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Research Article
Morphological and phylogenetic evidence for recognition of two new species of Hyphoderma (Basidiomycota) from southern China, with a key to all Chinese Hyphoderma
expand article infoQian-Xin Guan, Yi-Fei Li, Chang-Lin Zhao
‡ Southwest Forestry University, Kunming, China
Open Access

Abstract

Wood-inhabiting fungi play crucial roles as decomposers in forest ecosystems and, in this study, two new wood-inhabiting corticioid fungi, Hyphoderma puerense and H. tenuissimum spp. nov., are proposed, based on a combination of morphological features and molecular evidence. Hyphoderma puerense is characterised by effused basidiomata with smooth to floccose hymenial surface, a monomitic hyphal system with clamped generative hyphae and ellipsoid basidiospores. Hyphoderma tenuissimum is characterised by resupinate basidiomata with tuberculate to minutely-grandinioid hymenial surface, septate cystidia and cylindrical to allantoid basidiospores. Sequences of ITS and nLSU rRNA markers of the studied samples were generated and phylogenetic analyses were performed with Maximum Likelihood, maximum parsimony and Bayesian Inference methods. These analyses showed that the two new species clustered into Hyphoderma, in which H. puerense grouped with H. moniliforme and H. tenuissimum formed a singleton lineage. In addition, an identification key to Chinese Hyphoderma is provided.

Keywords

Corticioid fungi, diversity, Hyphodermataceae, molecular phylogeny, taxonomy, Yunnan Province

Introduction

Fungi are eukaryotic microorganisms that play fundamental ecological roles as decomposers and mutualists of plants and animals. They drive carbon cycling in forest soils, mediate mineral nutrition of plants and alleviate carbon limitations of other soil organisms (Tedersoo et al. 2014). Fungi form an ecologically important branch of the tree of life, based on their distinct and diverse characters (James et al. 2020).

Hyphoderma Wallr. was typified by H. setigerum (Fr.) Donk (Donk 1957) and the genus is characterised by resupinate to effuse-reflexed basidiomata of ceraceous consistency and a smooth to tuberculate or hydnoid hymenophore. Hyphoderma species are characterised by a monomitic (rarely dimitic) hyphal structure with clamp connections on generative hyphae, presence of cystidia or not, suburniform to subcylindrical to cylindrical basidia and ellipsoid to subglobose, smooth, thin-walled basidiospores (Wallroth 1833; Bernicchia and Gorjón 2010). Currently, about 105 species have been accepted in Hyphoderma worldwide (Donk 1957; Nakasone 2008; Wu et al. 2010; Baltazar et al. 2016; Martín et al. 2018; Guan and Zhao 2021a, 2021b; Ma et al. 2021). Index Fungorum (http://www.indexfungorum.org; accessed on 16 July 2021) and MycoBank (https://www.mycobank.org; accessed on 16 July 2021) register 199 specific and infraspecific names in Hyphoderma.

Hyphoderma has been studied using molecular data, particularly the internal transcribed spacer (ITS) region and the large subunit nuclear ribosomal RNA gene (nLSU). Larsson (2007) showed that H. obtusum J. Erikss. and H. setigerum clustered into the Meruliaceae Rea and formed a sister taxon to Hypochnicium polonense (Bres.) Å. Strid. Telleria et al. (2012) proposed a new species, Hyphoderma macaronesicum Tellería, M. Dueñas, Beltrán-Tej., Rodr.-Armas & M.P. Martín and then discussed the relationships with the closely-related taxa in Hyphoderma. Research into the Hyphoderma setigerum complex showed that H. pinicola Yurch. & Sheng H. Wu represented a fifth species in this complex (Yurchenko and Wu 2014b). A revised family-level classification of the Polyporales revealed that four Hyphoderma species grouped into the residual polyporoid clade, belonging to Hyphodermataceae in that they grouped with three related genera in Meripilaceae: Meripilus P. Karst., Physisporinus P. Karst. and Rigidoporus Murrill (Justo et al. 2017).

In this study, two undescribed species of corticioid fungi from forest ecosystems were collected in the Yunnan Province, China. We present morphological and molecular phylogenetic evidence that support the recognition of two new species in Hyphoderma, based on the nuclear ribosomal internal transcribed spacer region (ITS1, 5.8S and ITS2) and the nuclear ribosomal nLSU (28S) gene.

