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Research Article
Emending Gymnopus sect. Gymnopus (Agaricales, Omphalotaceae) by including two new species from southern China
expand article infoJi-Peng Li‡§, Vladimír Antonín|, Genevieve Gates, Lu Jiang#, Tai-Hui Li‡, Yu Li§, Bin Song‡, Chun-Ying Deng¤
‡ Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou, China
§ Jilin Agricultural University, Changchun, China
| Moravian Museum, Brno, Czech Republic
¶ Tasmanian Institute of Agriculture, Hobart, Australia
# Shenzhen Wildlife Conservation Division, Shenzhen, China
¤ Guizhou institute of biology, Guizhou Academy of Sciences, Guiyang, China

Corresponding author: Tai-Hui Li ( mycolab@263.net )

Corresponding author: Yu Li ( yuli966@126.com )

Academic editor: R. Henrik Nilsson
© 2022 Ji-Peng Li, Vladimír Antonín, Genevieve Gates, Lu Jiang, Tai-Hui Li, Yu Li, Bin Song, Chun-Ying Deng.
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: Li J-P, Antonín V, Gates G, Jiang L, Li T-H, Li Y, Song B, Deng C-Y (2022) Emending Gymnopus sect. Gymnopus (Agaricales, Omphalotaceae) by including two new species from southern China. MycoKeys 87: 183-204. https://doi.org/10.3897/mycokeys.87.76125
Open Access

Abstract

Based on phylogenetic analyses, some newly studied Chinese mushroom specimens were found to represent two distinct species within the genus Gymnopus. Along with G. fusipes (sect. Gymnopus) they form a distinct clade with high support, although their macromorphological characters seem to be closer to members of Gymnopus sect. Levipedes or sect. Vestipedes (Collybiopsis). When examined in detail, their micromorphological characters, especially the type of pileipellis, support them as new members of G. sect. Gymnopus. Therefore, two new species, G. omphalinoides and G. schizophyllus, and the emended circumscription of sect. Gymnopus are proposed in this paper. Detailed morphological descriptions, colour photos, illustrations of the two new species, morphological comparisons with similar taxa and the molecular-phylogenetic analyses of the combined nrITS and nrLSU data are presented. A key to the known species of G. sect. Gymnopus is also presented.

Keywords

Morphology, new taxa, phylogeny, taxonomy

Introduction

Gymnopus (Pers.) Roussel sect. Gymnopus is a monotypic section and its type species, Gymnopus fusipes (Bull.) Gray, also typifies the genus (Antonín and Noordeloos 2010). The sectional name, therefore, was proposed automatically. Formerly, G. fusipes was placed in Collybia (Fr.) Staude sect. Striipedes (Fr.) Quél. as C. fusipes (Bull.) Quél. (Singer 1986). Based on morphology, several species, in fact, several sections, were moved from Collybia to Gymnopus, a genus that was defined mainly based on American and European material (Antonín et al. 1997). Since then, the character of the pileipellis, especially the terminal cells, has become a significant factor in the delimitation of the sections within the genus. After undergoing a series of revisions, Gymnopus sensu lato (s.l.) was restricted as a monophyletic genus (Gymnopus sensu stricto (s. str.)) that comprised four sections. The other three sections are G. sect. Androsacei (Kühner) Antonín & Noordel, sect. Impudicae (Antonín & Noordel.) Antonín & Noordel. and sect. Levipedes (Quél.) Halling (Oliveira et al. 2019).

Morphologically, the current circumscription of G. sect. Gymnopus was adopted from Clémençon (1981) as Collybia sect. Striipedes. As a monotypic section, its circumscription is dominated by its type species which is characterised by a fleshy pileus, fusoid stipe with a distinct pseudorrhiza and a pileipellis made up of inflated, irregular, often coralloid elements, similar to the Dryophila-type structure (Antonín and Noordeloos 2010; Oliveira et al. 2019). It stands in stark contrast to other sections. Many studies published in recent years with an emphasis on Gymnopus reported or described species from the other sections, and discussions relating to the type species or G. sect. Gymnopus were hardly addressed. Wilson and Desjardin (2005) and Mata et al. (2007) noted that G. fusipes and members of G. sect. Levipedes share a similar pileipellis and that the type species of the genus mainly differs in the stipe with a pseudorrhiza. Besides, only Collybia subsulcatipes A.H. Sm. was considered a probable member of G. sect. Gymnopus based on morphology (Antonín and Noordeloos 1997, as Collybia sulcatipes A.H. Smith). It is characterised by a smooth or longitudinally grooved to subsulcate stipe with a long pseudorrhiza (Smith 1944). Nevertheless, whether this species belongs to this section is difficult to confirm because of the lack of molecular data.

Phylogenetically, Mata et al. (2004) reported on the phylogenetic position of G. fusipes and showed that it forms a distinct clade that is closely related to Setulipes androsaceus (L.) Antonín and always among other clades dominated by Gymnopus taxa. Wilson and Desjardin (2005) also produced a similar phylogenetic result. As the species typified the genus, these results had repercussions on the generic relationships. Hence, S. androsaceus was transferred to Gymnopus (Mata et al. 2004) and was designated as the type species of G. sect. Androsacei (Noordeloos and Antonín 2008). Subsequently, Oliveira et al. (2019) used a multi-gene phylogenetic analysis to restrict the concept of genus Gymnopus and to further confirm that G. sect. Androsacei is the closest group to G. sect. Gymnopus. However, there was no update on the phylogenetic nature of G. sect. Gymnopus due to the lack of new material.

