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Article

The Morphological Characteristics and Phylogenetic Analyses Revealed an Additional Taxon in Heteroradulum (Auriculariales)

by
Jia-Jin Li
1,2,3,
Chang-Lin Zhao
1,2,4,5,* and
Chao-Mao Liu
2,*
1
Laboratory for Forest Resources Conservation and Utilization in the Southwest Mountains of China, Ministry of Education, Southwest Forestry University, Kunming 650224, China
2
College of Biodiversity Conservation, Southwest Forestry University, Kunming 650224, China
3
Yunnan Academy of Biodiversity, Southwest Forestry University, Kunming 650224, China
4
Yunnan Key Laboratory for Fungal Diversity and Green Development, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China
5
School of Life Sciences, Tsinghua University, Beijing 100084, China
*
Authors to whom correspondence should be addressed.
Diversity 2022, 14(1), 40; https://doi.org/10.3390/d14010040
Submission received: 23 November 2021 / Revised: 30 December 2021 / Accepted: 5 January 2022 / Published: 9 January 2022
(This article belongs to the Special Issue Diversity and Evolution of Fungi)
Browse Figures
Versions Notes

Abstract

:
Auriculariales is diverse, embracing a number of corticioid, poroid, and hydnoid genera. The present study covers a new wood-inhabiting fungal species of Heteroradulum niveum sp. nov that is proposed on the basis of a combination of morphological features and molecular evidence. The species is characterized by the resupinate basidiomata, a monomitic hyphal system with generative hyphae with clamp connections; tubular cystidia; two- to four-celled basidia; and allantoid, colorless, thin-walled, smooth, IKI–, CB–, basidiospores (6.5–13.5 × 2.7–5.5 µm). Sequences of ITS and nLSU rRNA gene regions of the specimens were generated, and phylogenetic analyses were carried out with methods of maximum parsimony, maximum likelihood, and Bayesian inference. These phylogenetic analyses inferred from ITS+nLSU indicated that H. niveum is nested in Heteroradulum within Auriculariales. Further study within Heteroradulum on the basis of ITS+nLSU dataset revealed that it formed a monophyletic lineage with a strong support (100% BS, 100% BP, 1.00 BPP) and then grouped with H. yunnanensis.

1. Introduction

The Auriculariales is a characteristic order of Agaricomycetes (Basidiomycota), in which it has been introduced to embrace a number of corticioid, poroid, and hydnoid genera on the basis of a result of morphological, phylogenetic, and cytological studies [1,2,3]. The Auriculariales are wood decomposers inhabiting various hosts, from the tropics to the subarctic zone, in which some of them are able to survive under extreme climatic conditions [4]. Currently, the delimitation of Auriculariales has been principally based on the characteristics observed under optical and electron microscopy and supports by molecular analyses [5].
Heteroradulum Lloyd ex Spirin & Malysheva was typified by H. kmetii (Bres.) Spirin & Malysheva [4], which is characterized by a combination of annual or perennial, resupinate, or effused-reflexed basidiomata with a leathery consistency; hymenophore smooth to odontioid; a monomitic hyphal structure (rare dimitic) with clamp connections on generative hyphae; and the presence of cystidia, basidia narrowly ovoid to obconical, longitudinally septate with a well-developed enucleate stalk and basidiospores hyaline, thin-walled, smooth, cylindrical, acyanophilous, and negative in Melzer’s reagent [4]. Currently, seven species have been accepted in Heteroradulum worldwide [4,6,7,8,9,10,11].
The molecular systematics involving Heteroradulum based on the internal transcribed spacer (ITS) regions and the large subunit nuclear ribosomal RNA gene (nLSU) sequences revealed that the taxonomy and phylogeny of the Auriculariales with stereoid basidiocarps were employed, in which H. adnatum Spirin & Malysheva and H. semis Spirin & Malysheva were described as new taxa [4]. The genus Protohydnum A. Möller [12] was revised, which showed that Heteroradulum grouped with Exidiopsis (Bref.) Möller [13] and Tremellochaete Raitv [14]. Phylogenetic analyses based on ITS+nLSU DNA sequence data indicated that Heteroradulum belonged to Auriculariaceae, which showed that Heteroradulum was to be related to Grammatus H.S. Yuan & C. Decock [15]. Sequences of ITS and LSU nrRNA gene regions of the studied samples were generated, which showed that H. yunnanensis C.L. Zhao formed a monophyletic lineage with a strong support and then grouped with H. adnatum [11].
In the present study, we collected the material supposedly belonging to an undescribed species of corticioid fungi from Yunnan Province, P.R. China. We present morphological and molecular phylogenetic evidence that supports the recognition of a new species within the Heteroradulum, on the basis of the internal transcribed spacer (ITS) region nLSU sequences.

