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Taxonomy and phylogeny of Dichostereum (Russulales), with descriptions of three new species from southern China
expand article infoShi-Liang Liu, Shuang-Hui He
‡ Beijing Forestry University, Beijing, China
Open Access

Abstract

Nine species of Dichostereum were subjected to phylogenetic analyses, based on a combined dataset of ITS1-5.8S-ITS2-nrLSU-tef1 sequences. The morphology of specimens collected from China and Australia were studied. Three species, D. austrosinense, D. boidinii and D. eburneum, collected from southern China, are described and illustrated as new to science, based on the morphological and molecular evidence. Dichostereum austrosinense is characterised by the relatively large gloeocystidia (80–130 × 8–15 µm) and basidiospores (7.3–8 µm in diam.) with large warts and crests. Dichostereum boidinii is distinguished by its thick basidiomata and relatively small basidiospores (5.5–6.5 µm in diam.) with large warts and crests. Dichostereum eburneum is unique in having pale basidiomata growing on bark of living Castanopsis, abundant crystals in the context and basidiospores with dense and large ornamentations. A key to the 5 species of Dichostereum in China is given.

Keywords

Amyloid basidiospores, corticioid fungi, dichohyphae, Peniophoraceae, Vararia

Introduction

Dichostereum Pilát, typified with D. durum (Bourdot & Galzin) Pilát, is a small and well-delimited corticioid genus in Russulales. It is characterised by resupinate basidiomata with smooth or grandinioid hymenophore, dimitic hyphal system with dextrinoid dichohyphae and clamped generative hyphae, gloeocystidia and ellipsoid or subglobose, ornamented basidiospores with a strong amyloid reaction in Melzer’s reagent (Hallenberg 1985; Bernicchia and Gorjón 2010). Previously, Dichostereum was placed in Lachnocladiaceae, which includes genera with dextrinoid skeletal hyphae (Reid 1965; Parmasto 1968, 1970; Hallenberg 1985). However, recent phylogenetic analyses, based on DNA sequences, showed that Dichostereum formed a monophyletic lineage in the Peniophoraceae clade, which includes genera with or without dextrinoid hyphae (Larsson and Larsson 2003; Miller et al. 2006; Larsson 2007).

Dichostereum was once treated as a subgenus of Vararia P. Karst. (Peniophoraceae, Russulales) by some mycologists since the two genera are very similar in morphology except that the latter has smooth basidiospores (Boidin 1967; Parmasto 1970; Lanquetin 1973). Boidin and Lanquetin (1977) emended the description of Dichostereum and retained it as a separate genus. Later, Boidin and Lanquetin (1980) monographed the genus and provided a key to its 11 species based on evidence of morphology, distribution and intercompatibility tests of cultures. Based on limited sampling, their results showed that D. effuscatum (Cooke & Ellis) Boidin & Lanq. and D. granulosum (Pers.) Boidin & Lanq. were widely distributed, while the other species seemed to be rather endemic (Boidin and Lanquetin 1980). Few studies on the genus have been carried out since then and many regions including East Asia need further collecting and study (Boidin et al. 1987, Boidin and Michel 1998).

Previously, two species, Dichostereum boreale (Pouzar) Ginns & M.N.L. Lefebvre (= D. granulosum) and D. pallescens (Schwein.) Boidin & Lanq., were reported in temperate China (Dai 2011). The species diversity of the genus in China is still unclear. In the present paper, we provide a morphological and phylogenetic study of the genus based on specimens mostly collected from southern China. This is part of an ongoing study of the corticioid fungi of the Russulales in China.

Materials and methods

Morphological studies

Voucher specimens were deposited in the herbaria of Beijing Forestry University, Beijing, China (BJFC) and in the Centre for Forest Mycology Research, U.S. Forest Service, Madison, USA (CFMR). Freehand sections were made from dried basidiomata and mounted in 2% (w/v) potassium hydroxide (KOH), 1% phloxine (w/v) or Melzer’s reagent. Microscopic examinations were carried out with a Nikon Eclipse 80i microscope (Nikon Corporation, Japan) at magnifications up to 1000×. Drawings were made with the aid of a drawing tube. All measurements were carried out with sections mounted in Melzer’s reagent. Ornamentations were excluded from the measurements of basidiospores. Scanning electron micrographs (SEM) were taken with a JEOL JSM-6700F microscope (JEOL, Japan). Dried specimens were mounted directly in gold and platinum and examined and photographed at 10.0 kV. Colour names and codes follow Kornerup and Wanscher (1978). Herbarium code designations are from Index Herbariorum (Thiers, continuously updated).