In this study, two new species of G. sect. Gymnopus are described based on morphology and phylogenetic analysis. Detailed morphological descriptions, colour photos, illustrations of the species, morphological comparisons with similar taxa and molecular-phylogenetic analyses of combined nuclear ribosomal internal transcribed spacer (nrITS) and nuclear ribosomal large subunit (nrLSU) data are presented. An emended circumscription and a key to the species of G. sect. Gymnopus are provided.

Material and methods

Abbreviations

For Latin names: G. = Gymnopus; Ma. = Marasmius; Mi. = Micromphale; My. = Mycetinis; P. = Paragymnopus.

For phylogenetic analysis: ML = Maximum Likelihood; BI = Bayesian Inference; BP = Bootstrap Proportions; PP = Posterior Probability.

For collection locality: FNNR = Fanjingshan National Nature Reserve; MC = Maguan County; MR = Meizihu Reservoir; TFP = Tianluhu Forest Park; WSA = Wutongshan Scenic Area; YNNR = Yunkaishan National Nature Reserve.

For climate: AAT = average annual temperature; AAR = average annual rainfall; MST = major soil type; MMMM = mid-subtropical mountain moist monsoon; SEM = subtropical eastern monsoon; SM = subtropical monsoon; SSM = south subtropical monsoon; SSO = south subtropical oceanic.

For soil type: B = brown; DBS = dark brown soil; La = laterite; LRS = lateritic red soil; MSMS = mountain shrub meadow soils; MRS = mountain red soil; RS = red soil; YBS = yellow brown soil; YS = yellow soil.

Specimen collection and drying treatment

Nine collections from China were examined in this study: one came from the Guizhou Province (Tongren City), three collections from the Yunnan Province (one from Pu’er City and two from Maguan County) and five collections from the Guangdong Province (one from Guangzhou City, one from Shenzhen City and three from Xinyi City). The exact localities and their environmental characteristics are shown in Table 1. The fresh basidiomata of each collection were wrapped in separate mesh bags and dried in an electric drier operated below 50 °C. Dried collections were deposited in the Fungarium of Guangdong Institute of Microbiology, China (GDGM), Fungarium of the Herbarium of Kunming Institute of Botany, Chinese Academy of Sciences (KUN-HKAS) or Herbarium Mycology of Jilin Agricultural Science and Technology University (HMJU). The herbarium abbreviations follow Thiers (2021).

Table 1.
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The environmental characteristics of localities for each collection.

Locality Climate Average annual temperature Average annual rainfall Major soil type References
FNNR MMMM 16.9 °C 1351 mm YS Xiao et al. 1998; Zhong et al. 2011
MC SEM 16.9 °C 1345 mm La, LRS, RS, YS, YBS, BS, DBS Zhao 2007
MR SM 17.8 °C 1514.6 mm La, LRS, RS Tao 2002, 2006
TFP SSM 22 °C 1725 mm LRS Huang and Li 2006; Kong et al. 2013
WSA SSO 22.4 °C 1948.4 mm LRS, RS, MSMS Xv et al. 2009; Zhou et al. 2011
YNNR SSM 18 °C 2300–2600 mm LRS, MRS, YS Huang (1998); Li et al. 2021b

Morphological studies

Fresh basidiomata were photographed and used for macromorphological descriptions. The colours are coded from Kornerup and Wanscher (1978). The ecology of the specimens is presented below. Lamellae were counted where ‘L’ refers to the number of full-length lamellae and ‘l’ refers to the number of lamellulae tiers.

Micromorphological structures were observed via a ZEISS Axio Lab. A1 microscope based on the hand-made sections of dried basidiomata mounted in 5 % KOH on a glass slide. When necessary, Congo Red solution was used as a stain and Melzer’s reagent was used to test amyloid or dextrinoid reactions. For the various microscopic structures, ‘n’ refers to the number of measured elements. For basidiospores, ‘E’ represents the quotient of length and width in any one spore, and ‘Q’ represents the mean of E values. Basidiospore measurements do not include apiculus and are presented as ‘(a)b–c(d)’, where ‘b–c’ represents the minimum of 90 % of the measured values and ‘a’ and ‘d’ represent the extreme values. The main body (sterigmata or excrescences not included) of basidia, basidioles, pleurocystidia and cheilocystidia were measured (if present).

DNA extraction, amplification and sequencing

Genomic DNA was extracted from dried tissue via a Magen HiPure Fungal DNA Kit (Magen Biotech Co., Ltd., Guangzhou) Fungal DNA Kit as in Li et al. (2021a). The nrITS (the nuclear ribosomal internal transcribed spacer) region and the nrLSU (nuclear ribosomal large subunit) gene were amplified by the polymerase chain reaction (PCR) technique using the primers ITS5 and ITS4 (nrITS; White et al. 1990), and LR0R and LR5 (nrLSU; Vilgalys and Hester 1990; Cubeta et al. 1991), respectively. A common PCR programme was used for amplification of both markers and is given below: 4 min at 95 °C; 35 cycles of 45 s at 95 °C, 45 s at 53 °C, 60 s at 72 °C; 10 min at 72 °C. Amplified products were used for Sanger dideoxy sequencing performed by Beijing Genomics Institute (BGI). The newly generated sequences were assembled from two overlapping reads and trimmed via BioEdit v.7.0.9 (Hall 2011). Before depositing in GenBank (Sayers et al. 2021; Table 2), quality control was done following the methods in Nilsson et al. (2012).

Table 2.
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Information on DNA sequences used in the phylogenetic analyses. Newly generated sequences are highlighted in bold and type specimen is marked with an asterisk (*).