Materials and methods

Morphology

The studied specimens are deposited at the Herbarium of Southwest Forestry University (SWFC), Kunming, Yunnan Province, P.R. China. Macromorphological descriptions are based on field notes and photos captured in the field and lab. Colour terminology follows Petersen (Petersen 1996). Micromorphological data were obtained from the dried specimens when observed under a light microscope following Dai (2012). The following abbreviations are used: KOH = 5% potassium hydroxide water solution, CB = Cotton Blue, CB– = acyanophilous, IKI = Melzer’s Reagent, IKI– = both inamyloid and indextrinoid, L = mean spore length (arithmetic average for all spores), W = mean spore width (arithmetic average for all spores), Q = variation in the L/W ratios between the specimens studied and n = a/b (number of spores (a) measured from given number (b) of specimens).

Molecular phylogeny

The CTAB rapid plant genome extraction kit-DN14 (Aidlab Biotechnologies Co., Ltd, Beijing) was used to obtain genomic DNA from the dried specimens following the manufacturer’s instructions (as done in Zhao and Wu 2017). The nuclear ribosomal ITS region was amplified with the primers ITS5 and ITS4 (White et al. 1990). The nuclear ribosomal LSU gene was amplified with the primers LR0R and LR7 (Vilgalys and Hester 1990; Rehner and Samuels 1994). The PCR procedure for ITS was as follows: initial denaturation at 95 °C for 3 min followed by 35 cycles at 94 °C for 40 s, 58 °C for 45 s and 72 °C for 1 min and a final extension of 72 °C for 10 min. The PCR procedure for nLSU was as follows: initial denaturation at 94 °C for 1 min followed by 35 cycles at 94 °C for 30 s, 48 °C for 1 min and 72 °C for 1.5 min and a final extension of 72 °C for 10 min. The PCR products were purified and sequenced at Kunming Tsingke Biological Technology Limited Company, Kunming, Yunnan Province, P.R. China. All newly-generated sequences were deposited in NCBI GenBank (Table 1).

Table 1.

List of species, specimens and GenBank accession numbers of sequences used in this study.