2. Materials and Methods

2.1. Morphological Studies

The studied specimens are deposited at the herbarium of Southwest Forestry University (SWFC), Yunnan Province, China. Macromorphological descriptions are based on photos captured in the field and lab and field notes. Color terminology follow Petersen [16]. Micromorphological data were obtained from the dried specimens and observed under a light microscope following Dai [17]. The following abbreviations were used: KOH = 5% potassium hydroxide water solution, CB– = acyanophilous, CB = Cotton Blue, IKI– = both inamyloid and indextrinoid, IKI = Melzer’s reagent, 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, n = a/b (number of spores (a) measured from given number (b) of specimens).

2.2. Molecular Methods

CTAB rapid plant genome extraction kit-DN14 (Aidlab Biotechnologies Co., Ltd., Beijing, China) was used to obtain genomic DNA from dried specimens, according to the manufacturer’s instructions followed previous study [18]. ITS region was amplified with primer pair ITS5 and ITS4 [19]. Nuclear LSU region was amplified with primer pair LR0R and LR7 (http://lutzonilab.org/nuclear-ribosomal-dna/; accessed on 5 January 2022). The PCR procedure for ITS and nLSU followed previous study [18]. All newly generated sequences in the present study were deposited in NCBI GenBank (Table 1).
Sequences were aligned in MAFFT 7 (https://mafft.cbrc.jp/alignment/server/; accessed on 5 January 2022) using G-INS-i strategy for ITS+nLSU datasets, and manually adjusted in BioEdit [25]. Aligned dataset was deposited in TreeBase (submission ID 28346). Sistotrema brinkmannii (Bres.) J. Erikss. and Bjerkandera adusta (Willd.) P. Karst. were selected as an outgroup for phylogenetic analyses of ITS+nLSU dataset following a previous study [26] (Figure 1); Exidiopsis effusa (Bref. ex Sacc.) Möller and Tremellochaete japonica (Lloyd) Raitv [14] obtained from GenBank were used as an outgroup to root trees following Guan et al. [11] in the ITS+nLSU analysis (Figure 2).
Maximum parsimony analysis was applied to two combined ITS+nLSU datasets. Its approaches followed Zhao and Wu [18], and the tree construction procedure was performed in PAUP* version 4.0b10 [27]. 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 1000 random sequence additions. Max-trees were set to 5000, branches of zero length were collapsed, and all parsimonious trees were saved. Clade robustness was assessed using bootstrap (BT) analysis with 1000 replicates [28]. Descriptive tree statistics: tree length (TL), consistency index (CI), retention index (RI), rescaled consistency index (RC), and homoplasy index (HI) were calculated for each maximum parsimonious tree generated on the basis of PAUP* version 4.0b10 [27]. Datamatrix was also analyzed using maximum likelihood (ML) approach with RAxML-HPC2 through the Cipres Science Gateway (www.phylo.org, accessed on 5 January 2022) [29]. Branch support (BS) for ML analysis was determined by 1000 bootstrap replicates.
MrModeltest 2.3 [30] was used to determine the best-fit evolution model for each dataset for Bayesian inference (BI). The soft of MrBayes 3.1.2 was calculated for BI [31]. Four Markov chains were run for 2 runs from random starting trees for 1.1 million generations for ITS+nLSU (Figure 1), or for 0.25 million generations for ITS+nLSU (Figure 2). The first quarter of all generations was discarded as burn-in. The majority rule consensus tree of all remaining trees was calculated.