Taxon name ITS LSU Collection No. Locality Reference
Agaricales sp. AB859204 AB859204 Sw2-1 Japan GenBank
G. adventitius nom. prov. KY026760 KY026760 SFSU:DED8813 Not given Petersen and Hughes (2016)
G. alliifoetidissimus MT023348 MT017526 GDGM 76695 China Li et al. (2021a)
G. androsaceus KY026750 KY026750 CULTENN5609 USA Petersen and Hughes (2016)
G. androsaceus MH857175 MH868714 CBS 240.53 France Vu et al. 2019
G. androsaceus MH857174 MH868713 CBS 239.53 France Vu et al. 2019
G. androsaceus KY026748 KY026748 CULTENN5021h2 Canada Petersen and Hughes (2016)
G. androsaceus KY026663 KY026663 TENN:F-59594 Russia Petersen and Hughes (2016)
G. atlanticus KT222654 KY302698 URM 87728 Brazil Coimbra et al. (2015)
G. aurantiipes AY263432 AY639410 SFSU:AWW118 Indonesia Wilson et al. (2004)
G. brunneiniger MT232388 MW187069 XAL: Cesar50 Mexico César et al. (2020)
G. brunneodiscus MH589973 MH589988 BRNM 714974 South Korea Ryoo et al. (2020)
G. cremeostipitatus KF251071 KF251091 BRNM 747547 South Korea Antonín et al. (2014)
G. densilamellatus KP336685 KP336694 BRNM 714927 South Korea Ryoo et al. (2016)
G. dryophiloides MH589967 MH589985 BRNM 781447 South Korea Ryoo et al. (2020)
G. dryophilus DQ241781 AY640619 TENN:F-57012 Not given Matheny et al. (2006)
G. dysodes KY026666 FJ750265 TENN:F-61125 USA Hughes and Petersen (2016)
G. foetidus KY026739 KY026739 TENN:F-69323 USA Hughes and Petersen (2016)
G. frigidomarginatus nom. prov. KY026648 KY026648 TENN:F-55679 USA Hughes and Petersen (2016)
G. fusipes AY256711 AY256711 TENN:F-59300 Austria Mata et al. (2004)
G. fusipes KY026727 KY026727 TENN:F-69254 Slovakia Hughes and Petersen (2016)
G. fusipes AY256710 AY256710 TENN:F-59217 France Mata et al. (2004)
G. impudicus LT594119 LT594119 BRNM 714849 Czech Republic Ryoo et al. (2016)
G. inflatotrama nom. prov. KY026619 KY026619 TENN:F-48143 USA Hughes and Petersen (2016)
G. inflatotrama nom. prov. KY026744 KY026744 TFB 4529 USA Hughes and Petersen (2016)
G. inflatotrama nom. prov. KY026640 KY026640 TENN:F-53490 USA Hughes and Petersen (2016)
G. inflatotrama nom. prov. KY026632 KY026632 TENN:F-51233 USA Hughes and Petersen (2016)
G. inusitatus JN247553 JN247557 BCN:SCM B-4058 Spain Antonín et al. (2012)
G. iocephalus DQ449984 KY019630 TENN:F-52970 USA Mata et al. (2007)
G. irresolutus MF100973 Unavailable SFSU:DED 8209 São Tomé Desjardin and Perry (2017)
G. montagnei DQ449988 AF261327 JMCR 143 Not given Mata et al. (2007)
G. neobrevipes MH673477 MH673477 TENN:F-14505 USA Petersen and Hughes (2019)
G. novae-angliae nom. prov. KY026745 KY026745 CULTENN4975 USA Hughes and Petersen (2016)
G. novomundi nom. prov. KY026759 KY026759 SFSU-DED5097 USA Hughes and Petersen (2016)
G. ocior KY026678 KY026678 TENN:F-65135 Belgium Hughes and Petersen (2016)
G. omphalinoides sp. nov. MW134044 MW134730 *GDGM 78318 China This study
G. omphalinoides sp. nov. MW134047 MW134733 HMJU 00506 China This study
G. omphalinoides sp. nov. MW134040 MW134726 GDGM 44411 China This study
G. omphalinoides sp. nov. MW134045 MW134731 GDGM 78483 China This study
G. omphalinoides sp. nov. OK087326 Unavailable KUN-HKAS 107312 China This study
G. pallipes MW582856 OK087327 GDGM 81513 China Li et al. (2021b) and this study
G. portoricensis KY026627 KY026627 TENN:F-50999 Puerto Rico Hughes and Petersen (2016)
G. schizophyllus sp. nov. MW134041 MW134727 GDGM 76287 China This study
G. schizophyllus sp. nov. MW134042 MW134728 GDGM 77038 China This study
G. schizophyllus sp. nov. MW134043 MW134729 *GDGM 77165 China This study
G. schizophyllus sp. nov. MW134046 MW134732 KUN-HKAS 96494 China This study
G. similis KP336690 KP336697 BRNM 714981 South Korea Ryoo et al. (2016)
G. spongiosus KY026686 KY026686 TENN:F-65912 USA Hughes and Petersen (2016)
G. subsupinus KM975399 KM975375 PDD:96595 New Zealand GenBank
G. talisiae KT222655 KX958401 URM 87730 Brazil Coimbra et al. (2015)
Ma. androsaceus JN943605 JN941145 Sara Landvik:NN008037 Sweden Antonín et al. (2014)
Ma. androsaceus AF519893 AF519891 MUCL35155 Not given Klonowska et al. (2013)
Ma. otagensis MT974597 MT974601 PDD:106823 New Zealand GenBank
Ma. otagensis MT974600 MT974602 PDD:113265 New Zealand GenBank
Mi. foetidum KP877447 Unavailable NEHU.MBSRJ.48 India Borthakur and Joshi (2016)
My. alliaceus KY696752 KY696752 TENN:F-55630 Russia Petersen and Hughes (2017)
My. scorodonius KY696748 KY696748 TENN:F-53474 USA Petersen and Hughes (2017)
Pa. perforans KY026625 KY026625 TENN:F-50319 Sweden Petersen and Hughes (2017)