Species name Specimen No. GenBank accession No. References
ITS LSU
Climacocystis borealis FD-31 KP135308 KP135210 Justo et al. (2017)
Diplomitoporus crustulinus FD-137 KP135299 KP135211 Justo et al. (2017)
Hyphoderma amoenum USO 286622 HE577030 Telleria et al. (2012)
H. assimile CBS 125852 MH863808 MH875272 Vu et al. (2019)
H. cremeoalbum NH 11538 DQ677492 DQ677492 Larsson (2007)
H. crystallinum CLZhao 9338 MW917161 MW913414 Guan and Zhao (2021a)
CLZhao 9374 MW917162 MW913415 Guan and Zhao (2021a)
CLZhao 10224 MW917163 MW913416 Guan and Zhao (2021a)
CLZhao 11723 MW917164 MW913417 Guan and Zhao (2021a)
CLZhao 15841 MW917165 MW913418 Guan and Zhao (2021a)
CLZhao 18459 MW917166 MW913419 Guan and Zhao (2021a)
H. definitum GEL 2898 AJ406509 Yurchenko and Wu (2014)
NH 12266 DQ677493 DQ677493 Larsson (2007)
H. fissuratum CLZhao 6731 MT791331 MT791335 Ma et al. (2021)
CLZhao 6726 MT791330 MT791334 Ma et al. (2021)
H. floccosum CLZhao 17129 MW301683 MW293733 Guan and Zhao (2021b)
CLZhao 17296 MW301686 MW293736 Guan and Zhao (2021b)
CLZhao 16492 MW301688 MW293734 Guan and Zhao (2021b)
CLZhao 17215 MW301687 MW293735 Guan and Zhao (2021b)
H. granuliferum KHL 12561 JN710545 JN710545 Yurchenko and Wu (2014)
H. incrustatum KHL 6685 AY586668 Yurchenko and Wu (2014)
H. litschaueri NH 7603 DQ677496 DQ677496 Larsson (2007)
FP-101740-Sp KP135295 KP135219 Floudas and Hibbett (2015)
H. macaronesicum MA:Fungi:16099 HE577027 Yurchenko and Wu (2014)
TFC:Mic.15981 HE577028 Yurchenko and Wu (2014)
H. medioburiense NH 10950 DQ677497 DQ677497 Larsson (2007)
H. membranaceum CLZhao 5844 MW917167 MW913420 Guan and Zhao (2021a)
CLZhao 6971 MW917168 MW913421 Guan and Zhao (2021a)
H. microporoides CLZhao 6857 MW917169 MW913422 Guan and Zhao (2021a)
CLZhao 8695 MW917170 MW913422 Guan and Zhao (2021a)
H. moniliforme Wu 0211–42 KC928282 Yurchenko and Wu (2015)
Wu 0211–46 KC928284 KC928285 Yurchenko and Wu (2015)
H. mopanshanense CLZhao 6498 MT791329 MT791333 Ma et al. (2021)
CLZhao 6493 MT791328 MT791332 Ma et al. (2021)
H. nemorale TNM F3931 KJ885183 KJ885184 Yurchenko and Wu (2015)
Wu 9508–14 KC928280 KC928281 Yurchenko and Wu (2015)
H. nudicephalum Wu 9307–29 AJ534269 Nilsson et al. (2003)
Wu 9508–225 AJ534268 Nilsson et al. (2003)
H. obtusiforme KHL 1464 JN572909 Yurchenko and Wu (2014)
KHL 11105 JN572910 Yurchenko and Wu (2014)
H. obtusum JS 17804 AY586670 Yurchenko and Wu (2014)
H. occidentale KHL 8469 AY586674 Yurchenko and Wu (2014)
KHL 8477 DQ677499 DQ677499 Larsson (2007)
H. paramacaronesicum MA:Fungi:87736 KC984399 Martín et al. (2018)
MA:Fungi:87737 KC984405 Martín et al. (2018)
H. pinicola Wu 0108–32 KJ885181 KJ885182 Yurchenko and Wu (2014)
Wu 0108–36 KC928278 KC928279 Yurchenko and Wu (2014)
H. prosopidis E09/58–9 HE577029 Yurchenko and Wu (2015)
H. puerense CLZhao 9476* MW443045 Present study
CLZhao 9583 MW443046 MW443051 Present study
H. roseocremeum NH 10545 AY586672 Yurchenko and Wu (2014)
H. setigerum FCUG 1200 AJ534273 Nilsson et al. (2003)
H. setigerum FCUG 1688 AJ534272 Nilsson et al. (2003)
H. sinense CLZhao 7963 MW301679 MW293730 Guan and Zhao (2021b)
CLZhao 17811 MW301682 MW293732 Guan and Zhao (2021b)
CLZhao 7981 MW301680 MW293731 Guan and Zhao (2021b)
Hyphoderma sp. KUC20121102–21 KJ668522 Unpublished
KUC11052 KJ714002 Jang et al. (2015)
Wu 0311–25 KR868735 Unpublished
Wu 0310–6 KR868736 Unpublished
Wu 0808–87 KR868737 Unpublished
GEL3689 DQ340327 Unpublished
H. subsetigerum Wu 9304–18 AJ534277 Nilsson et al. (2003)
Wu 9202–15 AJ534278 Nilsson et al. (2003)
H. subsetigerum HHB11620 GQ409521 Yurchenko and Wu (2014)
CFMR MJL1536 GQ409522 Yurchenko and Wu (2014)
H. tenuissimum CLZhao 6930 MW443047 MW443052 Present study
CLZhao 7003 MW443048 MW443053 Present study
CLZhao 7221* MW443049 MW443054 Present study
CLZhao 16210 MW443050 MW443055 Present study
H. transiens NH 12304 DQ677504 DQ677504 Larsson (2007)
H. variolosum CBS 734.91 MH862320 MH873992 Vu et al. (2019)
CBS 735.91 MH862321 MH873993 Vu et al. (2019)
Hypochnicium erikssonii NH 9635 DQ677508 Larsson (2007)
H. geogenium NH 10910 DQ677509 Larsson (2007)
MA-Fungi 48308 FN552534 JN939576 Telleria et al. (2010)
H. michelii MA-Fungi 79155 NR119742 NG060635 Telleria et al. (2010)
H. punctulatum FP101698sp KY948827 KY948860 Justo et al. (2017)
H. sphaerosporum RLG15138sp KY948803 KY948861 Justo et al. (2017)
H. wakefieldiae MA-Fungi 7675 FN552531 JN939577 Telleria et al. (2010)
Physisporinus subcrocatus Dai 15917 KY131870 KY131926 Wu et al. (2017)
P. subcrocatus Dai 12800 KY131869 KY131925 Wu et al. (2017)
P. tibeticus Cui 9588 KY131873 KY131929 Wu et al. (2017)
Cui 9518 KY131872 KY131928 Wu et al. (2017)
Rigidoporus eminens Dai 17200 MT279690 MT279911 Wu et al. (2017)
R. undatus Miettinen-13591 KY948731 KY948870 Justo et al. (2017)

The sequences were aligned in MAFFT version 7 (Katoh et al. 2019) using the G-INS-i strategy. The alignment was adjusted manually using AliView version 1.27 (Larsson 2014). Each dataset was aligned separately at first and then the ITS1, 5.8S, ITS2 and nLSU regions were combined with Mesquite version 3.51. The combined dataset was deposited in TreeBASE (submission ID 28564). Climacocystis borealis (Fr.) Kotl. and Pouzar and Diplomitoporus crustulinus (Bres.) Domański were selected as outgroup (Fig. 1) as inspired by a previous study (Justo et al. 2017).