3. Results

3.1. Molecular Phylogeny

The dataset of ITS+nLSU included sequences from 24 fungal specimens representing 22 species (Figure 1). The dataset includes 1922 characters an aligned for the length, of which 1350 characters are constant, 410 are parsimony-informative, and 309 are variable and parsimony-uninformative. Maximum parsimony analysis yielded one equally parsimonious tree (TL = 1922, CI = 0.5723, RI = 0.4207, HI = 0.4277, RC = 0.2408). The best model for the dataset of ITS+nLSU estimated and applied in the Bayesian analysis was GTR+I+G (lset nst = 6, prset statefreqpr = dirichlet (1,1,1,1), rates = invgamma). ML analysis and Bayesian analysis resulted in a similar topology to MP analysis, and Bayesian analysis has an average standard deviation of split frequencies = 0.008747 (BI), and the effective sample size (ESS) across the two runs was the double of the average ESS (avg ESS) = 1108. The phylogram based on ITS+nLSU sequences (Figure 1) demonstrated that the new taxon clustered into genus Heteroradulum and formed a well-supported lineage within Auriculariales.
As shown in Figure 2, the ITS+nLSU dataset included 22 fungal specimens representing 7 species. The dataset had an aligned length of 1967 characters, of which 1724 characters are constant, 159 are parsimony-informative, and 84 are variable and parsimony-uninformative. Maximum parsimony analysis yielded 42 equally parsimonious trees (TL = 412, HI = 0.2694, RI = 0.8490, CI = 0.7306, RC = 0.6202). The best model for the ITS+nLSU dataset estimated and applied in the Bayesian analysis was GTR+I+G (lset nst = 6, rates = invgamma; prset statefreqpr = dirichlet (1,1,1,1)). ML analysis and Bayesian analysis resulted in a similar topology to MP analysis, Bayesian analysis had an average standard deviation of split frequencies = 0.009184 (BI), and the effective sample size (ESS) across the two runs was double the average ESS (avg ESS) = 247. The phylogenetic tree (Figure 2) inferred from ITS+nLSU sequences revealed that Heteroradulum niveum sp. nov. formed a monophyletic lineage with high supports of 100% BS, 100% BP, and 1.00 BPP, and then grouped with H. yunnanensis.

3.2. Taxonomy

Heteroradulum niveum J.J. Li & C.L. Zhao sp. nov. Figure 3 and Figure 4.
MycoBank no.: 841986
Holotype—China. Yunnan Province, Wenshan, Pingba Town, Wenshan National Nature Reserve, 104.25° E, 23.37° N, 2195.6 m asl., on the fallen angiosperm branch, on the broad-leaved forest, mainly with oak, leg. C.L. Zhao, 25 July 2019, CLZhao 16280 (SWFC).
Etymology—niveum (Lat.): referring to the white hymenial surface of type specimens.
Fruiting body—Basidiomata annual, resupinate, leathery, without odor or taste when fresh, becoming membranaceous upon drying, up to 15 cm long, 4 cm wide, 100–200 µm thick. Hymenial surface smooth, white when fresh, becoming white to slightly cream upon drying, older basidiomata with more or less pronounced black stains. Sterile margin white.
Hyphal system—Monomitic, generative hyphae with clamp connections, IKI–, CB–; tissues unchanged in KOH; subiculum indistinct; hymenium thicken, generative hyphae colorless, thin-walled, unbranched, more or less interwoven, 2.5–4 µm in diameter.
Hymenium—Cystidia tubular, 15–34 × 2.5–7 µm; basidia narrowly ovoid to obconical, longitudinally septate, two- to four-celled, embedded, with a well-developed enucleate stalk, 9–19 × 8–15 µm.
Spores—Basidiospores allantoid, colorless, smooth, thin-walled, IKI–, CB–, (6.2–)6.5–13.5(–14) × (2.5)2.7–5.5(–5.8) µm, L = 10.02 µm, W = 4.38 µm, Q = 2.1–2.4 (n = 150/5).
Additional specimens examined—China. Yunnan Province, Wenshan, Xichou County, Xiaoqiaogou, Wenshan National Nature Reserve, 104.46° E, 23.22° N, 1541.5 m asl., on the fallen angiosperm branch, leg. C.L. Zhao, 16 January 2019, CLZhao 11204 (SWFC 011204), CLZhao 11210 (SWFC 011210); Pingba Town, Wenshan National Nature Reserve, 104.25° E, 23.37° N, 2195.6 m asl., on the fallen angiosperm branch, leg. C.L. Zhao, 25 July 2019, CLZhao 16260 (SWFC 016260); 26 July 2019, CLZhao 16398 (SWFC 016398), CLZhao 16424 (SWFC 016424), CLZhao 16432 (SWFC 016432), CLZhao 16472 (SWFC 016472); on the angiosperm trunk, leg. C.L. Zhao, 26 July 2019, CLZhao 16483 (SWFC 016483).