Phylogenetic analyses

Representative species and their sequences were selected to cover all sections of Gymnopus s. str. based on recent publications (Mata et al. 2004; Petersen and Hughes 2016; Oliveira et al. 2019; César et al. 2020). In addition, four sequences annotated as Marasmius otagensis were added to the matrix following an unpublished phylogenetic tree provided by Dr Jerry Cooper (Landcare Research, New Zealand). Two species of Mycetinis Earle were selected as the outgroup according to the phylogenetic results of Oliveira et al. (2019), Li et al. (2021a) and Li et al. (2021b). Our two-marker dataset, composed of ITS1-5.8S-ITS2-LSU sequences, was partitioned and used for the phylogenetic analyses. The samples NEHU MBSRJ48, HAKS 107312 and SFSU:DED 8209 have only ITS sequences available, and their LSU data were treated as missing data in the dataset. Information on sequences used in the phylogenetic analysis of this study is shown in Table 2. Sequences of each marker (nrITS and nrLSU) were aligned using MAFFT v.7.313 (Katoh and Standley 2013), applying the L-INS-I strategy, and manually concatenated and adjusted in BioEdit v.7.0.9 (Hall 2011). The combined dataset comprised four partitions (ITS1, the 5.8S gene, ITS2 and the LSU gene) and was analysed in the Maximum Likelihood (ML) and Bayesian Inference (BI) methods. The ML analysis was performed in RAxML v.8.2.10 (Stamatakis 2014), and the BI analysis was performed in MrBayes v.3.2.6 (Ronquist et al. 2012). The optimal substitution model for BI analysis was chosen by Modelfinder (Kalyaanamoorthy et al. 2017) using the Bayesian Information Criterion (BIC). The ML analysis was conducted using the GTRGAMMA substitution model, applying rapid bootstrap algorithm, with 5000 replicates. The BI analysis was implemented using two runs with four chains each for ten million generations sampling every hundredth generation. The average standard deviation of split frequencies was examined to make sure that the value was below 0.01. After discarding the first 25 % of trees as burn-in, a 50% majority rule consensus tree was generated from the remaining trees. Convergence of the MCMC chains was visualised in Tracer v. 1.7.1 (Rambaut et al. 2018) and examined manually. The tree files were viewed and edited in FigTree v1.4.3 (Rambaut 2009). The multiple sequence alignment and the ML and BI tree files were deposited in TreeBASE as Study ID 28774 (https://www.treebase.org).

Results

Phylogenetic results

A BLAST search of nrITS sequences revealed that a sequence annotated as “Micromphale foetidum” (KP877447) was the most similar (7–8 different sites or more than 98.16% similarity) to the two new species described in this study.

The combined dataset comprised 113 sequences including 58 nrITS and 55 nrLSU. The alignment is 1,716 bases long, of which 1,263 are constant sites, 139 are variable and parsimony-uninformative sites and 314 (18 %) are parsimony-informative sites. The best-fit model for each partition applied in the BI analysis was HKY+F+I+G4 (for the nrITS1, nrITS2 and nrLSU markers) and K2P (for the nr5.8S gene). ML and BI analyses produced nearly identical topologies and only the ML phylogram is presented (Fig. 1). The ML-BP and BI-PP support values are shown above and below the branches, respectively.

Figure 1. 

Phylogram generated by ML analysis of the combined dataset (ITS1-5.8S-ITS2-LSU region). ML-BP ≥ 70 % and BI-PP ≥ 0.95 are shown above and below the branches, respectively.

In the generated phylogenetic tree (Fig. 1), Gymnopus s. str. formed a strongly supported clade (BI-PP/ML-BP = 1.00/100 %). Inside this clade, four samples from China (GDGM 76287, 77038, 77165 and KUN-HKAS 96494) of one morphospecies and five samples from China (GDGM 44411, 78318, 78483, KUN-HKAS 107312 and HMJU 00506) of the other morphospecies grouped in two different lineages implying two distinct species within Gymnopus s. str. The nine samples from China along with a sample from India (NEHU MBSRJ48) formed a single clade with high support (BI-PP/ML-BP = 1.0/88 %). This clade and two samples from New Zealand (PDD: 106823, 113265) grouped in one clade as sister to G. fusipes (G. sect. Gymnopus). Furthermore, they formed a distinct group as a monophyletic clade with high support (BI-PP/ML-BP = 1.00/98 %).

Taxonomy

Gymnopus omphalinoides J.P. Li, T.H. Li & Y. Li, sp. nov.

MycoBank No: 837641
Figs 2, 3

Typification

China, Guangdong Province, Shenzhen City, Wutongshan Scenic Area, 16 September 2019, H. Huang, L.Q. Wu & N. Zhan (GDGM 78318, holotype!).

Etymology

The epithet ‘omphalinoides’ (Lat.) refers to the omphalinoid or Omphalina-like basidiomata of the new species.

Diagnosis

Differs from G. volkertii Murrill in its striate or grooved pileus and smaller basidiospores (4.0–5.5 × 2.5–3 μm). Basidiomata mainly gregarious on decayed wood in broadleaf forest; pileus disc reddish orange to dark brown becoming paler with age; lamellae broad, adnate and ventricose; stipe glabrous.