Figure 1. 

Maximum parsimony strict consensus tree illustrating the phylogeny of the two new species and related species in Hyphoderma, based on ITS1+5.8S+ITS2+nLSU sequences. Branches are labelled with maximum likelihood bootstrap values > 70%, parsimony bootstrap values > 50% and Bayesian posterior probabilities > 0.95, respectively.

Maximum parsimony analysis in PAUP* version 4.0a169 (http://phylosolutions.com/paup-test/) was applied to the combined ITS1+5.8S+ITS2+nLSU dataset. All characters were equally weighted and gaps were treated as missing data. Trees were inferred using the heuristic search option with TBR branch swapping and 1,000 random sequence additions. Max-trees were set to 5,000, branches of zero length were collapsed and all parsimonious trees were saved. Clade robustness was assessed using bootstrap (BT) analysis with 1,000 pseudoreplicates (Felsenstein 1985). Descriptive tree statistics – tree length (TL), composite consistency index (CI), composite retention index (RI), composite rescaled consistency index (RC) and composite homoplasy index (HI) – were calculated for each maximum parsimonious tree generated. The combined dataset was also analysed using Maximum Likelihood (ML) in RAxML-HPC2 through the CIPRES Science Gateway (Miller et al. 2012). Branch support (BS) for the ML analysis was determined by 1,000 bootstrap pseudoreplicates.

MrModeltest 2.3 (Nylander 2004) was used to determine the best-fit evolution model for each dataset (ITS1+5.8S+ITS2+nLSU) for Bayesian Inference (BI). BI was calculated with MrBayes version 3.2.7a (Ronquist et al. 2012). Four Markov chains were run for two runs from random starting trees for 3 million generations (Fig. 1). The first 25% of all generations was discarded as burn-in. A majority rule consensus tree was computed from the remaining trees. Branches were considered as significantly supported if they received a maximum likelihood bootstrap support value (BS) of > 70%, a maximum parsimony bootstrap support value (BT) of > 70% or a Bayesian posterior probability (BPP) of > 0.95.

Results

Molecular phylogeny

The ITS1+5.8S+ITS2+nLSU dataset comprised sequences from 86 fungal specimens representing 46 taxa. The dataset had an aligned length of 2,034 characters, of which 1,360 characters were constant, 131 were variable and parsimony-uninformative and 543 (35%) were parsimony-informative. Maximum parsimony analysis yielded 108 equally parsimonious trees (TL = 3,317, CI = 0.3361, HI = 0.6946, RI = 0.7051 and RC = 0.2370). The best model of nucleotide evolution for the ITS1+5.8S+ITS2+nLSU dataset estimated and applied in the Bayesian analysis was found to be GTR+I+G. Bayesian analysis and ML analysis resulted in a similar topology as in the MP analysis. The Bayesian analysis had an average standard deviation of split frequencies = 0.008952 (BI) and the effective sample size (ESS) across the two runs is double the average ESS (avg. ESS) = 1,771. The Bayesian tree is shown here (Fig. 1).

The phylogram inferred from ITS1+5.8S+ITS2+nLSU sequences (Fig. 1) highlights the two undescribed species in Hyphoderma; H. puerense as a sister to H. moniliforme and H. tenuissimum that forms an independent monophyletic lineage (100% parsimony bootstrap support, 100% likelihood bootstrap support and 1.00 BPP).

Taxonomy

Hyphoderma puerense C.L. Zhao & Q.X. Guan, sp. nov.

MycoBank No: 838411
Figs 2, 3

Holotype

China. Yunnan Province, Puer, Jingdong County, Huilianghe Village, GPS co-ordinates 24°04'45"N, 100°56'32"E, altitude 1246 m a.s.l., on fallen angiosperm branch, leg. C.L. Zhao, 4 January 2019, CLZhao 9476 (SWFC).

Etymology

puerense (Lat.): referring to the locality (Puer) of the specimens.

Description

Basidioma annual, resupinate, adnate, byssoid, without odour and taste when fresh, up to 15 cm long, 3 cm wide, 100–260 µm thick. Hymenial surface smooth to floccose, cream when fresh, cream to slightly buff on drying. Margin sterile, thinning out, narrow, cream.

Hyphal system monomitic, generative hyphae with clamps, colourless, thick-walled, frequently branched, interwoven, 2.5–4.5 µm in diameter; IKI-, CB-; tissues unchanged in KOH; subhymenial hyphae densely covered by crystals.

Figure 2. 

Basidiomata of Hyphoderma puerense (holotype). Scale bars: 2 cm (a); 1 mm (b).

