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Research Article
Dendrocorticiopsis orientalis gen. et sp. nov. of the Punctulariaceae (Corticiales, Basidiomycota) revealed by molecular data
expand article infoChia-Ling Wei, Che-Chih Chen§|, Shuang-Hui He, Sheng-Hua Wu§
‡ Department of Biology, National Museum of Natural Science, Taichung, Taiwan
§ National Chung Hsing University, Taichung, Taiwan
| Academia Sinica, Taipei, Taiwan
¶ Beijing Forestry University, Beijing, China
Open Access

Abstract

Dendrocorticiopsis orientalis is presented in this study as a new genus and new species based on morphological and phylogenetic evidence. This new taxon is characterized by resupinate, smooth and membranaceous basidiomata, monomitic hyphal system with clamps, colorless dendrohyphidia, variable presence of cystidia, and ellipsoid to ovoid basidiospores measuring 5–7 × 3.2–5.2 μm. The phylogenetic analyses based on the ITS1-5.8S-ITS2 (ITS) + nuclear 28S rDNA (28S) dataset of Corticiales indicated that the new taxon is nested in Punctulariaceae, separated from other genera with strong support values. Descriptions, specimen photo, and illustrations of the new taxon are provided in this study. A morphological comparison of the four genera of Punctulariaceae is given.

Keywords

Corticioid fungi, East Asia, phylogeny, taxonomy, wood-decaying fungi

Introduction

Corticiales K.H. Larss. is a small order of corticioid fungi with four families: Corticiaceae Herter, Dendrominiaceae Ghobad-Nejhad, Punctulariaceae Donk, and Vuilleminiaceae Maire ex Lotsy. The members of the order show a variety of nutritional ecologies, including lignicolous saprobes, foliicolous species, plant pathogens, and lichenicolous species (Ghobad-Nejhad et al. 2010, 2021). Species of Punctulariaceae are mainly saprobic on angiosperm trees, causing white rot. Morphologically, they are characterized by having effused to effused-reflexed basidiomata, smooth to tuberculate hymenial surface, a monomitic hyphal system with clamped generative hyphae, mostly absence of cystidia, sparsely to regularly branched dendrohyphidia, and ellipsoid to subglobose basidiospores which are negative in Melzer’s reagent and acyanophilous in cotton blue. When Donk (1964) established this family, he adopted Talbot’s suggestion (Talbot 1958) and designated Punctularia Pat. as the type genus. Ghobad-Nejhad et al. (2010) were the first to use a phylogenetic approach to analyze Punctulariaceae, and they recognized three genera, viz., Dendrocorticium M.J. Larsen & Gilb., Punctularia, and Punctulariopsis Ghobad-Nejhad. This arrangement was generally accepted by mycologists (Hibbett et al. 2014; He et al. 2019; Wijayawardene et al. 2020).

Most of the previous studies of Punctulariaceae focused on European species (Bernicchia and Gorjón 2010; Gorjón and Bernicchia 2017), although species from other continents received attention as well (Ghobad-Nejhad et al. 2010; Baltazar et al. 2013; Ariyawansa et al. 2015). However, the study of this family in Asia is insufficient and needs an update (Petch 1916; Cooke 1956; Guan et al. 2021). During surveys of corticioid fungi in East Asian regions, we found an unknown species morphologically similar to Dendrocorticium spp. Phylogenetic analyses were conducted by using ITS+28S sequences to evaluate the generic placement of the target taxon, and the results indicated that it represents a new genus and a new species of the Punctulariaceae.

Materials and methods

Morphological studies

Descriptions and illustrations are based on dried specimens deposited at the herbaria of the National Museum of Natural Science (TNM) and Beijing Forestry University (BJFC). Specimens were sliced into thin sections under stereo microscope (Nikon SMZ645) and mounted in 5% KOH with 1% phloxine in preparation for observations and measurements. Melzer’s reagent (IKI) and cotton blue were applied to detect amyloidity or dextrinoidity, and cyanophily, respectively. Microscopic studies were carried out under 1,000× magnification using an optical microscope (Olympus BX43). For presenting the range of basidiospore dimensions, 5% values of minimum and maximum are given in parentheses.

