or 40 sn(nrLSU) and, for terminal elongation, the reaction batches were incubated at 72 °C for 5 min. The PCR products were examined on 1% agarose gel, detected by JY 600 electrophoresis (Beijing JUNYI Electrophoresis Co., Ltd., Beijing, China) and then sent to BGI Co., Ltd. (Beijing, China) for sequencing.

Phylogenetic analyses

The obtained sequences were compared with the representative ITS sequences and nrLSU sequences retrieved from GenBank. Based on previous phylogenetic studies (Moncalvo et al. 2002; Matheny et al. 2006; Liu et al. 2021; Tian and Matheny 2021; Tian et al. 2021; Zhang et al. 2021, 2024; Wang et al. 2024), other species of Stropharia were also included, while Hypholoma australe (Murrill) Murrill and Hypholoma fasciculare (Huds.) P. Kumm were included as the outgroups. Sequences were aligned with MAFFT 7.0 (Katoh and Standley 2013) and edited with MEGA 7.0 (Kumar et al. 2016). The selection of the model was done by ModelFinder (Kalyaanamoorthy et al. 2017), based on the Bayesian Information Criterion (BIC). For this purpose, we chose the GTR+F+I+G4 model.

Following previous phylogenetic studies (Cai et al. 2020; Zhang et al. 2022; Qi et al. 2023), we designated Entoloma undatum (Gillet) M.M. Moser and Entoloma sericeum Quél., Mém. Soc. Émul, which are closely related to this genus, as the outgroup for phylogenetic analysis. The previously described methods were used to align and edit the sequences. At the same time, for BIC, we chose the GTR+F+I+G4 model.

Maximum Likelihood (ML) analysis and Bayesian Inference (BI) analysis were used to infer the phylogenetic position of the new species. Maximum Likelihood analysis estimation was performed by IQ-TREE (Nguyen et al. 2015). BI phylogeny using Markov Chain Monte Carlo (MCMC) methods was carried out with MrBayes 3.2.2 (Ronquist et al. 2012). The significance thresholds were set to > 0.90 for Bayesian posterior probability (PP) and > 70% for ML bootstrap proportions (BP). All sequences used in this study are listed in Table 1.

Table 1.
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Specimens used in molecular phylogenetic studies and their GenBank accession numbers.