Cystidia tubular, encrusted with small crystals, 25–97 × 5.5–9.5 µm.

Basidia clavate to subcylindrical, slightly constricted in the middle to somewhat sinuous, with 4 sterigmata and a basal clamp, 20–30 × 4.5–6 µm.

Figure 3. 

Microscopic structures of Hyphoderma puerense (holotype) a basidiospores b basidia and basidioles c cystidia d a section of hymenium. Scale bars: 5 µm (a); 10 µm (b–d).

Basidiospores ellipsoid, colourless, thin-walled, smooth, IKI-, CB-, (5.5–)6–7.5(–8) × 3–4.5(–5) µm, L = 6.53 µm, W = 3.71 µm, Q = 1.73–1.79 (n = 60/2).

Habitat and ecology

Climate of the sample collection site is subtropical monsoon climate area, the forest type is evergreen angiosperm forest and samples were collected on fallen angiosperm branches.

Figure 5. 

Microscopic structures of Hyphoderma tenuissimum (holotype) a basidiospores b basidia and basidioles c cystidia d a section of hymenium. Scale bars: 10 µm (a–d).

Additional specimens examined

China. Yunnan Province, Puer, Jingdong County, Huilianghe Village, GPS co-ordinates 24°04'45"N, 100°56'32"E, altitude 1246 m a.s.l., on fallen angiosperm branch, leg. C.L. Zhao, 5 January 2019, CLZhao 9583 (SWFC).

Hyphoderma tenuissimum C.L. Zhao & Q.X. Guan, sp. nov.

MycoBank No: 838412
Figs 4, 5

Holotype

China. Yunnan Province, Chuxiong, Zixishan Forestry Park, GPS co-ordinates 25°01'26"N, 101°24'37"E, altitude 2313 m a.s.l., on fallen angiosperm branch, leg. C.L. Zhao, 1 July 2018, CLZhao 7221 (SWFC).

Etymology

tenuissimum (Lat.): referring to the thin basidiomata.

Description

Basidioma annual, resupinate, adnate, membranaceous when fresh, hard membranaceous upon drying, up to 20 cm long, 3 cm wide, 30–100 µm thick. Hymenial surface tuberculate to minutely-grandinioid, slightly buff when fresh, buff upon drying, cracking. Margin sterile, slightly buff, 1 mm wide.

Figure 4. 

Basidiomata of Hyphoderma tenuissimum (holotype). Scale bars: 2 cm (a); 1 mm (b).

Hyphal system monomitic, generative hyphae with clamps, colourless, thick-walled, frequently branched, interwoven, 3–5 µm in diameter, IKI-, CB-; tissues unchanged in KOH.

Cystidia large, cylindrical, with 4–12 clamped septa, with abundant encrustations, 50–220 × 6.5–13 µm.

Basidia clavate to subcylindrical, constricted, somewhat sinuous, with 4 sterigmata and a basal clamp connection, 17–31 × 4.5–8 µm.

Basidiospores cylindrical, colourless, thin-walled, smooth, with oil drops inside, IKI–, CB–, 7–10.5(–11) × 3–4.5(–5) µm, L = 8.75 µm, W = 4.15 µm, Q = 2.02–2.18 (n = 120/4).

Habitat and ecology

Climate of the sample collection site is subtropical monsoon climate area, the forest type is evergreen angiosperm forest and samples were collected on fallen angiosperm branches.

Additional specimens examined

China. Yunnan Province, Chuxiong, Zixishan National Forestry Park, GPS co-ordinates 25°01'26"N, 101°24'37"E, altitude 2263 m a.s.l., on fallen angiosperm branch, leg. C.L. Zhao, 1 July 2018, CLZhao 6930, CLZhao 7003 (SWFC); Wenshan, Pingba Town, Wenshan National Nature Reserve, GPS co-ordinates 23°18'19"N, 104°42'47"E, altitude 1976 m a.s.l., on fallen angiosperm branch, leg. C.L. Zhao, 25 July 2019, CLZhao 16210 (SWFC).

Discussion

In the present study, two new species, Hyphoderma puerense and H. tenuissimum are described, based on phylogenetic analyses and morphological characters.

Phylogenetically, the two new taxa were found to belong to Hyphoderma, in which H. puerense forms a sister species to H. moniliforme and H. tenuissimum forms an independent monophyletic lineage (100% BS, 100% BP and 1.00 BPP).