DNA extraction and sequencing

DNA was extracted from dried specimens using the Plant Genomic DNA Extraction Miniprep System (Viogene Biotek corporation, New Taipei City, Taiwan), following the manufacturer’s protocol. ITS1-5.8S-ITS2 and partial 28S regions were amplified with the primer pairs ITS1/ITS4 (White et al. 1990) and LR0R/LR5 (Vilgalys and Hester 1990). The PCR protocols for ITS and 28S followed Chen et al. (2020). PCR products were purified and sequenced by MB Mission Biotech company (Taipei City, Taiwan). New sequences were assembled and adjusted using BioEdit v7.2.5 (Hall 1999) and subsequently submitted to GenBank (Table 1).

Table 1.

Information of species and strains used in phylogenetic analyses, including their localities, voucher numbers, and GenBank accession numbers (ITS and 28S). Newly generated sequences are shown in bold. Voucher number of holotypes are marked with an asterisk (*).

Species Locality Voucher no. GenBank accession no.
ITS 28S
Australovuilleminia coccinea Ghobad-Nejhad & Hallenb. New Zealand PDD:94158* HM046875 HM046930
Basidiodesertica hydei Oman DST2020a_SQUCC15289* MW077150 MW077159
Corticium roseum China Ghobad-Nejhad 2428 MW805872 MW805836
C. thailandicum Thailand Ghobad-Nejhad 3012 MW805868 MW805831
Cytidia salicina (Fr.) Burt Finland Haikonen 24631 GU590881 HM046921
Dendrocorticiopsis orientalis Sheng H. Wu, C.L. Wei & S.H. He Taiwan WEI 20-166* MW580922 MW580924
D. orientalis Taiwan WEI 20-173 MW580925 MW580927
D. orientalis Taiwan BCRC 36235 EU232219 EU232303
D. orientalis China He 4195 MW580926 MW580921
Dendrocorticium polygonioides (P. Karst.) M.J. Larsen & Gilb. France CBS 106.56 MH857525 MH869062
D. roseocarneum (Schwein.) M.J. Larsen & Gilb. South Korea KUC20121109-32 KJ668559 KJ668413
Dendrominia dryina (Pers.) Ghobad-Nejhad & Duhem France Duhem 5283 JX892936 JX892937
D. ericae (Duhem) Ghobad-Nejhad & Duhem France Duhem 4840* JX892938 JX892939
Disporotrichum dimorphosporum USA CBS 433.85 MH861895 MH873584
D. dimorphosporum Netherlands CBS 419.70* MH859776 MH871538
Erythricium hypnophilum France MG169 MW805858 MW805823
E. laetum Kotiranta 21287 GU590875 GU590878
Gloeophyllum abietinum (Bull.) P. Karst. Switzerland H 22988 JX524619 KC782733
L. fuciformis Netherlands CBS 182.49 MH856485 MH868023
L. roseipellis CBS 299.82 EU622846 EU622844
Lawreymyces palicei Palice 4369* AY542865 AY542865
Lawreymyces palicei Palice 2509 AY542864 AY542864
Marchandiomyces aurantioroseus (P. Karst.) Ghobad-Nejhad Sweden Hallenberg 8186 KP864659 HM046929
M. corallinus JL128-98 AY583327 AY583331
Mycobernardia incrustans France Duhem 3613 MW805860 MW805825
M. incrustans Canada CBS172.36 MH855759 MH867272
Punctularia atropurpurascens (Berk. & Broome) Petch Taiwan WEI 17-662 MW570883 MW570888
P. bambusicola C.L. Zhao China CLZhao 9098* MW559983 MW559985
P. strigosozonata (Schwein.) P.H.B. Talbot HHB-11897-sp DQ398958 AF518642
Punctulariopsis efibulata (M.J. Larsen & Nakasone) Ghobad-Nejhad USA Burdsall 8824* KR494276 KR494277
P. obducens (Hjortstam & Ryvarden) Ghobad-Nejhad Ethiopia Ryvarden 28131 HM046918 HM046933
P. subglobispora (Hallenb. & Hjortstam) Ghobad-Nejhad Argentina Hallenberg 12761* HM046917 HM046932
Veluticeps abietina (Pers.) Hjortstam & Tellería Sweden KHL 12474 EU118619 EU118619
Vuilleminia comedens (Nees) Maire T-583 DQ398959 AF518666
V. coryli Boidin, Lanq. & Gilles Turkmenistan Parmasto 54999 JN387996 JN388005
V. cystidiata Parmasto South Korea KUC20131022-26 KJ668433 KJ668285
V. erastii Ghobad-Nejhad Canada DAOM 199025* JN387998 JN388007
V. macrospora (Bres.) Hjortstam France Duhem 4860 JX892940 JX892941
V. megalospora Bres. Italy Ryvarden 43185 HM046887 HM046926
V. nilsii Ghobad-Nejhad & Duhem France Duhem 4847* JX892947 JX892948
V. pseudocystidiata Boidin, Lanq. & Gilles France Boidin 14838* HM046888 HM046928
Waitea circinata USA CBS472.82 MH861518 MH873265
W. guianensis French Guiana GUY13-110 MW449090 MW449101