Description

Basidiomata omphalinoid, collybioid or gymnopoid. Pileus 10–40 mm broad, membranous, hemispheric when young, becoming convex, plano-convex to applanate, generally umbilicate to sometimes slightly depressed at the centre, inflexed then straight or reflexed at margin, with a marginal zone often undulating with age, glabrous, radially striate or grooved towards the margin, orange (6B7) or reddish orange (7B7) to brown (7D8) overall when young, somewhat reddish orange (7B7) or dark brown (7F8), then paler towards the margin, white or pale orange (6A3) to light brown (6D4), often greyish orange (6B4) to dark brown (6F8) at the disc. Lamellae adnate, broad, ventricose to broadly ventricose, white when fresh, sometimes with greyish red (7B4) to brown (7E7) tint somewhere, margin entire to split and sometimes grooved, L = 12–17, l = 3–5. Stipe 10–30 mm long, 2–4 mm thick in the middle, central, cylindrical, or compressed, with dense basal mycelium when young that disappears when old, hollow, fibrous, glabrous, slightly longitudinally striate when old, rooting deep in the substrate, but eventually attaches to the stump, dull white to greyish red (7B4) when young, soon darker towards the base, white to reddish orange (7A7) at apex, finally entirely dark brown (7F8). Odour not distinctive.

Figure 2. 

Basidiomata of Gymnopus omphalinoides a GDGM 78483 b GDGM 78318 holotype! (with magnifying slightly longitudinally striate stipe) c KUN-HKAS 107312 d, e GDGM 44411 f HMJU 00506. a photographed by M. Zhang b photographed by L.Q. Wu, c photographed by X.H. Wang d, e photographed by J.P. Li f photographed by J.Z. Xu. For a detailed display, the slightly longitudinally striate stipe is magnified in b, and the split lamellar edge is magnified in e, f. Scale bars: 1 cm.

Figure 3. 

Microscopic features of Gymnopus omphalinoides (GDGM 78318, holotype!) a Basidiospores b Basidia c Basidioles d Cheilocystidia e Stipitipellis f terminal elements of the pileipellis. Drawing by J.P. Li. Sale bars: 10 μm (a–d), 20 μm (e, f).

Basidiospores [n=80] (3.5–) 4.0–5.5 (–6.0) × 2.5–3 (–3.5) μm (average= 4.63 × 2.93 μm, E = 1.33–1.83 (–2), Q=1.58), obovoid, ellipsoid to subellipsoid, sometimes amygdaliform. Basidia [n=20] 17–31 × 3–5 μm, clavate, 4-spored. Basidioles [n=20] 17–32 × 4–5.5 μm, clavate, cylindrical. Lamellar edge sterile. Cheilocystidia [n=20] 17–32 × 4–10 μm, irregularly clavate, sphaeropedunculate or almost so, with tendency to be inflated, with or without finger-like apical projection(s) or more or less diverticulate elements. Pileipellis a cutis composed of cylindrical, thin-walled hyphae, up to 12.5 μm wide, smooth or with scattered diverticula, hyaline to slightly brownish; Rameales-like structures present, rare to abundant; terminal cells short, broad, mostly inflated, vesiculose or pyriform to cystidioid (clavate), obtuse and sometimes diverticulate, mixed with a few irregularly branched, slightly coralloid elements and some resembling Dryophila-type structures. Stipitipellis a cutis composed of cylindrical, slightly thick to thick-walled, smooth, non-dextrinoid, parallelly arranged hyphae, up to 12 μm wide, with or without Rameales-like structure. Caulocystidia absent. Clamp connections present.

Ecology

Saprotrophic, gregarious or in small clusters, usually rooting around the roots and stumps in broadleaf forests.

Additional specimens examined

China, Guangdong Province, Guangzhou City, Tianluhu Forest Park, longitude and latitude not recorded, alt. not recorded, 4 April 2019, T.H. Li, W.Q. Deng, J.Y. Xu & J.P. Li (GDGM 44411); Guizhou Province, Tongren City, Fanjingshan National Nature Reserve, 27°48'33"N, 108°44'45"E, alt. 640 m, 14 July 2019, J.Z. Xu (HMJU 00506); Yunnan Province, Pu’er City, Meizihu Reservoir, 22°45'0"N, 100°58'48"E, alt. 1300 m, 19 September 2019, M. Zhang, T. Li & J.Y. Xu (GDGM 78483); Yunnan Province, Maguan County, Nanlao Village, 23°03'21"N, 104°31'12"E, alt. 1190 m, 5 August 2017, X.H. Wang (KUN-HKAS 107312).

Remarks

Gymnopus omphalinoides is a very distinct species due to its generally omphalinoid basidiomata, by a membranous and striate or grooved, reddish brown to brown pileus that becomes paler with age, by the broad, adnate, ventricose lamellae that are sometimes split to grooved at the edge, and by a pileipellis often with scattered cystidioid (clavate) or vesiculose to pyriform terminal elements. Collection GDGM 78318 is characterised by having cheilocystidia with more or less finger-like apical projection(s) and by a pileipellis with scattered Rameales-like structures, but the collection GDGM 44411 differs in its cheilocystidia with diverticulate elements and pileipellis with more Rameales-like structures.