Morphologically, Hyphoderma puerense is similar to H. obtusiforme J. Erikss. & Å. Strid and H. obtusum in having a smooth hymenium, non-septate cylindrical cystidia and ellipsoid basidiospores. However, H. obtusiforme differs from H. puerense by both larger basidia (30–40 × 8–9 µm) and basidiospores (10–14 × 5–7 µm; Eriksson and Ryvarden 1975). Hyphoderma obtusum also differs from H. puerense by larger basidia (30–35 × 6–8 µm) and basidiospores (8–9 × 5–6.5 µm; Eriksson 1958). Hyphoderma puerense is similar to H. roseocremeum (Bres.) Donk in having smooth hymenium and non-septate cylindrical cystidia. However, Hyphoderma roseocremeum differs through the presence of larger basidiospores (8–12 × 3–4 µm; Bernicchia and Gorjón 2010).

Morphologically, Hyphoderma tenuissimum is similar to H. floccosum C.L. Zhao & Q.X. Guan, H. mopanshanense, H. nudicephalum Gilb. & M. Blackw., H. pinicola, H. setigerum and H. subsetigerum Sheng H. Wu in having septocystidia and cylindrical basidiospores. However, Hyphoderma floccosum differs from H. tenuissimum by having a floccose hymenial surface and tubular cystidia (Guan and Zhao 2021b); H. mopanshanense is separated from H. tenuissimum by having porulose to pilose hymenial surface and smaller basidia (15–18.5 × 3–4.5 µm; Ma et al. 2021); H. nudicephalum differs from H. tenuissimum in the nature of the septocystidial apex (lacking encrustation; swollen up to 14 µm; Gilbertson and Blackwell 1988); H. pinicola is separated from H. tenuissimum by having basidia with two sterigmata and larger basidiospores (13–16 × 4–4.5 µm; Yurchenko and Wu 2014b); H. setigerum differs by having a combination of thin basidiomata with very long septocystidia (Bernicchia and Gorjón 2010); and H. subsetigerum differs from H. tenuissimum by having narrower basidia (20–30 × 4.5–5.5 µm) and smaller basidiospores (6–8 × 2.8–3.2 µm; Wu 1997).

Nilsson et al. (2003) highlighted the phylogeography of Hyphoderma setigerum (Basidiomycota) in the Northern Hemisphere in a study based on molecular analysis, morphological studies and crossing tests. Nine preliminary taxa were shown to exist inside the H. setigerum complex; in the present study, H. tenuissimum belongs to the H. setigerum complex, based on the morphological character of long septocystidia and phylogenetic evidence. A previous study indicated the importance of vicariance in the evolution of this species complex (Nilsson et al. 2003) and our study shows that the specimens of H. tenuissimum are collected in Zixishan National Forestry Park (GPS co-ordinates 25°01'26"N, 101°24'37"E), Chuxiong, Yunnan Province, China, which is distinct from H. setigerum s. str. (Norway: Oppland and Finland: Pohjois-Häme). The present samples of H. subsetigerum and H. nudicephalum were collected in Yunnan Province, China, but neither of these taxa groups together closely with H. tenuissimum (Fig. 1).

In the current phylogenetic tree, two partially annotated GenBank sequences (KJ668522 and KJ714002) of Hyphoderma sp. (South Korea) cluster closely with four sequences of the new species Hyphoderma tenuissimum, although whether they really belong to this species remains to be assessed. It is certainly conceivable that they do, which would mean that Hyphoderma tenuissimum has been collected and sequenced at least six times in Asia. Regarding the new taxon H. puerense (Fig. 1), four partially annotated GenBank sequences (KR868735, KR868736, KR868737 and DQ340327) form a reasonably well-supported clade together with our two specimens of H. puerense. We interpret this to mean that all six taxa represent H. puerense. All of the samples in this clade are from Asia, which supports the point of the importance of vicariance in the evolution in this genus.