4. Discussion

In the present study, a new species, Heteroradulum niveum, is described on the basis of phylogenetic analyses and morphological characters.
Phylogenetically, Alvarenga and Gibertoni [5] employed the phylogenetic reconstruction using ITS+nLSU topology in the lineages of Auriculariales, showing that Heteroradulum grouped closely with Adustochaete Alvarenga & K.H. Larss., Amphistereum Spirin & Malysheva, and Exidiopsis (Bref.) Möller. In the present study, the new species formed a monophyletic lineage with high supports of 100% BS, 100% BP, and 1.00 BPP and then grouped with H. yunnanensis. However, morphologically, H. yunnanensis differs from H. niveum by its odontoid hymenial surface (50–100 μm long) and larger basidiospores (17–24 × 5–8 µm) [11].
Morphologically, Heteroradulum niveum is similar to H. adnatum on the basis of presence of the white hymenial surface. However, H. adnatum differs from H. niveum by having the hydnoid hymenophore and wider basidiospores (11.4–14.2 × 5.2–7.2 µm) [4].
Heteroradulum niveum is reminiscent of two species of Heteroradulum, H. deglubens and H. kmetii, on the basis of the character by the smooth hymenophore, but H. deglubens differs from H. niveum by having a greyish pink hymenial surface with reddish tints and larger basidiospores (13.1–19.8 × 6.1–8.1 µm) [4], whereas H. kmetii differs in its perennial, pileal basidiomata; pinkish or reddish hymenial surface; and larger basidiospores (14.3–22.3 × 6–9.2 µm) [4].
Heteroradulum niveum shares the similar characteristics of the allantoid basidiospores with H. lividofuscum. However, H. lividofuscum differs from H. niveum by having the hydnoid hymenophore, a dimitic hyphal structure, the presence of abundant gloeocystidia, and larger basidiospores (17.6–23.1 × 7.3–9 µm) [4].
On the basis of biogeography of Heteroradulum (Figure 5), the species is mainly distributed in Europe, such as in Austria, Russia, France, Germany, Poland, the United Kingdom, the Netherlands, Portugal, Sweden, Italy, Denmark, Norway, Finland, and Spain [32]. On the other hand, H. adnatum has been found in Mexico, H. brasiliense has been found in Brazil, H. spinolosum has been found in North America, and H. yunnanensis was discovered as a new species by Guan et al. in China [4,11].
In addition, the results of BLAST queries in NCBI based on ITS and nLSU separately showed the sequences producing significant alignment descriptions: in ITS BLAST results, the top 10 records for Heteroradulum yunnanensis (maximum record descriptions: max score 765; total score 765; query cover 95%; E value 0; ident 90.39%), Exidiopsis calcea (maximum record descriptions: max score 769; total score 769; query cover 85%; E value 0; ident 93.49%), Adustochaete rava (maximum record descriptions: max score 745; total score 745; query cover 93%; E value 0; ident 90.07%), Sebacina filicicola (maximum record descriptions: max score 713; total score 713; query cover 97%; E value 0; ident 89.10%), and E. grisea (maximum record descriptions: max score 699; total score 699; query cover 71%; E value 0; ident 96.25%). In nLSU BLAST results, the top 10 records for H. yunnanensis (maximum record descriptions: max score 2457; total score 2457; query cover 99%; E value 0; ident 99.19%), Auricularia fuscosuccinea (maximum record descriptions: max score 2377; total score 2377; query cover 98%; E value 0; ident 98.17%), and A. subglabra (maximum record descriptions: max score 2375; total score 2375; query cover 99%; E value 0; ident 97.96%).
Wood-rotting fungi are an extensively studied group of Basidiomycota [17,32,33,34], but Chinese wood-rotting fungal diversity is still not well known, especially in the subtropics and tropics. Many recently described taxa of fungi are from subtropical and tropical areas [17,35,36,37,38]. The new species presented in the current study is also from the subtropics. It is possible that new taxa will be found after further investigations and molecular analyses.

