Research Article
Print
Research Article
Taxonomy and phylogeny of Sidera (Hymenochaetales, Rickenella clade) from China and North America revealing two new species
expand article infoZhan-Bo Liu‡, Hong-Min Zhou‡, Hong-Gao Liu§, Yuan Yuan‡
‡ Beijing Forestry University, Beijing, China
§ Zhaotong University, Zhaotong, China

Corresponding author: Yuan Yuan ( yuanyuan1018@bjfu.edu.cn )

Academic editor: Maria-Alice Neves
© 2023 Zhan-Bo Liu, Hong-Min Zhou, Hong-Gao Liu, Yuan Yuan.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Liu Z-B, Zhou H-M, Liu H-G, Yuan Y (2023) Taxonomy and phylogeny of Sidera (Hymenochaetales, Rickenella clade) from China and North America revealing two new species. MycoKeys 96: 173-191. https://doi.org/10.3897/mycokeys.96.100743
Open Access

Abstract

Sidera, belonging to the Rickenella clade of Hymenochaetales, is a worldwide genus with mostly poroid hymenophore of wood-inhabiting fungi. Two new species in the genus, Sidera americana and S. borealis, are described and illustrated from China and North America based on morphological and molecular evidence. They were mainly found growing on rotten wood of Abies, Picea and Pinus. S. americana is characterized by annual, resupinate basidiomata with silk sheen when dry, round pores (9–11 per mm), a dimitic hyphal system, and allantoid basidiospores measuring 3.5–4.2 × 1 μm. S. borealis is characterized by annual, resupinate basidiomata with cream to pinkish buff dry pore surface, angular pores (6–7 per mm), a dimitic hyphal system, and allantoid basidiospores measuring 3.9–4.1 × 1–1.1 μm. Phylogenetic analysis based on a combined 2-locus dataset [ITS1-5.8S-ITS2 (ITS) + nuclear large subunit RNA (nLSU)] shows that the two species are members of Sidera, and they are compared with morphologically similar and phylogenetically related species, respectively. An identification key to 18 accepted species of Sidera in worldwide is provided.

Keywords

Phylogenetic analysis, polypore, wood-rotting fungi

Introduction

Larsson et al. (2006) used the name ‘Rickenella clade’ for species in Rickenella Raithelh. and 18 additional genera for the first time. Athelopsis lunata (Romell ex Bourdot & Galzin) Parmasto [= Sidera lunata (Romell ex Bourdot & Galzin) K.H. Larss.] is a member of Rickenella clade in their phylogenetic analysis of Hymenochaetales. Miettinen and Larsson (2011) established the new genus Sidera Miettinen & K.H. Larss. to accommodate Athelopsis lunata, Ceriporiopsis lowei Rajchenb. [= Sidera lowei (Rajchenb.) Miettinen], Skeletocutis lenis (P. Karst.) Niemelä [= Sidera lenis (P. Karst.) Miettinen] and Skeletocutis vulgaris (Fr.) Niemelä & Y.C. Dai [= Sidera vulgaris (Fr.) Miettinen], because these four species formed a monophyletic group and didn’t group together with any other species or genera within Rickenella clade in their phylogenetic analysis of 5.8S + nLSU. Yu et al. (2021) studied the taxonomic positions of the genera Resinicium Parmasto and Skvortzovia Bononi & Hjortstam, which belong to Rickenella clade. With the much richer sampling available to us, the phylogenetic analyses also prompted us to study the taxonomic position of Sidera within the Rickenella clade.

Sidera, a genus with mostly poroid hymenophore of wood-inhabiting fungi distributed in most continents except Africa (Miettinen and Larsson 2011; Liu et al. 2022; Wu et al. 2022a), is treated as a member of Rickenella clade within Hymenochaetales, with Sidera lenis as the generic type. To date, 16 species are accepted in Sidera (Miettinen and Larsson 2011; Du et al. 2019, 2020; Liu et al. 2021, 2022). Seven species of Sidera have previously been recorded from China: S. inflata Z.B. Liu & Y.C. Dai, S. minutissima Y.C. Dai et al., S. parallela Dai et al., S. punctata Z.B. Liu & Y.C. Dai, S. roseo-bubalinaZ.B. Liu & Y.C. Dai, S. salmonea Z.B. Liu et al., and S. tibetica Z.B. Liu et al. (Du et al. 2020; Liu et al. 2021, 2022).