DNA extraction and sequencing

The CTAB plant genome rapid extraction kit DN14 (Aidlab Biotechnologies Co. Ltd, Beijing) was used for DNA extraction and PCR amplification from dried specimens or cultures. The ITS, partial nrLSU and tef1 markers were amplified with the primer pairs ITS5/ITS4 (White et al. 1990), LR0R/LR7 (Vilgalys and Hester 1990) and 983F/1567R (Rehner and Buckley 2005), respectively. The PCR procedures followed Dai and He (2016). DNA sequencing was performed at Beijing Genomics Institute and the sequences were deposited in GenBank (Benson et al. 2018). The sequence quality control followed Nilsson et al. (2012). BioEdit v.7.0.5.3 (Hall 1999) and Geneious v.11.1.15 (Kearse et al. 2012) were used for chromatogram check and contig assembly.

Phylogenetic analyses

The molecular phylogeny was inferred from a combined dataset of ITS1-5.8S-ITS2-nrLSU-tef1 sequences of representative members of Peniophoraceae sensu Larsson (2007) (Table 1). Echinodontium tinctorium (Ellis & Everh.) Ellis & Everh. was selected as the outgroup (Liu et al. 2017a). The sequences of the three markers (ITS, nrLSU and tef1) were aligned separately using MAFFT v.7 (Katoh et al. 2017, http://mafft.cbrc.jp/alignment/server/) with the G-INS-i iterative refinement algorithm and optimised manually in BioEdit v.7.0.5.3. The programme Gblocks v.0.91b (Castresana 2000) was then used to exclude poorly aligned positions of the ITS alignment. The separate alignments were concatenated using Mesquite v.3.5.1 (Maddison and Maddison 2018). The combined alignments were deposited in TreeBase (http://treebase.org/treebase-web/home.html, submission ID: 23332).

Species and sequences used in the phylogenetic analyses. Newly generated sequences are set in bold. Holotypes are marked with *.

Taxa Voucher Locality ITS nrLSU tef1
Asterostroma bambusicola He 4132 Thailand KY263865 KY263871 MH669240
A. cervicolor He 4020 China KY263859 KY263869
Baltazaria eurasiaticogalactina CBS 666.84 France AY293211
B. octopodites FLOR 56449 Brazil MH260025 MH260047
Dichostereum austrosinense He 4871* China MH538317 MH538334
He 4316 China MH538316 MH538335
He 3551 China MH538314 MH550363
D. boidinii He 5026* China MH538324 MH538330
He 1662 China MH538309 MH550360
He 4410 China MH538315 MH538331 MH550361
He 462 China MH538311
Dai 16117 China MH538312 MH538327 MH550362
D. durum Fungi Gallici 1985 France AF506429 AF506429
D. eburneum He 5374* China MH538318 MH538337 MH550366
D. effuscatum GG 930915 France AF506390 AF506390
FP 101758 Sp USA MH538323 MH538336 MH550367
CBS 516.80 USA AF323739
D. granulosum NH 7137 Canada AF506391 AF506391
FP 133479 Sp USA MH538321 MH538333 MH550368
He 1887 China MH538313 MH538332
D. pallescens Kropp 2 USA MH538320 MH538326 MH550365
CBS 717.81 USA AF518614
He 3266 China MH538310 MH538325 MH550364
D. aff. pallescens KHL 10258 Puerto Rico AF506428 AF506428
D. rhodosporum Dai 18625A Australia MH538319 MH538329 MH550370
D. sordulentum FP 11735 Sp USA MH538322 MH538328 MH550369
Duportella tristicula He 4775 China MH669235 MH669239 MH669245
Echinodontium tinctorium HHB 12866 Sp USA KY172888 KY172903 MH550371
Gloiothele lactescens EL 8-98 Sweden AF506453 AF506453
G. lamellosa KHL11031 Venezuela AF506454 AF506454
Lachnocladium cf. brasiliense CALD 161213-1 Brazil MH260037 MH260055
L. schweinfurthianum KM 49740 Cameroon MH260033 MH260051
L. sp. KHL10556 Jamaica AF506461 AF506461
Parapterulicium subarbusculum FLOR 56456 Brazil MH260026 MH260026
FLOR 56459 Brazil MH260027 MH260049
Peniophora polygonia He 3668 China MH669233 MH669237 MH669243
P. rufa He 2788 China MH669234 MH669238 MH669244
Scytinostroma portentosum EL11-99 Sweden AF506470 AF506470
Vararia investiens He 2104 USA MH669236 MH669242
FP 151122 USA MH971976 MH971977
Vesiculomyces citrinus He 3716 China KY860369 KY860429 MH669241