Species Voucher GenBank accession number References
ITS nrLSU
Calocybe carnea CBS552.50 AF357028 AF223178 Hofstetter et al. (2002)
Calocybe chrysenteron AB10-09-142 KP192603 — Bellanger et al. (2015)
Calocybe coacta HMJU 269 OK649907 OL687156 Xu et al. (2021)
Calocybe convexa SYAU-FUNGI-007 KU528826 KU528830 Li et al. (2017)
Calocybe convexa SYAU-FUNGI-008 NR156303 NG058936 Li et al. (2017)
Calocybe gangraenosa Hae251.97 AF357032 AF223202 Li et al. (2017)
Calocybe ionides HC77/133 AF357029 AF223179 Li et al. (2017)
Calocybe naucoria PAM02081103 KP192543 — Bellanger et al. (2015)
Calocybe obscurissima FR2014101 KP192650 — Bellanger et al. (2015)
Calocybe pseudoflammula FR2014054 KP192579 — Bellanger et al. (2015)
Clitolyophyllum akcaabatense KATO Fungi 3184 KT934393 KT934394 Cai et al. (2020)
Clitolyophyllum umbilicatum HMJU 262 OK649905 OK649873 Xu et al. (2021)
Clitolyophyllum umbilicatum HMJU 1558 OK649906 OK649874 Xu et al. (2021)
Clitolyophyllum umbilicatum HMJU 5573 PP986998 PP987056 This study
Entoloma undatum TB7144 EF421108 AF261315 Mu et al. (2023)
Entoloma sericeum GLM 45918 — AY207197 Walther et al. (2005)
Gerhardtia citrinolobata JBSD 126508 KY363576 KY363578 Vizzini et al. (2017a)
Gerhardtia highlandensis PBM2806 (CUW) GU734744 EF535275 Cai et al. (2020)
Hypholoma australe PBM3481 HQ832446 HQ832456 Tian et al. (2021)
Hypholoma fasciculare TJB10226 HQ222023 HQ832457 Tian et al. (2021)
Hypsizygus ulmarius DUKE-JM/HW EF421105 AF042584 Cai et al. (2020)
Lyophyllum maleolens AB11-11-328 KP192607 — Bellanger et al. (2015)
Lyophyllum sykosporum IFO30978 AF357050 AF223208 Hofstetter et al. (2002)
Lyophyllum transforme GC08101108 KP192653 — Bellanger et al. (2015)
Myochromella boudieri BSI96/84 AF357047 DQ825430 Cai et al. (2020)
Myochromella inolens CBS330.85 AF357045 AF223201 Hofstetter et al. (2002)
Ossicaulis borealis SYAU-FUNGI-076 OP782047 OP782284 Qi et al. (2023)
Ossicaulis borealis SYAU-FUNGI-079 OP782050 OP782285 Qi et al. (2023)
Ossicaulis lignatilis D604 DQ825426 AF261397 Cai et al. (2020)
Ossicaulis yunnanensis IJ152 KY411962 KY411960 Yang et al. (2017)
Ossicaulis yunnanensis IH26 KY411961 KY411959 Yang et al. (2017)
Sagaranella gibberosa CBS328.50 AF357041 AF223197 Hofstetter et al. (2002)
Sagaranella tylicolor BSI92/245 AF357040 AF223195 Hofstetter et al. (2002)
Stropharia acanthostipitata JLCLD4-120329-01 MF882993 MF882995 Vizzini et al. (2017b)
Stropharia acanthostipitata JBSD127401 NR156637 NG060022 Vizzini et al. (2017b)
Stropharia aeruginosa HMJAU 4789 MW492533 MW492636 Tian et al. (2021)
Stropharia aeruginosa HMJAU 22865 MW492534 MW492637 Tian et al. (2021)
Stropharia albonitens FO46892 — AF291368 Wei et al. (2001)
Stropharia albonitens G0187 — MK278582 Varga et al. (2019)
Stropharia ambigua PBM 2257 AY818350 AY646102 Yang et al. (2005)
Stropharia atroferruginea HU32915 MK141060 MK434168 Khan et al. (2019)
Stropharia atroferruginea HU32916 MK141061 MK433557 Khan et al. (2019)
Stropharia caerulea BJTC FM225 MZ577604 — Liu et al. (2021)
Stropharia caerulea BJTC FM1177 MZ577597 — Liu et al. (2021)
Stropharia caerulea BJTC FM1449 MZ577571 — Liu et al. (2021)
Stropharia caerulea BJTC FM1512 MZ577579 — Liu et al. (2021)
Stropharia coronilla CBS 534.50 MH856747 MH868269 Vu et al. (2019)
Stropharia hardii TENN-F-071760 MW821365 MW821382 Tian et al. (2021)
Stropharia hardii SV S3 — AF261636 Moncalvo et al (2002)
Stropharia hardii SV S7 — AF261637 Moncalvo et al (2002)
Stropharia hornemannii TRTC156845 JN021094 — Dentinger et al. (2011)
Stropharia hornemannii TRTC150931 JN021093 — Dentinger et al. (2011)
Stropharia hornemannii TRTC150919 JN021092 — Dentinger et al. (2011)
Stropharia inuncta GLM46029 — AY207303 Walther et al. (2005)
Stropharia inuncta NL-5406 — MK278584 Varga et al. (2019)
Stropharia jilinensis HMJAU 22486 JF961347 — Tian and Bau (2014)
Stropharia lignicola T17(HMJAU 37429) MW492530 MW492633 Tian et al. (2021)
Stropharia lignicola Ti4(HMJAU 37510) MW492531 MW492634 Tian et al. (2021)
Stropharia mammillata CBS 535.50 MH856748 MH868270 Vu et al. (2019)
Stropharia melanosperma OMDL K OR945032 — Unpublished
Stropharia melanosperma S.D. Russell iNaturalist # 91080138 OM972388 — Unpublished
Stropharia microaeruginosa HMJU 12422 PP702369 PP702382 This study
Stropharia microaeruginosa HMJU 12635 PP715434 PP715435 This study
Stropharia populicola BJTC FM1483 MZ661117 MZ661121 Liu et al. (2021)
Stropharia populicola BJTC FM1480 MZ661094 MZ661118 Liu et al. (2021)
Stropharia populicola HSA361 MZ661093 MZ661119 Liu et al. (2021)
Stropharia rugosoannulata Z3(HMJAU46972) MW492535 MW492640 Tian et al. (2021)
Stropharia rugosoannulata HMJAU25602 MW492537 MW492639 Tian et al. (2021)
Stropharia rugosoannulata ACD0479 — OP235390 Unpublished
Stropharia subrugosoannulata HMJU 12439 PP702370 PP702383 This study
Stropharia subrugosoannulata HMJU 12441 PP702371 PP702384 This study
Tephrocybe confusa GC08110114 KP192633 — Bellanger et al. (2015)
Tephrocybella constrictospora TO HG3329 MF614962 MF614963 Hyde et al. (2017)
Tephrocybella griseonigrescens TO HG21112014 NR137975 KR476785 Crous et al. (2015)