Key to 30 accepted species of Hyphoderma in China

1 Cystidia absent 2
Cystidia present 5
2 Hymenial surface grandinioid H. acystidiatum
Hymenial surface smooth 3
3 Basidiospores > 10.5 µm in length H. densum
Basidiospores < 10.5 µm in length 4
4 Hymenophore cracked; basidiospores > 8.5 µm in length H. fissuratum
Hymenophore uncracked; basidiospores < 8.5 µm in length H. sibiricum
5 Hymenophore smooth 6
Hymenophore tuberculate, porulose, grandinioid or odontoid 15
6 Two types of cystidia present 7
One type of cystidia present 8
7 Moniliform cystidia absent H. microcystidium
Moniliform cystidia present H. sinense
8 Hymenophore uncracked 9
Hymenophore cracked 11
9 Basidiospores > 11 µm in length H. definitum
Basidiospores < 11 µm in length 10
10 Basidiospores > 8.5 µm in length H. microporoides
Basidiospores < 8.5 µm in length H. puerense
11 Cystidia moniliform 12
Cystidia cylindrical 13
12 Basidiospores > 9 µm in length H. litschaueri
Basidiospores < 9 µm in length H. moniliforme
13 Basidiospores ellipsoid < 10 μm in length H. rimulosum
Basidiospores cylindrical > 10 μm in length 14
14 Basidiospores > 12 µm in length H. cremeum
Basidiospores < 12 µm in length H. subclavatum
15 Hymenophore odontoid or grandinioid 16
Hymenophore tuberculate, porulose 19
16 Hymenophore odontoid 17
Hymenophore grandinioid 18
17 Basidiospores < 4.5 µm in width H. transiens
Basidiospores > 4.5 µm in width H. formosanum
18 Basidiospores larger 7–10.5 × 3–4.5 µm H. tenuissimum
Basidiospores smaller 6–8 × 2.8–3.2 μm H. subsetigerum
19 Cystidia of two types 20
Cystidia of one type 23
20 Septate cystidia absent 21
Septate cystidia present 22
21 Basidiospores < 4 µm in width H. variolosum
Basidiospores > 4 µm in width H. crystallinum
22 Basidia 2-sterigmata, basidiospores > 13 µm in length H. pinicola
Basidia 4-sterigmata, basidiospores < 13 µm in length H. floccosum
23 Septate cystidia present 24
Septate cystidia absent 25
24 Hymenophore porulose to pilose, basidia < 5 µm in width H. mopanshanense
Hymenophore tuberculate, basidia > 5 µm in width H. setigerum
25 Hymenophore porulose H. obtusiforme
Hymenophore tuberculate, colliculose 26
26 Cystidia < 30 µm in length H. cremeoalbum
Cystidia > 30 µm in length 27
27 Basidia > 30 µm in length 28
Basidia < 30 µm in length 29
28 Hymenophore cracking, cystidia < 10 µm in width H. medioburiense
Hymenophore not cracking, cystidia > 10 µm in width H. clavatum
29 Hymenophore colliculose H. nemorale
Hymenophore tuberculate H. membranaceum

Acknowledgements

The research was supported by the Yunnan Fundamental Research Project (Grant No. 202001AS070043) and Science Research Foundation of Yunnan Provincial Department of Education Project (Project No. 2021Y275).