For both Maximum Likelihood (ML) and Bayesian Inference (BI), a partitioned analysis was performed with the following five partitions: ITS1, 5.8S, ITS2, nrLSU and tef1. The ML analysis was performed using RAxML v.8.2.10 (Stamatakis 2014) with the bootstrap values (ML-BS) obtained from 1,000 replicates and the GTRGAMMA model of nucleotide evolution. The maximum parsimony (MP) analysis was performed using PAUP* 4.0a162 (Swofford 2003). Trees were generated using 100 replicates of random stepwise addition of sequence and tree-bisection reconnection (TBR) branch-swapping algorithm with all characters given equal weight. Branch supports (MP-BS) for all parsimony analyses were estimated by performing 1,000 bootstrap replicates with a heuristic search of 10 random-addition replicates for each bootstrap replicate. The BI was performed using MrBayes 3.2.6 (Ronquist et al. 2012). The best-fit substitution model for each partitioned locus was estimated separately with jModeltest v.2.17 (Darriba et al. 2012). Four Markov chains were run for 6,000,000 generations until the split deviation frequency value was lower than 0.01. The convergence of the runs was checked using Tracer v.1.7 (Rambaut et al. 2018). Trees were sampled every 100th generation. The first quarter of the trees, which represented the burn-in phase of the analyses, was discarded and the remaining trees were used to calculate Bayesian posterior probabilities (BPP) in the majority rule consensus tree. All trees were visualised in FigTree 1.4.2 (Rambaut 2014).

Results

Phylogenetic inference

The ITS-nrLSU-tef1 sequence dataset contained 37 ITS, 38 nrLSU and 18 tef1 sequences from 40 samples representing 26 ingroup taxa and the outgroup (Table 1). Twenty ITS, 18 nrLSU and 18 tef1 sequences were generated for this study. The dataset had an aligned length of 2239 characters, of which 1596 were constant, 163 variable characters were parsimony-uninformative and 480 were parsimony-informative. MP analysis yielded six most parsimonious trees. jModelTest suggested TIM2ef+G, K80+G, TPM1uf+G, TIM2+I+G and TrN+I+G to be the best-fit models of nucleotide evolution for ITS1, 5.8S, ITS2, nrLSU and tef1 markers, respectively, for the Bayesian analysis. The average standard deviation of split frequencies of BI was 0.004704 at the end of the run. MP and BI analyses resulted in an almost identical tree topology compared to the ML analysis. Only the ML tree is shown in Fig. 1 with ML and MP bootstrap values ≥50% and Bayesian posterior probabilities ≥0.95 labelled along the branches.

In the tree (Fig. 1), the nine sampled species of Dichostereum formed a strongly supported clade in Peniophoraceae (ML-BS = 91, MP-BS = 97, BPP = 1.00). Vararia investiens (Schwein.) P. Karst., the generic type of Vararia, formed a sister lineage to Dichostereum, but this close relationship did not receive significant support. Of the three new species, samples of D. austrosinense and D. boidinii formed two strongly supported lineages, whilst the single specimen of D. eburneum formed the sister taxon to D. boidinii and D. aff. pallescens. Dichostereum effuscatum from France and USA and both D. granulosum and D. pallescens from north America and China, formed three strongly supported lineages. Single samples of D. durum from France, D. rhodosporum from Australia and D. sordulentum from USA formed their own distinct lineages.

Figure 1. 

Phylogeny of Dichostereum and representatives of Peniophoraceae inferred from ITS-nrLSU-tef1 sequences. Topology is from ML analysis with maximum likelihood bootstrap support values (≥50, former), parsimony bootstrap support values (≥50, middle) and Bayesian posterior probability values (≥0.95, latter) shown along the branches. Different species of Dichostereum are indicated as coloured blocks. The new species are set in bold. Scale bar: 0.05 nucleotide substitutions per site.

Taxonomy

Dichostereum austrosinense S.H. He & S.L. Liu, sp. nov.

MycoBank No: MB826931
Figs 2a, 3, 6a

Typification

CHINA. Guangxi Autonomous Region, Jinxiu County, Dayaoshan Nature Reserve, Shengtangshan, on fallen angiosperm trunk, 15 Jul 2017, He 4871 (holotype, BJFC 024390, ITS GenBank accession number: MH538317; isotype in CFMR).