Note: Newly generated sequences are in bold.

Results

Phylogenetic analyses

The combined dataset included 123 sequences, of which 113 were retrieved from GenBank. Both ML and BI methods produced the same tree topology, thus, only the ML tree is shown in Figs 1, 2. In both figures, Bayesian PP values (left) and MLBP values (right) are presented near each node. In the BLAST results, the S. subrugosoannulata sequences showed 92.84% similarity to S. hardii (OP679883) with 89% query coverage for ITS and 99.41% similarity to S. lignicola (NG079687), with 100% query coverage for nrLSU. The S. microaeruginosa sequences showed 96.88% similarity to S. aeruginosa (OR336166) with 97% query coverage for ITS and 99.69% similarity to S. aeruginosa (MK278581) with 94% query coverage for nrLSU; The C. umbilicatum sequences showed 99.38% similarity to C. umbilicatum (OK649905) for ITS.

Figure 1. 

ML and Bayesian phylogenetic analysis of Stropharia, based on ITS and nrLSU sequences. This study species is in bold.

Phylogenetic analyses indicate that the specimens from south-eastern China are in two separate clades with a high degree of support, which suggests that they represent two distinct new species. S. subrugosoannulata clusters with S. hardii and S. lignicola, implying they were phylogenetically closely related to each other. S. microaeruginosa, S. aeruginosa and S. albonitens appear to be the most closely related species (Fig. 1). According to the results of the phylogenetic analysis, the voucher HMJU 5573 was clustered with C. umbilicatum (BPP = 0.99, MLBP = 99) (Fig. 2).

Figure 2. 

ML and Bayesian phylogenetic analysis of Clitolyophyllum based on ITS and nrLSU sequences. This study species is in bold.

Taxonomy

Stropharia subrugosoannulata J.Z. Xu, sp. nov.

Fungal Names: FN 572029
Fig. 3

Diagnosis

Stropharia subrugosoannulata is distinguished from other species of the genus Stropharia by the pileus covered with greyish-orange squamules in the centre, stipe light brown and surface covered with white triangular squamules. Acanthocytes present in the basal mycelium of stipe. Chrysocystidia rare.

Figure 3. 

Stropharia subrugosoannulata (HMJU 12441, holotype) A habitat and basidiocarps B SEM images of basidiospores C basidia D cheilocystidia E pleurocystidia F basidiospores G acanthocytes H pileipellis. Scale bars: 5 cm (A); 5 µm (C, F); 10 µm (D, E, G, H).

Holotype

China, Fujian Province, Sanming City, Tianbaoyan Nature Reserve, Longwu Village, on soil, Phyllostachys pubescens, alt. 700 m, 21 October 2023, J.P. Liao (HMJU 12441, holotype).