References

  • Baltazar JM, Silveira RMB, Rajchenberg M (2016) Type studies of J. Rick’s corticioid homobasidiomycetes (Agaricomycetes, Basidiomycota) housed in the Herbarium Anchieta (PACA). Phytotaxa 255(2): 101–132. https://doi.org/10.11646/phytotaxa.255.2.1
  • Bernicchia A, Gorjón SP (2010) Fungi Europaei 12: Corticiaceae s.l. Alassio: Edizioni Candusso.
  • Donk MA (1957) Notes on resupinate Hymenomycetes IV. Fungus 27: 1–29.
  • Eriksson J (1958) Studies in the Heterobasidiomycetes and HomobasidiomycetesAphyllophorales of Muddus National Park in North Sweden. Symbolae Botanicae Upsalienses 16(1): 1–172.
  • Eriksson J, Ryvarden L (1975) The Corticiaceae of North Europe; Fungiflora: Oslo, Norway, Volume 3, 288–546.
  • Floudas D, Hibbett DS (2015) Revisiting the taxonomy of Phanerochaete (Polyporales, Basidiomycota) using a four gene dataset and extensive ITS sampling. Fungal Biology 119(80): 679–719. https://doi.org/10.1016/j.funbio.2015.04.003
  • Gilbertson RL, Blackwell M (1988) Some new or unusual corticioid fungi from the Gulf Coast region. Mycotaxon 33: 375–386.
  • Guan QX, Zhao CL (2021a) Taxonomy and phylogeny of the wood-inhabiting fungal genus Hyphoderma with descriptions of three new species from East Asia. Journal of Fungi 7(4): e308. https://doi.org/10.3390/jof7040308
  • Jang Y, Jang S, Min M, Hong JH, Lee H, Lee H, Lim YW, Kim JJ (2015) Comparison of the diversity of basidiomycetes from dead wood of the Manchurian fir (Abies holophylla) as evaluated by fruiting body collection, mycelial isolation, and 454 sequencing. Microbial Ecology 70(3): 634–645. https://doi.org/10.1007/s00248-015-0616-5
  • Justo A, Miettinen O, Floudas D, Ortiz-Santana B, Sjökvist E, Linder D, Nakasone K, Niemelä T, Larsson K, Ryvarden L, Hibbetta DS (2017) A revised family-level classification of the Polyporales (Basidiomycota). Fungal Biology 121(9): 798–824. https://doi.org/10.1016/j.funbio.2017.05.010
  • Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20(4): 1160–1166. https://doi.org/10.1093/bib/bbx108
  • Martín MP, Zhang LF, Fernández-López J, Dueñas M, Rodríguez-Armas JL, Beltrán-Tejera E, Telleria MT (2018) Hyphoderma paramacaronesicum sp. nov. (Meruliaceae, Polyporales, Basidiomycota), a cryptic lineage to H. macaronesicum. Fungal Systematics and Evolution 2: 57–68. https://doi.org/10.3114/fuse.2018.02.05
  • Miller MA, Pfeiffer W, Schwartz T (2012) The CIPRES Science Gateway: enabling high-impact science for phylogenetics researchers with limited resources. Association for Computing Machinery 39: 1–8. https://doi.org/10.1145/2335755.2335836
  • Nilsson RH, Hallenberg N, Nordén B, Maekawa N, Wu SH (2003) Phylogeography of Hyphoderma setigerum (Basidiomycota) in the Northern Hemisphere. Mycological Research 107(6): 645–652. https://doi.org/10.1017/S0953756203007925
  • Nylander JAA (2004) MrModeltest v.2. Program Distributed by the Author. Evolutionary Biology Centre, Uppsala University, Uppsala.
  • Petersen JH (1996) The Danish Mycological Society’s colour-chart. Foreningen til Svampekundskabens Fremme, Greve.
  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029
  • Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R, Ruiz LV, Vasco-Palacios AM, Thu PQ, Suija A, Smith ME, Sharp C, Saluveer E, Saitta A, Rosas M, Riit T, Ratkowsky D, Pritsch K, Põldmaa K, Piepenbring M, Phosri C, Peterson M, Parts K, Pärtel K, Otsing E, Nouhra E, Njouonkou AL, Nilsson RH, Morgado LN, Mayor J, May TW, Majuakim L, Lodge DJ, Lee SS, Larsson K-H, Kohout P, Hosaka K, Hiiesalu I, Henkel TW, Harend H, Guo L-d, Greslebin A, Grelet G, Geml J, Gates G, Dunstan W, Dunk C, Drenkhan R, Dearnaley J, De Kesel A, Dang T, Chen X, Buegger F, Brearley FQ, Bonito G, Anslan S, Abelland S, Abarenkov K (2014) Global diversity and geography of soil fungi. Science 346: 1256688. https://doi.org/10.1126/science.1256688
  • Telleria MT, Dueñas M, Beltrán-Tejera E, Rodríguez-Armas JL, Martín MP (2012) A new species of Hyphoderma (Meruliaceae, Polyporales) and its discrimination from closely related taxa. Mycologia 104(5): 1121–1132. https://doi.org/10.3852/11-344
  • Telleria MT, Duenas M, Melo I, Hallenberg N, Martin MP (2010) A re-evaluation of Hypochnicium (Polyporales) based on morphological and molecular characters. Mycologia 102(6): 1426–1436. https://doi.org/10.3852/09-242
  • Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172(8): 4238–4246.
  • Vu D, Groenewald M, Vries M, Gehrmann T, Stielow B, Eberhardt U, Al-Hatmi A, Groenewald JZ, Cardinali G, Houbraken J, Boekhout T, Crous PW, Robert V, Verkley GJM (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom Fungi and reveals thresholds for fungal species and higher taxon delimitation. Studies in Mycology 92: 135–154. https://doi.org/10.1016/j.simyco.2018.05.001
  • Wallroth CFW (1833) Flora Cryptogamica Germaniae 2 Algas et fungos. Norimbergae [Nüremberg], Schragius [J.L. Schrag], 923 pp.
  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gefand DH, Sninsky JJ, White JT (Eds) PCR Protocols: A Guide to Methods and Applications. Academic Press, San Diego, 18: 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
  • Wu F, Chen JJ, Ji XH, Vlasák J, Dai YC (2017) Phylogeny and diversity of the morphologically similar polypore genera Rigidoporus, Physisporinus, Oxyporus and Leucophellinus. Mycologia 109(5): 749–765. doi: 10.1080/00275514.2017.1405215
  • Wu SH, Nilsson HR, Chen CT, Yu SY, Hallenberg N (2010) The white-rotting genus Phanerochaete is polyphyletic and distributed throughout the phlebioid clade of the Polyporales (Basidiomycota). Fungal Diversity 42(1): 107–118. https://doi.org/10.1007/s13225-010-0031-7
  • Zhao CL, Wu ZQ (2017) Ceriporiopsis kunmingensis sp. nov. (Polyporales, Basidiomycota) evidenced by morphological characters and phylogenetic analysis. Mycological Progress 16(1): 93–100. https://doi.org/10.1007/s11557-016-1259-8