Etymology

austrosinense” referring to the distribution in southern China.

Basidiomata

Perennial, resupinate, effused, closely adnate, inseparable from substrates, coriaceous to soft corky, at first as irregular small patches, later confluent up to 15 cm long, 4.5 cm wide, up to 1 mm thick. Hymenophore surface smooth, greyish-orange [5B(4–5)], brownish-yellow [5C(7–8)] to light brown [6D(4–8)], not cracking; margin abrupt, concolorous or darker than hymenophore surface.

Microscopic structures

Hyphal system dimitic. Context thickening, compact, composed of generative hyphae, dichohyphae, embedded basidiospores and scattered crystals. Generative hyphae rare, with clamp connections, hyaline, thin- to slightly thick-walled, 2–3 µm in diam. Dichohyphae dominant, hyaline to yellow, distinctly thick-walled, dichotomously branched with acute tips, weakly dextriniod. Catahymenium composed of dichohyphae, gloeocystidia, basidia and basidioles. Dichohyphae in this layer abundant, similar to those in the context, but strongly dextrinoid, more slender and more frequently branched, 20–50 μm across, 2–4 µm wide at lowest part. Gloeocystidia abundant, subcylindrical to subfusiform, hyaline, slightly thick-walled, with or without solidified contents, 80–130 × 8–15 µm. Basidia narrowly cylindrical, usually slightly sinuous, hyaline, thin-walled, with 4 sterigmata and a basal clamp connection, 50–80 × 5–8 µm; basidioles in shape similar to basidia, but slightly smaller. Basidiospores abundant, subglobose with a distinct apiculus, hyaline to pale yellowish-brown in KOH, thick-walled, strongly amyloid, (7–) 7.3–8 (–9) µm in diam.; walls ornamented with large warts and crests.

Additional specimens examined

CHINA. Hainan Province, Lingshui County, Diaoluoshan Nature Reserve, on fallen angiosperm trunk, 17 Mar 2016, He 3551 (BJFC 022052); Jiangxi Province, Lianping County, Jiulianshan Nature Reserve, on fallen angiosperm branch, 13 Aug 2016, He 4316 (BJFC 023758).

Remarks

Dichostereum austrosinense is overall characterised by the relatively large gloeocystidia and basidiospores with large warts and crests. Dichostereum peniophoroides (Burt) Boidin & Lanq. is similar to D. austrosinense but differs in having wider gloeocystidia (7–22 µm), slightly larger basidiospores (7–9 µm) with larger ornamentations and a distribution in Caribbean regions (Lanquetin 1973; Boidin and Lanquetin 1980). Dichostereum austrosinense is also similar to D. rhodosporum (Wakef.) Boidin & Lanq. which differs in having paler basidiomata, smaller ornamentations of basidiospores and a distribution in Australia and New Zealand (Boidin and Lanquetin 1980, Figs 2 and 6).

Figure 2. 

Basidiomata of Dichostereum species. a D. austrosinense (holotype, He 4871) b D. boidinii (holotype, He 5026) c D. eburneum (holotype, He 5374) d D. granulosum (He 1887) e D. pallescens (He 3266) f D. rhodosporum (Dai 18625A). Scale bar: 1 cm.

Figure 3. 

Microscopic structures of Dichostereum austrosinense (drawn from the holotype). a Basidiospores b Basidia c Gloeocystidia d Dichohyphae from hymenium e Dichohyphae from subiculum. Scale bar: 10 µm.

Dichostereum boidinii S.H. He & S.L. Liu, sp. nov.

MycoBank No: MB826932
Figs 2b, 4, 6b

Typification

CHINA. Hubei Province, Wufeng County, Breeding base of Magnolia, on angiosperm stump, 14 Aug 2017, He 5026 (holotype, BJFC 024544, ITS GenBank accession number: MH538324; isotype in CFMR).

Etymology

boidinii” (Lat.), named to honour Dr. Jacques Boidin (Lyon, France) for his contribution to the taxonomy of Dichostereum.

Basidiomata

Perennial, resupinate to effused-reflexed with slightly elevated margin, closely adnate, inseparable from substrates, coriaceous to soft corky, up to 8 cm long, 4 cm wide, 1.5 mm thick. Hymenophore surface smooth, greyish-orange [6B(3–4)], brownish-orange [6C(4–6)] to light brown [6D(4–6)], not cracking; margin abrupt, concolorous or darker than hymenophore surface.