Etymology

“sub” means “near”, named as it is similar to S. rugosoannulata.

Description

Pileus 25–60 mm diam., planoconcave or almost plane with or without being depressed in the centre, red copper to dull red (7C3–8B3), covered with greyish-orange (7B5) squamules in the centre, the margins with partial veil remnants. Lamellae adnate to adnexed, crowded, titian red to terra-cotta (7D6–7E7), with lamellulae in 1–3 tiers. Stipe 25–48 mm long and 6–10 mm wide, sometimes evanescent annulus in the upper part of the stipe, slightly broad with whitish rhizoids at the base. Surface longitudinally striate, light brown (6D6) and covered with white triangular squamules.

Basidiospores [30/4/3] (5.3) 5.8–6.3–6.8 (7.0) × (3.2) 3.4–3.7–4.0 (4.1) µm, Q = (1.50) 1.56–1.86 (1.91), Qm = 1.72, ellipsoid to subovate, obvious germ-pore, fawn to light fawn in KOH and Melzer’s reagent. Contains 1–2 guttulates. Basidia (10.6) 13.8–16.8–19.4 (19.9) × (4.1) 5.6–6.8–7.7 (8.7) µm. 2–4 spored, clavate, sterigmata up to 2.6 µm long, hyaline in KOH. Pleurocystidia (24.0) 26.3–30.5–36.9 (39.0) × (7.9) 8.3–10.1–12.8 (13.9) µm, clavate with or without umbo, hyaline in KOH, containing amorphous contents. Cheilocystidia (27.9) 29.1–33.2–37.1 (41.4) × (8.8) 9.0–10.7–13.0 (15.5) μm. Clavate, expanding at the tip, tapering downwards, sometimes curved. Chrysocystidia is rare. Lamellae trama regular, parallel to subparallel, 5.1–12.7 μm wide, hyaline in KOH. Pileipellis a cutis of parallel, hyphae 5.1–11.6 µm wide. Acanthocytes present in the basal mycelium of stipe. Clamp connections are present.

Habitat

Gregarious on the soil in the phyllostachys pubescens.

Known distribution

Known only from south-eastern China.

Additional material examined

Fujian Province, Sanming City, Tianbaoyan Nature Reserve, Longwu Village, on soil, Phyllostachys pubescens alt. 700 m, 21 October 2023, J.P. Liao (HMJU 12439).

Comments

The species is characterised mainly by the pileus covered with greyish-orange squamules in the centre, the margins with partial veil remnants, stipe light brown and surface covered with white triangular squamules, Sometimes evanescent annulus in the upper part of the stipe, chrysocystidia rare.

Stropharia microaeruginosa J.Z. Xu, sp. nov.

Fungal Names: FN 572030
Fig. 4

Diagnosis

Stropharia microaeruginosa pileus bluish-grey when young becoming lighter toward margins, later greyish-turquoise lightening towards the edges and surface radially striate when young, lamellae adnate to subdecurrent, stipe with white squamules at the base, acanthocytes absent making it unique amongst the Stropharia species.

Figure 4. 

Stropharia microaeruginosa (HMJU 12635, holotype). A habitat and basidiocarps B SEM images of basidiospores C basidia D basidiospores E pileipellis F pleurocystidia G cheilocystidia. Scale bars: 2 cm (A); 5 µm (C, D); 10 µm (E, F, G).

Holotype

China, Fujian Province, Sanming City, Tianbaoyan Nature Reserve,Shangping Village, scattered in the moss under mixed forests dominated by phyllostachys pubescens and coniferous forest, alt. 1100 m, 31 October 2023, J.P. Liao (HMJU 12635, holotype).

Etymology

“micro” means “small”, referring to the small basidiocarps and the margins often with partial veil remnants.