Author Contributions

Conceptualization, C.-L.Z.; methodology, C.-L.Z. and J.-J.L.; software, C.-L.Z., C.-M.L. and J.-J.L.; validation, C.-L.Z. and J.-J.L.; formal analysis, C.-L.Z. and J.-J.L.; investigation, C.-L.Z. and C.-M.L.; resources, C.-L.Z. and C.-M.L.; writing—original draft preparation, C.-L.Z. and J.-J.L.; writing—review and editing, C.-L.Z. and J.-J.L.; visualization, C.-L.Z. and J.-J.L.; supervision, C.-L.Z.; project administration, C.-L.Z.; funding acquisition, C.-L.Z. All authors have read and agreed to the published version of the manuscript.

Funding

The research was supported by the National Natural Science Foundation of China (Project No. 32170004, U2102220) for Chang-Lin Zhao and Yunnan Fundamental Research Project (grant no. 202001AS070043) for Chang-Lin Zhao, and received support from the Yunnan Academy of Biodiversity, Southwest Forestry University.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Publicly available datasets were analyzed in this study. This data can be found here: (https://www.mycobank.org/page/Simple%20names%20search; http://purl.org/phylo/treebase, submission ID 28346; accessed on 5 June 2021).

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Maximum parsimony strict consensus tree illustrating the phylogeny of Heteroradulum niveum and related species in Auriculariaceae based on ITS+nLSU sequences. Branches are labeled with maximum likelihood bootstrap higher than 70%, parsimony bootstrap proportions higher than 50%, and Bayesian posterior probabilities more than 0.95.
Figure 1. Maximum parsimony strict consensus tree illustrating the phylogeny of Heteroradulum niveum and related species in Auriculariaceae based on ITS+nLSU sequences. Branches are labeled with maximum likelihood bootstrap higher than 70%, parsimony bootstrap proportions higher than 50%, and Bayesian posterior probabilities more than 0.95.
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Figure 2. Maximum parsimony strict consensus tree illustrating the phylogeny of Heteroradulum niveum and related species in genus Heteroradulum on the basis of ITS+nLSU sequences. Branches are labeled with maximum likelihood bootstrap higher than 70%, parsimony bootstrap proportions higher than 50%, and Bayesian posterior probabilities more than 0.95.
Figure 2. Maximum parsimony strict consensus tree illustrating the phylogeny of Heteroradulum niveum and related species in genus Heteroradulum on the basis of ITS+nLSU sequences. Branches are labeled with maximum likelihood bootstrap higher than 70%, parsimony bootstrap proportions higher than 50%, and Bayesian posterior probabilities more than 0.95.
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Figure 3. Basidiomata of Heteroradulum niveum. Bars: (A) = 1 cm; (B) = 2 mm (holotype).
Figure 3. Basidiomata of Heteroradulum niveum. Bars: (A) = 1 cm; (B) = 2 mm (holotype).
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Figure 4. Microscopic structures of Heteroradulum niveum (holotype): basidiospores (A); basidia and basidioles (B); cystidia (C); A section of hymenium (D). Bars: (A–D) = 10 µm.