Among the known species of Gymnopus with a striate or grooved pileus and ventricose lamellae, G. bisporus (J. Carbó & Pérez-De-Greg.) J. Carbó & Pérez-De-Greg., G. dentatus Murrill, G. discipes (Clem.) Murrill, G. dysosmus Polemis & Noordel., G. fuscotramus Mešić, Tkalčec & Chun Y. Deng, G. pubipes Antonín, A. Ortega & Esteve-Rav. and G. volkertii are similar to the new species. However, G. bisporus, belonging to sect. Levipedes, has a brown to reddish brown pileus and larger basidiospores (9.0–11 × 4.5–5.5 μm), and true cheilocystidia are absent (Antonín and Noordeloos 2010); G. dentatus has a dentate pileus margin, a white stipe and larger basidiospores (7–8.5 × 6–7 μm), growing on lawns (Murrill 1916); G. discipes has free lamellae and a white stipe arising from a hypogaeous disk (Murrill 1916); G. dysosmus, sect. Impudicae, has garlic-smelling basidiomata, dark greyish brown lamellae, larger basidiospores (8.0–11 × 3.3–4.5 μm), and caulocystidia (Antonín and Noordeloos 2010); G. fuscotramus, belonging to sect. Vestipedes [= Marasmiellus fuscotramus (Mešić, Tkalčec & Chun Y. Deng) J.S. Oliveira], has abundant rhizomorphs, larger basidiospores (8.2–9.6 × 3.7–4.4), and pale grey-brown lamellar and pileus trama (Mešić et al. 2011); G. pubipes, sect. Levipedes, has deeply emarginate to adnexed lamellae and an entirely pubescent stipe with numerous caulocystidia (Antonín and Noordeloos 2010); and G. volkertii has a umbonate and estriate pileus, adnexed lamellae, and larger basidiospores (8.2–9.6 × 3.7–4.4 μm), growing on lawn (Murrill 1916).

Gymnopus schizophyllus J.P. Li, T.H. Li & Y. Li, sp. nov.

MycoBank No: 837642
Figs 4, 5

Typification

China, Guangdong Province, Xinyi City, Yunkaishan National Nature Reserve, 22°17'08"N, 111°12'47"E, alt. 1453 m, 26 July 2019, B. Song, H.S. Wen & J.P. Li (GDGM 77165, holotype!).

Etymology

The epithet “schizophyllus” (Lat.) refers to the split edge of lamellae which is not so common in the genus.

Diagnosis

Differs from G. omphalinoides in its more or less depressed to slightly umbilicate pileus and more often split lamellar edge. Basidiomata mainly gregarious on decayed wood in broadleaf forest; pileus often pale orange to light brown; lamellae, adnate and generally split at the edge; stipe glabrous.

Description

Basidiomata gymnopoid or collybioid. Pileus 10–20 mm broad, membranous, hemispherical when young, then convex, with slightly inflexed margin, expanding to plano -convex , with a depressed disc, undulating at the margin, glabrous, radially striate or grooved towards the margin, often pale orange (6A3) to light brown (6D8), darker at the centre, sometimes to dark brown (6F8), white to light brown (6D8) towards the margin. Lamellae adnate, linear to arcuate, sometimes furcate to branched or venose, generally split at the edge, dull white to brownish orange (7C7), pale at the edge, sometimes with brown (7E8) to dark brown (7F8) tints somewhere, L = 10–20, l = 3–4. Stipe 11–21 mm long, 0.8–1 mm thick in middle, central, cylindrical, straight or sometimes curved, insititious, hollow, fibrous, glabrous, rooting deep in the substrate, but eventually attaches to the stump, white to orange-white (6A2) at first, slightly darker at base, then darker towards the apex, finally entirely light brown (7D8) to brown (7E8). Odour not distinctive.

Basidiospores [n=80] 4–6 (–6.5) × 2.5–3 (–3.5) μm (average = 4.90 × 2.93 μm, E = (1.29–) 1.33–2.00 (–2.20), Q = 1.68) or [n=20] 6.5–8 × 2.5–3 μm (average = 7.35 × 2.86 μm, E = 2.17–3.2, Q = 2.65), obovoid, ellipsoid to subellipsoid, sometimes amygdaliform. Basidia [n=20] 15–32 × 4–6 μm, clavate, 4-spored, rarely 1–3-spored. Basidioles [n=20] 17–27.5 × 4–6.5 μm, clavate, cylindrical. Lamellar edge sterile. Cheilocystidia [n=20] 20–43 × 4.5–9 μm, irregularly clavate, tending to inflated, with finger-like apical projection(s) or more or less diverticulate elements. Pileipellis a cutis composed of thin-walled, cylindrical hyphae up to 18 μm wide, smooth or with scattered diverticula, hyaline to slightly greyish; Rameales-like structures present but very few; terminal elements short, broad, mostly inflated, vesiculose or pyriform to cystidioid (clavate), obtuse and sometimes diverticulate, mixed with a few irregularly branched elements, some resembling Dryophila-type structures. Stipitipellis a cutis composed of cylindrical hyphae, up to 19 μm wide, thin- to thick-walled, smooth, non-dextrinoid, diverticulate, parallelly arranged. Caulocystidia absent. Clamp connections present.

Ecology

Saprotrophic, gregarious or in small clusters, usually rooting around roots and stumps in broadleaf forests.

Additional specimens examined

China, Guangdong Province, Xinyi City, Yunkaishan National Nature Reserve, 22°17'10"N, 111°12'50"E, alt. 1450 m, 26 July 2019, B. Song, H.S. Wen & J.P. Li (GDGM 77038); Guangdong Province, Xinyi City, Yunkaishan National Nature Reserve, 22°17'06"N, 111°12'51"E, alt. 1450 m, 29 May 2019, B. Song, H.S. Wen & J.P. Li (GDGM 76287); Yunnan Province, Maguan County, Laojunshan Moutain, 22°56'49"N, 104°32'44"E, alt. 1960 m, 11 August 2016, X.H. Wang (KUN-HKAS 96494).

Remarks

Gymnopus schizophyllus is a very distinct species by the orange to brown pileus that becomes paler with age; by the lamellae with generally split edge; by the two sizes of basidiospores: 1) 4–6 (–6.5) × 2.5–3 (–3.5) μm from the usual 4-spored basidia and 2) a few larger basidiospores up to 8 μm long from the 1–3-spored basidia; and by a pileipellis often with scattered cystidioid (clavate) or vesiculose to pyriform terminal elements.