Description

Pileus 27–38 mm diam., centre of pileus bluish-grey (20F3) when young becoming lighter towards margins, later greyish-turquoise (24D4) lightens toward the edges, initial convex, the edge of the pileus upturned at maturity, smooth surface, viscid to glutinous, the margins often with partial veil remnants, submembranous, surface radially striate when young, gradually becomes less obvious as it matures. Lamellae adnate to subdecurrent, moderately crowded, grey (15C1), with lamellulae in 1–3 tiers. Stipe 51–75 mm long and 3.7–6.0 mm wide, concolorous with the pileus and lightening upwards, white squamules at the base, sometimes evanescent annulus in the upper part of the stipe. Further, slightly broad and with whitish rhizoids at the base.

Basidiospores [30/4/3] (5.4) 6.2–7.3–8.2 (8.8) × (3.7) 4.0–4.3–4.9 (5.0) µm, Q = (1.10) 1.42–1.99 (2.06), Qm = 1.69, elliptical, with an obvious germ-pore, light brown in KOH. Contains 1–2 guttulates. Basidia (16.4) 17.9–21.0–23.9 (27.0) × (5.2) 5.9–7.3–9.0 (9.9) µm, 2–4 spored, clavate, sterigmata up to 3.4 µm long, hyaline in KOH. Pleurocystidia (27.6) 33.5–39.9–46.3 (47.4) × (10.2) 11.1–13.6–16.0 (16.3) μm, clavate, with or without short mucronate apex, with an amorphous highly refractive content distributed in enlarged or raised areas. Cheilocystidia (29.8) 30.7–36.1–41.4 (45.6) × (7.9) 8.4–11.6–14.4 (16.1) μm. clavate, with homogenous content, mucronate at the apex, expanded apically, tapering downwards, sometimes curved. Chrysocystidia rare. Lamellae trama regular, subparallel, 6.7–14.3 µm wide, hyaline in KOH. Pileipellis a cutis of subparallel, slightly upturned, hyphae 2.7–5.5 µm wide. Clamp connections are present.

Habitat

Scattered in the moss under mixed forests dominated by phyllostachys pubescens and coniferous forest

Known distribution

Known only from south-eastern China.

Additional material examined

Fujian Province, Sanming City, Tianbaoyan Nature Reserve, Shangping Village, scattered in the moss under mixed forests dominated by phyllostachys pubescens and coniferous forest, alt. 1100 m, 31 October 2023, J.P. Liao (HMJU 12422).

Comments

This species is characterised mainly by the centre of pileus bluish-grey when young becoming lighter toward margins, later greyish-turquoise lightening towards the edges, the margins often with partial veil remnants, surface radially striate, stipe concolorous with the pileus and white squamules at the base, the spores with an obvious germ pore and chrysocystidia rare.

Clitolyophyllum umbilicatum J.Z. Xu & Yu Li, Journal of Fungi 7 (12, no. 1101): 9 (2021)

Fig. 5

Description

Basidiocarps omphalioid or clitocyboid. Pileus 30–50 mm in diam., deeply depressed, pale orange to greyish-brown (6A3-6D3), margin incurved with white appendages, slightly wavy with age. Lamellae decurrent, moderately crowded, thin, bluish-grey to grey (20D2-19E1), with numerous tiers of lamellulae, edges entire. Stipe 40–60 mm long and 5–8 mm wide, central, cylindrical or slightly compressed, equal or slightly tapering towards the apex, surface brownish-grey to dark brown (6E2-6F5), radially striate. Context thin, fleshy.

Figure 5. 

Basidiomes of Clitolyophyllum umbilicatum (HMJU 5573). Scale bars: 2 cm.

Basidiospores [30/4/3] (4.5) 4.6–6.3–8.2 (8.6) x (3.1) 3.4–4.3–5.3 (5.8) μm, Q = (1.17) 1.18–1.89 (2.10), Qm = 1.50, subglobose-ellipsoid, smooth, inamyloid, cyanophilic. Basidia (20.6) 22.6–25.6–28.4 (28.6) x 5.4–7.0–8.7 (8.8) μm, narrowly clavate or clavate, 2–4 spores, with siderophilous granulations. Hymenophoral trama regular, hyphae 2.5–16.7 μm wide. Hymenial cystidia not observed. Pileipellis a cutis of subparallel, dense, cylindrical hyphae, hyphae 2.6–16.5 μm wide, thin-walled, irregular. Stipitipellis made up of regularly parallel, hyphae 3.3–17.5 μm wide. Clamp connections present.