Microscopic structures

Hyphal system dimitic. Context thickening, compact, composed of generative hyphae, dichohyphae, embedded basidiospores and scattered crystals. Generative hyphae rare, with clamp connections, hyaline, thin-walled, 2–3 µm in diam. Dichohyphae dominant, hyaline to yellow, distinctly thick-walled, dextriniod. Catahymenium composed of dichohyphae, gloeocystidia, basidia and basidioles. Dichohyphae in this layer abundant, similar to those in the context, but strongly dextrinoid, more frequently branched with short terminal branches, 20–40 μm across, 2–4 µm wide at lowest part. Gloeocystidia abundant, fusiform to subulate, hyaline, slightly thick-walled, with solidified contents, 20–60 × 7–12 µm. Basidia subclavate to subcylindrical, hyaline, thin-walled, with 4 sterigmata and a basal clamp connection, 25–40 × 5–7 µm; basidioles in shape similar to basidia, but slightly smaller. Basidiospores subglobose with a distinct apiculus, hyaline to pale yellowish-brown in KOH, thick-walled, strongly amyloid, (5–) 5.5–6.5 (–7) µm in diam.; walls ornamented with warts and crests.

Additional specimens examined

CHINA. Anhui Province, Huangshan County, Huangshan Nature Reserve, on fallen angiosperm trunk, 21 Oct 2011, He 462 (BJFC 012101); Hainan Province, Lingshui County, Diaoluoshan Nature Reserve, on rotten wood of Dacrydium, 13 Nov 2015, Dai 16117 (BJFC 020210); Jiangxi Province, Anyuan County, Sanbaishan Forest Park, on fallen angiosperm trunk, 15 Aug 2016, He 4410 (BJFC 023851); Yunnan Province, Kunming, Xishan Park, on angiosperm stump, 17 Jul 2013, He 1662 (BJFC 016129).

Remarks

Dichostereum boidinii is widely distributed in southern China and mainly characterised by the thick, brownish basidiomata and relatively small basidiospores with large warts and crests. Dichostereum pallescens is similar to D. boidinii but differs in having slender dichohyphae and smaller and sparser ornamentations of basidiospores (Boidin and Lanquetin 1980, Fig. 6). Dichostereum orientale Boidin & Lanq. resembles D. boidinii by sharing short terminal branches of dichohyphae, but differs in having smaller basidiospores (5–5.5 µm in diam.) and a distribution in Africa (Boidin and Lanquetin 1980). The ornamentation of basidiospores of D. boidinii is similar to D. austrosinense, but the latter species has larger gloeocystidia, basidia and basidiospores.

Figure 4. 

Microscopic structures of Dichostereum boidinii (drawn from the holotype). a Basidiospores b Basidia c Gloeocystidia d Dichohyphae from hymenium e Dichohyphae from subiculum. Scale bar: 10 µm.

Dichostereum eburneum S.H. He & S.L. Liu, sp. nov.

MycoBank No: MB826933
Figs 2c, 5, 6c

Typification

CHINA. Fujian Province, Wuyishan County, Wuyishan Nature Reserve, on bark of living Castanopsis, 6 Apr 2018, He 5374 (holotype, BJFC, ITS GenBank accession number: MH538318; isotype in CFMR).

Etymology

eburneum” referring to the white colour of hymenophore.

Basidiomata

Perennial, resupinate, effused, closely adnate, inseparable from substrate, coriaceous, at first as irregular small patches, later confluent up to 7 cm long, 2 cm wide, 200–500 µm thick. Hymenophore surface smooth, white (5A1), orange white (5A2) to greyish-orange [5B(3–4)], cracking with age; margin thinning out, concolorous with hymenophore.

Microscopic structures

Hyphal system dimitic. Context thickening, compact, composed of generative hyphae, dichohyphae, embedded basidiospores and abundant crystals. Generative hyphae rare, with clamp connections, hyaline, thin- to slightly thick-walled, 2–3 µm in diam. Dichohyphae dominant, hyaline to yellow, distinctly thick-walled, dextriniod, frequently branched, aseptate, 1–2 µm in diam. Catahymenium composed of dichohyphae, gloeocystidia, basidia and basidioles. Dichohyphae in this layer abundant, hyaline to pale yellow, distinctly thick-walled, strongly dextriniod, dichotomously branched with acute terminal tips, 15–30 μm across, 2–4 µm wide at lowest part. Gloeocystidia abundant, fusiform to subclavate, hyaline, thin-walled, with solidified contents, 20–50 × 5–10 µm. Basidia subcylindrical with basal part slightly swollen, hyaline, thin-walled, with 4 sterigmata and a basal clamp connection, 30–45 × 6–9 µm; basidioles in shape similar to basidia, but slightly smaller. Basidiospores subglobose with a distinct apiculus, hyaline to pale yellowish-brown in KOH, thick-walled, strongly amyloid, 6–7 (–8) µm in diam.; walls ornamented with dense, large warts and crests.