Morphologically, among the known species of Gymnopus with a striate or grooved pileus and similarly sized basidiospores, G. discipes, G. expallens (Peck) Murrill, G. fusipes (Bull.) Gray, G. micromphaloides R.H. Petersen & K.W. Hughes, G. oculatus Murrill, G. omphalinoides, G. pseudomphalodes (Dennis) J.L. Mata, G. purpureicollus (Corner) A.W. Wilson, Desjardin & E. Horak, G. sepiiconicus (Corner) A.W. Wilson, Desjardin & E. Horak and G. subflavescens Murrill are similar to the new species. However, G. discipes has a subfleshy pileus with a wide umbo, free and ventricose lamellae and a white stipe (Murrill 1916); G. expallens has basidiomata with a distinct odour, a hygrophanous pileus, adnexed and ventricose lamellae, and a broad stipe up to 4 mm (Murrill 1916); G. fusipes has a fleshy pileus and a fusoid stipe with pseudorrhiza (Antonín and Noordeloos 2010); G. micromphaloides, sect. Vestipedes [= Collybiopsis micromphaloides (R.H. Petersen & K.W. Hughes) R.H. Petersen], has adnexed and ventricose lamellae, a scurfy-vestured stipe, and strongly encrusted hyphae of the pileipellis (Petersen and Hughes 2014); G. oculatus has a white pileus in general, nearly free lamellae and a whitish pruinose, larger stipe (Murrill 1916); G. omphalinoides generally has a deeply umbilicate pileus, broad, adnate and ventricose lamellae; G. pseudomphalodes has a cream pileus and regularly cylindrical cheilocystidia (Dennis 1961); G. purpureicollus has a hygrophanous pileus, subfree to adnate lamellae with a decurrent tooth and a lamellar edge without cheilocystidia (Wilson et al. 2004); G. sepiiconicus, sect. Levipedes, has hyphae with annular incrustations in the stipitipellis (Wilson et al. 2004); and G. subflavescens has white basidiomata overall, crowded lamellae and small, globose basidiospores (Murrill 1916).

Figure 4. 

Basidiomata of Gymnopus schizophyllus a GDGM 77038 b GDGM 76287 c GDGM 77165 holotype! d KUN-HKAS 96494 a, c photographed by J.P. Li b photographed by H.S. Wen d photographed by S.H. Li. For a detailed display, the split lamellar edge is magnified in a. Scale bar: 1 cm.

Figure 5. 

Microscopic features of Gymnopus schizophyllus (GDGM 77165, holotype!) a Basidiospores b Basidia c Basidioles d Cheilocystidia e terminal elements of the pileipellis. Drawing by J.P. Li. Scale bars: 10 μm (a–c), 20 μm (d, e).

Discussion

According to the phylogenetic results, the two new species could be taken to represent a new section within Gymnopus s. s.tr., a new subsection of Gymnopus sect. Gymnopus or a new member of G. sect. Gymnopus. Suppose the two new species and samples from India represent a new section or subsection? In that case, the samples from New Zealand may occupy a taxonomic position at the same level due to their phylogenetic relationship. Thus, given the three alternative systematic interpretations for the two new species and the monophyletic group they form, we argue that the morphological features and evidence from the molecular data strongly support the two new species as members of G. sect. Gymnopus.

Morphologically, the taxonomic placement of G. omphalinoides and G. schizophyllus can be correlated with the pileipellis features, particularly its terminal cells. After comparison, the two new species with glabrous stipe and at least the part of Dryophila-like structures in pileipellis are easily confused with species within the G. sect. Levipedes (Fr.) Halling (Antonín and Noordeloos 2010). However, the new species have additional inflated and broad pileipellis terminal elements and are only distantly related to that section. Gymnopus sect. Androsacei and G. sect. Gymnopus are included in a strongly supported clade, indicating they are close. But G. sect. Androsacei has rhizomorphs, dextrinoid trama (at least in the stipe apex) and a pileipellis mixed with broom cells (Antonín and Noordeloos 2010). Furthermore, G. sect. Androsacei does not form a distinct monophyletic clade neither in this study nor in Oliveira et al. (2019), César et al. (2020), and so forth. This issue needs to be addressed in future studies. Currently, known species with molecular data are very few, which perhaps could explain this topologic structure. Additionally, a phylogenetic tree based on more genetic markers might provide an improved result. Besides, G. sect. Impudicae is characterised by basidiomata with distinctive odour and often inconspicuous cheilocystidia (Antonín and Noordeloos 2010). These divergent morphological features reflect the non-trivial phylogenetic distance from the two new species. Unexpectedly, the two new species have a membranous pileus and non-fusoid stipe devoid of pseudorrhiza, contrary to the traditional circumscription of G. sect. Gymnopus in macro-morphology. However, the molecular phylogenetic results reveal that the clade they form is the most closely related group to G. sect. Gymnopus except for the two samples from New Zealand. After examining the micromorphological structures intensively, the synapomorphy eventually came to the surface. Cheilocystidia of both newly described species are versiform diverticulated cells and generally agree in size and shape with those of G. fusipes (Fig. 6). Also, the pileipellis, composed of inflated elements with some resembling Dryophila-type structures, is similar to G. fusipes and follows the key rule for sectional delimitation in Gymnopus s. str. [for a detailed macro- and micromorphological description of G. fusipes see Antonín and Noordeloos (1997, 2010)]. Besides, the two new species lack a typical Rameales-type pileipellis and any well-developed caulocystidia, in contrast to G. sect. Vestipedes which is already a part of Collybiopsis (Antonín and Noordeloos 2010; Oliveira et al. 2019; Petersen and Hughes 2021). Furthermore, the original G. sect. Perforantia is currently considered a distinct genus – Paragymnopus – whose members usually have non-glabrous stipe and lack cheilocystidia (Petersen and Hughes 2016; Oliveira et al. 2019).

Figure 6. 