Habitat

Scattered on soil under mixed forests

Known distribution

The species is known to be distributed in China.

Specimens examined

China, Jilin Province, Yanbian Korean Autonomous Prefecture, Antu County, Red Pine King Scenic Spot, 31 July 2022, J.Z. Xu HMJU 5573.

Comments

This species was originally described from Gansu Province and is characterised by the omphalioid or clitocyboid habit, umbilicate pileus, central stipe, smooth, inamyloid spores and subregular pileipellis (Xu et al. 2021).

Discussion

Morphologically, S. rugosoannulata is the most similar species to S. subrugosoannulata in pileus margins with partial veil remnants, lamellae adnate, stipe equal or slightly tapered upwards and with annulus, whitish rhizoids at the base. The difference between S. subrugosoannulata and S. rugosoannulata is that the S. rugosoannulata has a larger pileus (50–150 mm), smooth, lamellae are white when young, turning dark brown or almost black with age and larger basidiospores (Murrill 1922). S. scabella showed similarities with S. subrugosoannulata in lamellae adnate and light yellow pileus, but S. scabella hemispherical to convex pileus, annulus obvious, inconspicuous germ-pore (Tian and Matheny 2021). S. jilinensis bears resemblance to S. subrugosoannulata due to the pileus covered with yellowish-brown squamules, the margins with partial veil remnants, but S. jilinensis has grey violet to yellowish-brown pileus, white stipe (Tian and Bau 2014). Phylogenetically, S. subrugosoannulata is closely related to S. hardii (Atkinson 1906) and S. lignicola (Tian et al. 2021) (Fig. 1). S. hardii differs from S. subrugosoannulata in that it does not have acanthocytes, spores purple-brown, the spores without an obvious germ pore (Atkinson 1906). S. lignicola also can be easily distinguished from S. subrugosoannulata by the pileus grey-yellow, incurved margin and stipe surface covered with recurved yellowish squamules towards the base (Tian et al. 2021).

S. microaeruginosa is very similar to S. aeruginosa in morphology; however, when compared that to the new species, S. aeruginosa basidiomata medium to large, annulus evident, acanthocytes present in the basal mycelium of stipe, the spores without an obvious germ pore (Zhao 2020). S. populicola bears resemblance to S. microaeruginosa due to pileus margins with partial veil remnants, lamellae adnate, sometimes evanescent annulus of the stipe, but S. populicola pileus non-sticky, pleurocystidia rare, acanthocytes present on the basal mycelium at stipe (Liu et al. 2021). S. microaeruginosa is similar to Stropharia venusta P.S. Silva, Cortez & R.M. Silveira in pileus viscid and the margins often with partial veil remnants, stipe with squamules, gill trama regular, but S. venusta pileus reddish-brown, lamellae adnexed to sinuate, acanthocytes present abundantly on rhizomorphs’ surface, cheilochrysocystidia absent (Da Silva et al. 2009). Phylogenetic analysis indicate that S. microaeruginosa is sister to S. aeruginosa and S. albonitens (Fig. 1); S. albonitens also can be distinguished from S. microaeruginosa by the basidiospores purple-brown, the spores without an obvious germ pore (Karsten 1879).

The specimen from Jilin Province shares the following characteristics with C. umbilicatum (Xu et al. 2021) in the original description: Basidiocarps omphalioid or clitocyboid. Pileus deeply depressed, margin slightly wavy with age. Lamellae decurrent, moderately crowded, thin, with numerous tiers of lamellulae, edges entire. Basidiospores subglobose-ellipsoid, smooth, inamyloid, cyanophilic. Basidia, narrowly clavate or clavate, with siderophilous granulations. Hymenial cystidia not observed. Clamp connections present. However, in the original description of C. umbilicatum, pileus surface smooth with radially striate, slightly hygrophanous. Phylogenetic analyses show that C. umbilicatum and C. akcaabatense are closely related (Fig. 2), but C. akcaabatense differs in that the lamellae at first whitish then light cream or beige, Stipe eccentric, Caulocystidia present (Sesli et al. 2016). Therefore, combining morphological and microscopic features, the specimen from Jilin was C. umbilicatum.