Remarks

Dichostereum eburneum is characterised by the pale basidiomata on bark of living tree, the presence of abundant crystals in context and basidiospores with dense and large ornamentations. Ecologically and macroscopically, D. eburneum resembles Dendrothele Höhn. & Litsch., but the microscopic features are largely different (Nakasone and Burdsall 2011). Dichostereum kenyense Boidin & Lanq. is similar to D. eburneum by sharing the large ornamentations of basidiospores, but differs in having wider span of dichohyphae, slightly larger basidiospores (7–8 µm) and a distribution in Africa (Boidin and Lanquetin 1980).

Figure 5. 

Microscopic structures of Dichostereum eburneum (drawn from the holotype). a Basidiospores; b Basidia c Gloeocystidia d Dichohyphae from hymenium e Dichohyphae from subiculum. Scale bar: 10 µm.

Figure 6. 

Scanning electron micrographs (SEM) of basidiospores of Dichostereum. a D. austrosinense (holotype, He 4871) b D. boidinii (holotype, He 5026) c D. eburneum (holotype, He 5374) d D. granulosum (He 1887) e D. pallescens (He 3266) f D. rhodosporum (Dai 18625A). Scale bar: 1 µm.

Key to 5 species of Dichostereum in China

1 Hymenophore grandinioid; basidiospores ellipsoid D. granulosum
Hymenophore smooth; basidiospores subglobose 2
2 Basidiomata white; on bark of living Castanopsis D. eburneum
Basidiomata brownish; on dead wood 3
3 Gloeocystidia ≥80 μm long D. austrosinense
Gloeocystidia <80 μm long 4
4 Basidiospores 6.5–7.5 µm in diam, ornamentation sparse D. pallescens
Basidiospores 5.5–6.5 µm in diam, ornamentation dense D. boidinii

Discussion

To date, 14 species of Dichostereum have been described worldwide including the three new species in the present paper (Boidin and Lanquetin 1980). Amongst them, 5 species, D. brevisporum (S.S. Rattan) Boidin & Lanq. from India, D. kenyense, D. orientale and D. ramulosum (Boidin & Lanq.) Boidin & Lanq. from Africa and D. peniophoroides from Caribbean regions, were not included in the present analyses. In order to resolve the infra-generic phylogenetic relationships of Dichostereum, samples of these species and any additional undescribed taxa should be included.

The family Peniophoraceae sensu Larsson (2007) formed a strongly supported clade in Russulales and included about 15 genera (Larsson and Larsson 2003; Miller et al. 2006; Larsson 2007; Leal-Dutra et al. 2018). Except for the coralloid Lachnocladium Lév. and the insect symbiont Entomocorticium H.S. Whitney, Bandoni & Oberw., all the other genera in the family are corticioid fungi, such as Asterostroma Massee, Peniophora Cooke, Scytinostroma Donk and Vararia. However, recent molecular and morphological studies showed that two species of Parapterulicium Corner with coralloid basidiomata belong to Peniophoraceae in the Russulales rather than Pterulaceae of the Agaricales (Leal-Dutra et al. 2018). In the phylogenetic tree, the type species, Parapterulicium subarbusculum Corner formed a distinct lineage, while P. octopodites Corner is closely related to Scytinostroma galactinum (Fr.) Donk and its relatives. More studies on the taxonomy and phylogeny of Peniophoraceae are needed, since some large genera such as Scytinostroma and Vararia are still polyphyletic and many species are undescribed.

Acknowledgements

The authors thank Drs. Rita Rentmeester and Karen Nakasone (Center for Forest Mycology Research, Northern Research Station, U.S. Forest Service, Madison, USA) for culture and literature loan. The authors acknowledge Dr. Yu-Cheng Dai (Beijing Forestry University, China) for providing specimens. This study was supported by the National Natural Science Foundation of China (Nos. 31670013 & 31470144) and the Fundamental Research Funds for the Central Universities (No. 2017PT09).

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