Phylogenetic analyses

The selection of species and samples for the ITS+28S dataset was inspired by Ghobad-Nejhad and Duhem (2014) and Guan et al. (2021). The dataset contained 43 samples from 37 species, including 35 ingroup species from 17 genera of the four families in Corticiales and 2 outgroup species from Gloeophyllales [Gloeophyllum abietinum (Bull.) P. Karst. and Veluticeps abietina (Pers.) Hjortstam & Tellería, Table 1]. Sequences were aligned in MAFFT v.7 (Katoh and Standley 2013). Partitioned phylogenetic analyses were carried out for the ITS+28S dataset based on maximum likelihood (ML) and Bayesian inference (BI) methods, using MrBayes v. 3.2.6. (Ronquist et al. 2012) and RaxML Black Box (Stamatakis 2014) at the CIPRES Science Gateway (http://www.phylo.org/). For the BI analysis, jModeltest 2.1.10 (Darriba et al. 2012) was first executed to estimate the best-fit substitution model based on Akaike Information Criterion (AIC). The GTR+G+I was used as the substitution model for the ITS1, ITS2 and 28S regions, while K80 was used for 5.8S region. The parameter settings for ML and BI analyses followed Wu et al. (2018). Only the phylogram inferred from the ML analysis is shown since the BI and ML analyses produced similar topologies. The statistical support values are presented above the branches of the ML tree when bootstrap values (BS) ≥ 70 and BI posterior probability (PP) ≥ 0.9. The complete phylogenetic trees and alignment were submitted to TreeBASE (submission number 29602; www.treebase.org).

Results

Phylogenetic inference

The final alignment of 43 sequences contained 1,647 sites (including gaps) of which 724 sites were from the ITS region and 923 sites from the 28S gene. Totally, 565 (34%) sites were parsimony informative. The ML tree (Fig. 1) shows the four highly supported families also recovered in previous studies (Ghobad-Nejhad and Duhem 2014; Ariyawansa et al. 2015; Ghobad-Nejhad et al. 2021; Guan et al. 2021). The four samples of the new species Dendrocorticiopsis orientalis formed a monophyletic group in Punctulariaceae with strong support values (BS = 100%; PP = 1), well separated from the other genera, viz., Dendrocorticium, Punctularia, and Punctulariopsis (Fig. 1). Therefore, Dendrocorticiopsis is treated as the fourth genus of Punctulariaceae.

Figure 1. 

The phylogram of Corticiales inferred from ML analysis using the combined ITS+28S dataset shows the position of Dendrocorticiopsis orientalis (shown in bold) in Punctulariaceae. Numbers above branches indicate statistical support of BS ≥ 70% and PP ≥ 0.9. Black stars (é) indicate strains of generic species.

Taxonomy

Dendrocorticiopsis Sheng H. Wu, C.L. Wei & S.H. He, gen. nov.

MycoBank No: MycoBank: MB838902

Diagnosis

Dendrocorticiopsis differs from other genera by having strictly resupinate basidiomata, ivory hymenphore, a compact texture, a monomitic hyphal system, nodose-septate hyphae, encrusted cystidia, dendrohyphidia and ellipsoid to ovoid basidiospores.

Description

Basidiomata resupinate, effused, adnate, membranaceous. Hymenial surface brownish ivory, grayish ivory to lilac ivory, smooth. Hyphal system monomitic; generative hyphae nodose-septate, colorless, slightly thick- to thick-walled. Subiculum uniform, with compact texture, usually with crystal masses; hyphae fairly horizontal. Hymenial layer thickening, with compact texture, usually with oily materials, hyphae more or less vertical. Dendrohyphidia numerous, thick-walled toward base, colorless. Cystidia clavate, apically with resinous materials. Basidia clavate to subclavate, 4-sterigmata, thick-walled toward base. Basidiospores ellipsoid to ovoid, sometimes broadly ellipsoid, smooth, thin-walled or occasionally slightly thick-walled, negative in Melzer’s reagent, acyanophilous.