Morphologically, Sidera is characterized by resupinate, white to cream or buff, mostly waxy fresh basidiomata, mostly poroid (one hydnoid species) hymenophore, a dimitic or monomitic hyphal system with generative hyphae with clamp connections, the presence of rosette-like crystals, and allantoid to lunate, hyaline, thin-walled basidiospores (Miettinen and Larsson 2011; Liu et al. 2021). Species in the genus cause a white rot.

In this study, we focus on Sidera represented by eight resupinate specimens from China, and North America. Phylogenetic analysis based on the ITS and nLSU rDNA sequences is carried out and two new species are described. The current study aims to further explore the species diversity of Sidera in the Asia-Pacific region, and more importantly, to confirm the taxonomic position of Sidera within the Rickenella clade of Hymenochaetales, based on the ITS+nLSU phylogenetic analysis. Morphological characters of all 18 currently accepted species of Sidera are summarized in Table 1. Furthermore, an identification key to accepted species is provided in the paper.

Table 1.
Download as
CSV
XLSX

The main characteristics of Sidera species. Pore and basidiospore sizes mainly from Liu et al. (2022). New species are shown in bold.

Species Growing habit Hymenophore Hyphal system Cystidioles Skeletal hyphae in KOH Spores shape Spore dimension (µm)
S. americana Annual Poroid, 9–11/mm Dimitic Present Almost unchanged Allantoid 3.5–4.2 × 1
S. borealis Annual Poroid, 6–7/mm Dimitic Present Almost unchanged Allantoid 3.9–4.1 × 1–1.1
S. inflata Annual Poroid, 9–10/mm Dimitic Present Swollen Allantoid 3–3.3 × 0.9–1.1
S. lenis Perennial Poroid, 4–6/mm Dimitic Present Swollen Allantoid to lunate 3.9–4.9 × 1.5–2
S. lowei Annual Poroid, 6–8/mm Monomitic Present, some branched – Allantoid 3.5–5 × 1–1.2
S. lunata Annual Hydnoid, 8–9/mm Monomitic Present – Allantoid 2.5–3.8 × 1.6–1.9
S. malaysiana Annual Poroid, 9–11/mm Dimitic Present Swollen Lunate 2.9–3.2 × 1–1.2
S. minutipora Annual Poroid, 5–7/mm Dimitic Present Swollen Allantoid 3.7–4.3 × 1–1.3
S. minutissima Annual Poroid, 7–9/mm Dimitic Present Almost unchanged Allantoid 3.8–4.4 × 0.9–1.3
S. parallela Annual Poroid, 6–8/mm Dimitic Present Almost unchanged Lunate 2.8–3.3 × 0.9–1.2
S. punctata Annual Poroid, 8–9/mm Monomitic Absent – Allantoid to lunate 3.8–4.8 × 1–1.3
S. roseo-bubalina Annual Poroid, 6–7/mm Monomitic Present – Lunate 3.9–4.5 × 0.8–1
S. salmonea Annual Poroid, 7–9/mm Dimitic Present Almost unchanged Lunate 3–3.5 × 0.9–1.1
S. srilankensis Annual Poroid, 6–8/mm Dimitic Present Almost unchanged Lunate 3.5–4 × 1–1.3
S. tenuis Annual Poroid, 8–10/mm Dimitic Present Almost unchanged Allantoid 4.2–5 × 0.8–1
S. tibetica Annual Poroid, 7–8/mm Dimitic Present Almost unchanged Lunate 2.9–3.1 × 1–1.1
S. vesiculosa Annual Poroid, 7–9/mm Monomitic Present – Allantoid to lunate 2.9–3.7 × 0.6–1
S. vulgaris Perennial Poroid, 6–8/mm Dimitic Present, some branched Almost unchanged Allantoid to lunate 2.9–3.6 × 0.9–1.4