Gymnopus fusipes (Mokrá near Brno, place called Nad dlouhým (Sivický les forest), 18 June 2002, A. Vágner, BRNM 670783) a Cheilocystidia b Pileipellis terminal cells. Drawings by V. Antonín. Scale bar: 20 µm.

As the characteristic of the pileipellis is a significant factor for sectional delimitation in Gymnopus, the features in macro-morphology are second. The current sectional concept was summarised based on features from one species, G. fusipes. That means the single known species circumscribes the current knowledge at the sectional level. This is also why only minor divergence in micro-morphology occurs between G. sect. Gymnopus and the two new species. Following the indication from phylogenetic results and similarity of micro-morphology, thus, an emended and improved concept of G. sect. Gymnopus is proposed herein by including G. omphalinoides and G. schizophyllus.

A very interesting and unusual characteristic is a splitting lamellar edge in both newly described species. What advantage such split lamellar edge could confer is difficult to surmise, but Antonín and Herink (1999) described the same characteristic in Gymnopus luxurians (Peck) Murrill [recently Collybiopsis luxurians (Peck) R.H. Petersen]. They proposed that this may be a reaction to specific climatic conditions (the higher humidity, the better hymenium development) because it was most distinct in the collections from greenhouses, botanic gardens and tropical Africa.

Borthakur and Joshi (2016) provided a nrITS sequence and a few morphological characteristics of the collection NEHU MBSRJ48 annotated as Micromphale foetidum which comes from a subtropical forest of Northeast India, quite similar to G. schizophyllus. However, the sequence is quite different from the sequences more well-recognised for the current Gymnopus foetidus (Sowerby) P.M. Kirk. It likely represents an incorrectly determined ITS sequence in GenBank like several others as argued by Nilsson et al. (2006) and Hofstetter et al. (2019). The specimen has a depressed to umbilicate pileus, a glabrous stipe and similarly sized basidiospores (5.2 × 2.88 μm). The nrITS sequence is highly similar to that of G. schizophyllus, implying they are possibly conspecific. The collection from India clearly belongs in G. sect. Gymnopus. The collections from New Zealand, named as Marasmius otagensis, are characterised by a depressed to umbilicate pileus, glabrous stipe and a pileipellis with broad, mostly inflated terminal elements (according to photos from Dr. Jerry Cooper). The phylogenetic placement indicates that this is another member of G. sect. Gymnopus.

Gymnopus sect. Gymnopus , emend.

Emended circumscription

Pileus membranous or fleshy; stipe smooth or slightly to deeply sulcate-striate, with a well-developed or reduced pseudorrhiza; spore print white to pale ochraceous; cheilocystidia versiform, clavate, fusoid, tending inflated, sometimes with more or less finger-like apical projection(s), or diverticulate elements; pileipellis a cutis, or this transitioning to a trichoderm, with broad terminal elements, mostly inflated, mixed with irregularly branched elements and some resembling Dryophila-type structures; no dextrinoid or cyanophilous structures; rooting in the substrate, frequently on roots or stumps.

Type species. Gymnopus fusipes (Bull.) Gray

Other currently recognised species. G. omphalinoides J.P. Li, T.H. Li & Y. Li, G. schizophyllus J.P. Li, T.H. Li & Y. Li

A key to species of Gymnopus sect. Gymnopus

1 Pileus fleshy; stipe with a distinct pseudorrhiza G. fusipes
– Pileus membranous; stipe without a pseudorrhiza but rooting in the substrate 2
2 Pileus generally deeply umbilicate; lamellae broad, adnate and ventricose G. omphalinoides
– Pileus more or less depressed; lamellae adnate, linear to arcuate G. schizophyllus

Acknowledgements

Grateful thanks are due to Prof. Xiang-Hua Wang (Kunming Institute of Botany, CAS, Kunming, China) for providing specimen(s), sequences, suggestions and photographs, Dr Jerry Adrian Cooper (Landcare Research, New Zealand) for providing sequences and photographs, Dr Rolf Henrik Nilsson (University of Gothenburg, Gothenburg, Sweden) for improving our work, Dr Ji-Ze Xu (Jilin Agricultural Science and Technology University, Jilin, China) for providing specimens and sequence data, Dr Md Iqbal Hosen, Prof. Wang-Qiu Deng, Dr Chao-Qun Wang (Guangdong Institute of Microbiology, Guangzhou, China) and Xiao-Ya An (Shenyang Agricultural University, Shenyang, China) for providing suggestions, Dr Ming Zhang, Mr. Ting Li, Mr. Juan-Yan Xu, Mr. Hao Huang, Mr. Li-Qiang Wu, Mr. Ning Zhan, Mr. Hua-Shu Wen (Guangdong Institute of Microbiology, Guangzhou, China), Prof. Shu-Hong Li (Yunnan Academy of Agricultural Sciences, Kunming, China) for hunting collection(s). This work was supported by the National Natural Science Foundation of China (Nos. 31750001, 31970016), the Science and Technology Planning Project of Guangdong Province, China (2019B121202005, 2018B030320001, 20070617627078), the government procurement project of Shenzhen, China (SZCG2019191412), China Agriculture Research System (CARS-20), the government procurement project of China (ZX2021-FJC083), Projects of Science and Technology Programs of Guizhou Province ([2019]2451, [2019]4007-2), GDAS’ Special Project of Science and Technology Development (Grant No. 2019GDASYL-0104011), and the Project of Comprehensive Scientific Investigation of Dalingshan Forest Park in Dongguan (441901-2021-08594). The studies of V.A. were made possible by the support provided to the Moravian Museum by the Ministry of Culture of the Czech Republic as part of its long-term conceptual development program for research institutions (DKRVO, ref. MK000094862).

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