Type species

Dendrocorticiopsis orientalis.

Etymology

Dendrocorticiopsis refers to the morphological resemblance to Dendrocorticium.

Dendrocorticiopsis orientalis Sheng H. Wu, C.L. Wei & S.H. He, sp. nov.

MycoBank No: MycoBank: MB838903
Figs 2, 3

Diagnosis

The noteworthy features of Dendrocorticiopsis orientalis are: (1) subiculum composed of a basal layer, with compact texture; (2) oily materials usually present in hymenial layer; (3) cystidia with resinous materials at apices; (4) shortly clavate to subclavate basidia; (5) ellipsoid to ovoid basidiospores measuring 5–7 × 3.2–5.2 μm.

Figure 2. 

Basidiomata of Dendrocorticiopsis orientalis (holotype, WEI 20-166). Scale bar: 1 cm.

Typification

Taiwan, Taichung City, Heping District, near trailhead of Mt. Tangmadan Trail, 24°09'53.0"N, 120°57'26.4"E, 670 m asl., on dead angiosperm trunk, 20 Aug 2020, leg. C.L. Wei, WEI 20-166 (holotype, TNM F34448). GenBank: ITS = MW580922; 28S = MW580924.

Figure 3. 

Micromorphological features of Dendrocorticiopsis orientalis (holotype, WEI 20-166) A profile of basidioma section B basidioma section C dendrohyphidia D cystidia E basidia F basidiospores. Scale bars: 50 μm (A); 10 μm (B–F).

Etymology

The epithet refers to the Eastern world, where the specimens were collected.

Description

Basidiomata annual, resupinate, effused, adnate, membranaceous, 50–100 μm thick in section. Hymenial surface brownish ivory, grayish ivory to lilac ivory, smooth, finely cracked; margin concolourous, slightly pruinose, rather determinate. Hyphal system monomitic; generative hyphae nodose-septate. Subiculum fairly uniform, composed of a basal layer, with fairly compact texture, usually with crystal masses; up to 30 μm thick, sometimes indistinct; hyphae mainly horizontal, colorless, fairly straight, 3–4 μm diam, with walls slightly thickened up to 1 μm. Hymenial layer thickening, with more or less compact texture, usually with oily materials, 50–70 μm thick; hyphae more or less vertical, colorless, 2–4 μm diam, with walls slightly thickened up to 1 μm. Dendrohyphidia numerous, 12–28 × 2–3 μm, thick-walled toward base, with walls up to 1 μm thick, colorless. Cystidia clavate, apically with resinous materials, gradually dissolving in KOH, 10–20 × 3.5–5.5 μm, slightly thick-walled, or thickening toward base, with walls up to 1 μm thick. Basidia clavate to subclavate, usually broadened at basal or middle parts, 18–35 × 5–7 μm, 4-sterigmata, thickening toward base, with walls up to 1 μm thick. Basidiospores ellipsoid to ovoid, or broadly ellipsoid, smooth, colorless, with homogenous contents, thin-walled or occasionally slightly thick-walled, negative in Melzer’s reagent, acyanophilous, mostly 5–7 × 3.2–5.2 μm. (5.5)6–7(7.5) × 4.2–5.2(5.5) μm, L = 6.50±0.42 μm, W = 4.66±0.32 μm, Q = 1.40 (n = 30) (holotype, WEI 20-166). (5.7)6.2–7(7.5) × (4.2)4.5–5(5.2) μm, L = 6.61±0.43 μm, W = 4.77±0.25 μm, Q = 1.39 (n = 30) (WEI 20-173). (4.2)5–6.8(7) × (3)3.2–5(5.2) μm, L = 5.8 μm, W = 4.2 μm, Q = 1.38 (He 4195).

Habitat

On dead angiosperm wood (e.g., Acacia and Castanopsis), occurring in August.

Distribution

In subtropical regions, known from China: Jiangxi and Taiwan.

Additional specimens examined (paratypes)

China, Jiangxi Province, Yichun City, Yifeng County, Guanshan National Nature Reserve, 500 m asl., on dead Castanopsis wood, 9 Aug 2016, leg. S.H. He, He 4195 (BJFC 023637). Taiwan, Taichung City, Heping District, near trailhead of Mt. Tangmadan Trail, 24°09'53.0"N, 120°57'26.4"E, 670 m asl., on dead angiosperm trunk, 20 Aug 2020 leg. C.L. Wei, WEI 20-173 (TNM F0034449).