Until now, a total of 15 species and three varieties of Strophaira have been reported from China. On the basis of observations and literature (Bau and Meng 2008; Meng 2008; Tian and Bau 2014; Zhao 2020; Liu et al. 2021; Tian et al. 2021), a key for the Strophaira species from China is provided.

Key to the species of Stropharia known from China

1 Pileus dry or slightly viscid when wet 2
– Pileus viscid to glutinous 6
2 Basidiospores subhexagonal in side view 3
– Basidiospores non-subhexagonal in side view 5
3 Pileus dark red to reddish-brown S. rugosoannulata
– Pileus yellowish-brown to pale yellow to yellowish-white 4
4 Cheilocystidia or pleurocystidia as chrysocystidia, on enriched soil 13
– Cheilocystidia as leptocystidia, rarely chrysocystidia, on saline-alkali or barren soil S. halophila
5 basidiospores with a conspicuous germ pore 14
– basidiospores with an inconspicuous germ pore 17
6 Hymenial acanthocytes present S. lignicola
– Hymenial acanthocytes absent 7
7 Pileus without green tone 8
– Pileus with green tone 10
8 Pileus brown or pale brown 9
– Pileus dark brown or orange-yellow 13
9 Basidiospores without a germ pore, black brown in KOH S. subsquamulosa
– Basidiospores with a germ pore, slightly dark brown in KOH S. albonitens
10 Cheilocystidia as leptocystidia 11
– Cheilocystidia as chrysocystidia S. chrysocystidia
11 Cheilocystidia clavate with a dull to capitate apex 12
– Cheilocystidia flexuously cylindrical with a branched apex S. aeruginosa var. earthwormia
12 Pileus fading brown or clay colour in age S. aeruginosa f. brunneola
– Pileus greyish-green with yellowish margin in age 15
13 Lamellae greyish-purple or purple grey brown 18
– Lamellae pale grey to pale cinnamon S. rugosoannulata f.lutea
14 Basidiospores black purple brown S. yunnanensis
– Basidiospores fawn to dark yellow 16
15 Cystidia as chrysocystidia S. aeruginosa
– Chrysocystidia rare S. microaeruginosa
16 Lamellae titian red to terra-cotta S. subrugosoannulata
– Lamellae purple grey to pale cinnamon S. hornemannii
17 Cheilocystidia as chrysocystidia and pleurocystidia from one show larger hollow pattern S. scabella
– Cheilocystidia with branch or spherical chain of cells arranged S. jilinensis
18 Pleurocystidia rare S. populicola
– Pleurocystidia as chrysocystidia S. hardii

Acknowledgements

We are very thankful to Mr. Samantha C. Karunarathna (College of Biological Resource and Food Engineering, Qujing Normal University) for their kind help during paper revision.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This research was funded by The Science and Technology Department of Jilin Province (20240602031RC).

Author contributions

Di Zhang: conceptualisation, experiment, software, writing—original draft preparation, morphological analysis. Jun-Jie Peng:morphological analysis, software. Jia-Jun Wang: experiment. A.K. Hasith Priyashnatha: writing—review and editing. Jin-Peng Liao and Hua-Xing Luo: sample collection. Shi-Chen Huang: writing—review and editing. Ji-Ze Xu: formal analysis, constructive discussions. All authors have read and agreed to the published version of the manuscript.

Author ORCIDs

Shi-Chen Huang https://orcid.org/0000-0001-5736-142X

Ji-Ze Xu https://orcid.org/0000-0003-2082-8529

Data availability

All of the data that support the findings of this study are available in the main text.

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