Figure 4. Microscopic structures of Heteroradulum niveum (holotype): basidiospores (A); basidia and basidioles (B); cystidia (C); A section of hymenium (D). Bars: (A–D) = 10 µm.
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Figure 5. Geographic distribution of Heteroradulum species worldwide.
Figure 5. Geographic distribution of Heteroradulum species worldwide.
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Table
Table 1. List of species, samples, and GenBank numbers of sequences employed in present study.
Table 1. List of species, samples, and GenBank numbers of sequences employed in present study.
Species NameSample No.GenBank Accession No.ReferencesCountry
ITSnLSU
Amphistereum leveilleanumFP 106715KX262119 [4]Russia
KX262168[4]USA
A. schrenkiiHHB 8476KX262130KX262178[4]USA
Auricularia americanaCui 11509KT152094KT152110[20]China
A. auricula-judaeMW 446AF291268AF291289[20]Germany
Basidiodendron eyreiTUFC 14484AB871753AB871734[4]Japan
Bjerkandera adustaHHB-12826-SpKP134983KP135198[21]North America
Ductifera sucinaKW 3886AY509551AY509551[22]New Zealand
Eichleriella alliciensHHB 7194KX262120KX262169[4]USA
E. bactrianaTAAM 104431KY262138KY262186[4]Germany
Elmerina caryaeDai 5215JQ764654JQ764633[23]Italy
E. cladophoraWei 5621JQ764659JQ764634[23]China
Exidia glandulosaMW 355AF291273AF291319[24]Germany
E. pithyaMW 313AF291275AF291321[24]Germany
Exidiopsis effusaOM 19136KX262145KX262193[4]Finland
Heteroradulum adnatumLR 23453KX262116KX262165[4]Mexico
H. deglubensTAAM 064782KX262101KX262148[4]Russia
H. niveumCLZhao 11204MZ352947MZ352932this studyChina
H. niveumCLZhao 11210MZ352948MZ352933this studyChina
H. niveumCLZhao 16260MZ352940MZ352934this studyChina
H. niveumCLZhao 16280MZ352941MZ352935this studyChina
H. niveumCLZhao 16398MZ352942MZ352936this studyChina
H. niveumCLZhao 16424MZ352943MZ352937this studyChina
H. niveumCLZhao 16432MZ352944 this studyChina
H. niveumCLZhao 16472MZ352945MZ352938this studyChina
H. niveumCLZhao 16483MZ352946MZ352939this studyChina
H. yunnanensisCLZhao 4023MT215564MT215568[11]China
H. yunnanensisCLZhao 8106MT215565MT215569[11]China
H. yunnanensisCLZhao 9132MT215566MT215570[11]China
H. yunnanensisCLZhao 9200MT215567MT215571[11]China
Sclerotrema griseobrunneumVS 7674KX262140KX262188[4]Russia
Sistotrema brinkmanniiIsolate 236JX535169JX535170[4]Russia
Tremellochaete japonicaLE 303446KX262110KX262160[4]Russia
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Li, J.-J.; Zhao, C.-L.; Liu, C.-M. The Morphological Characteristics and Phylogenetic Analyses Revealed an Additional Taxon in Heteroradulum (Auriculariales). Diversity 2022, 14, 40. https://doi.org/10.3390/d14010040

AMA Style

Li J-J, Zhao C-L, Liu C-M. The Morphological Characteristics and Phylogenetic Analyses Revealed an Additional Taxon in Heteroradulum (Auriculariales). Diversity. 2022; 14(1):40. https://doi.org/10.3390/d14010040

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Li, Jia-Jin, Chang-Lin Zhao, and Chao-Mao Liu. 2022. "The Morphological Characteristics and Phylogenetic Analyses Revealed an Additional Taxon in Heteroradulum (Auriculariales)" Diversity 14, no. 1: 40. https://doi.org/10.3390/d14010040

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