Notes

Both of the ITS and 28S sequences BLAST results showed that Dendrocorticiopsis orientalis is close to the strain BCRC 36235 that is annotated as Ganoderma applanatum (Pers.) Pat. in GenBank. According to personal communication with Bioresource Collection and Research Center (BCRC, Taiwan), the strain BCRC 36235 was indeed isolated from a Ganoderma specimen collected by Dr. Jin-Torng Peng in Nantou, Central Taiwan, on wood of Acacia confusa Merr. However, as suggested by Suldbold (2017), the ITS (EU232219) and 28S (EU232303) sequences of the strain BCRC 36235 are not true G. applanatum, and we supposed that the strain could be contaminated by D. orientalis, which is known to grow on Acacia. The specimen He 4195 collected on Castanopsis (Fagaceae) from Jiangxi Province has slightly smaller basidiospores (L = 5.8 μm, W = 4.2 μm) than the holotype.

Discussion

A comparison of morphological characteristics for distinguishing the four genera in Punctulariaceae is provided in Table 2. Dendrocorticiopsis is morphologically similar to Dendrocorticium, however, the latter has longer and narrowly clavate to tubular basidia usually longer than 45 μm, whereas Dendrocorticiopsis has clavate to subclavate basidia shorter than 35 μm. Punctularia differs from Dendrocorticiopsis by having resupinate or effused-reflexed basidiomata with a tuberculate hymenophore, colored dendrohyphidia, and through its lack of cystidia, while Punctulariopsis can be distinguished from Dendrocorticiopsis by possessing longer basidia and basidiospores, and mostly lacking cystidia.

Table 2.

Morphological characteristics used for distinguishing the four genera in Punctulariaceae.

Dendrocorticiopsis Dendrocorticium Punctularia Punctulariopsis
basidiomata resupinate resupinate or effused-reflexed resupinate or effused-reflexed resupinate
hymenial surface smooth smooth tuberculate smooth
dendrohyphidia colourless mostly colourless (yellowish in D. roseolum); some species with encrustations yellowish to brown or pink to rose colourless
cystidia clavate, apically with resinous materials mostly absent (D. roseolum with halocystidia; D. piceinum with leptocystidia) absent mostly absent (P. obducens with leptocystidia)
basidia clavate to subclavate; < 35 μm long narrowly clavate to tubular; mostly > 45 μm long narrowly clavate to tubular; 35–45 μm long narrowly clavate to tubular; > 45 μm long
basidiospores ellipsoid to ovoid; < 10 μm long broadly ellipsoid to subglobose; usually < 10 μm long ellipsoid; < 10 μm long broadly ellipsoid to subglobose; > 10 μm long
distributions subtropical regions temperate or tropical regions tropical to subtropical regions tropical to subtropical regions

Dendrocorticium violaceum H.S. Jacks. ex M.J. Larsen & Gilb. and D. polygonioides (P. Karst.) M.J. Larsen & Gilb. have similar-sized basidiospores to Dendrocorticiopsis orientalis [4–6.5 × 3–5 μm in D. violaceum, 6–9 × 4–6 μm in D. polygonioides (Larsen and Gilbertson 1977)]. However, D. violaceum is distributed in Canada, has a reflexed basidiomata margin (closely adnate in Dendrocorticiopsis orientalis), and grows mainly on deciduous wood. Dendrocorticium polygonioides is mainly distributed in Europe and has a whitish to violaceous surface, large basidia (50–60 × 5–7 μm), and usually encrusted dendrohyphidia (Larsen and Gilbertson 1977).

Acknowledgements

This study was supported by a Grant-in-Aid for Scientific Research (no. 109-08.1-SB-18) from the Council of Agriculture, Executive Yuan, ROC and the National Natural Science Foundation of China (No. 31750001). We are grateful to Miss Shin-Yi Ke for DNA extraction and PCR works, and to Miss Siou-Zhen Chen for managing studied specimens.

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Supplementary material

Supplementary material 1 

Alignments to TreeBase

Chia-Ling Wei, Che-Chih Chen, Shuang-Hui He, Sheng-Hua Wu

Data type: Alignments (fas. file)

Explanation note: We have uploaded the alignments to TreeBase and here is the link and the file. http://purl.org/phylo/treebase/phylows/study/TB2:S29602?x-access-code=cdd27042a420e43e26dd8e62ea382799&format=html.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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