Materials and methods

Morphological studies

Macro-morphological descriptions were based on field notes and dry herbarium specimens. Microscopic measurements and drawings were made from slide preparations of dried tissues stained with Cotton Blue and Melzer’s reagent as described by Dai (2010). Pores were measured by subjectively choosing as straight a line of pores as possible and measuring how many per mm. The following abbreviations are used in the description: CB = Cotton Blue; CB– = acyanophilous in Cotton Blue; IKI = Melzer’s reagent; IKI– = neither amyloid nor dextrinoid in Melzer’s reagent; KOH = 5% potassium hydroxide; n (a/b) = number of spores (a) measured from given number of specimens (b); L = mean spore length (arithmetic average of all the spores); W = mean spore width (arithmetic average of all the spores); and Q = variation in the L/W ratios between the specimens studied. When the variation in spore size is shown, 5% of the measurements were excluded from each end of the range, and these values are shown in parentheses. Special color terms follow Petersen (1996) and then herbarium abbreviations follow Thiers (2018). Voucher specimens from the study were deposited in the herbarium of the Institute of Microbiology, Beijing Forestry University (BJFC).

DNA extraction,PCR and sequencing

Total genomic DNA was extracted from dried specimens by a CTAB rapid plant genome extraction kit (Aidlab Biotechnologies Company, Limited, Beijing, China) according to the manufacturer’s instructions with some modifications (Li et al. 2014). The ITS regions were amplified with primers ITS4 and ITS5 (White et al. 1990). The nLSU regions were amplified with primers LR0R and LR7 (Vilgalys and Hester 1990).

The polymerase chain reaction (PCR) procedure for ITS was as follows: initial denaturation at 95 °C for 3 min, followed by 35 cycles at 94 °C for 40 sec, 58 °C for 45 sec, 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 sec, 48 °C for 1 min, and 72 °C for 1.5 min, and a final extension of 72 °C for 10 min (Zhao et al. 2015). Aliquots of PCR products were examined on 2% agarose gels stained with GelStar Nucleic Acid Gel Stain (Lonza Rockland, Inc., Rockland, YN, USA) and examined under UV light. The sequencing of the PCR products was conducted by the Beijing Genomics Institute, Beijing, China, with the same primers used in the PCR reactions. Species were identified by sequence comparison with accessions in the NCBI databases using the BLAST program.

Phylogenetic analyses

Phylogenetic trees were constructed using ITS + nLSU rDNA sequences, and phylogenetic analyses were performed with the Maximum Likelihood (ML), Maximum Parsimony (MP) and Bayesian Inference (BI) methods. Sequences of the species and strains were primarily adopted from ITS-based and 28S-based tree topology as described by Miettinen and Larsson (2011) and Liu et al. (2022). New sequences generated in this study, along with reference sequences retrieved from GenBank (Table 2), were aligned by MAFFT 7 (Katoh et al. 2019; http://mafft.cbrc.jp/alignment/server/) using the “G-INS-i” strategy and manually adjusted in BioEdit v.7.2.5 (Hall 1999). Unreliably aligned sections were removed before the analyses, and efforts were made to manually inspect and improve the alignment. The data matrix was edited in Mesquite v3.70 (Maddison and Maddison 2021; https://www.mesquiteproject.org/). The sequence alignment was deposited at TreeBase. Sequences of Exidia candida Lloyd and Exidiopsis calcea (Pers.) K. Wells outside Hymenochaetales obtained from GenBank were used as outgroups to root the tree in the ITS + nLSU analysis.

Table 2.
Download as
CSV
XLSX

Information for the sequences used in this study. * Newly generated sequences for this study. New species are shown in bold.

Species Specimen no. Locality GenBank accession no.
ITS nLSU
Atheloderma mirabile TAA 169235 Estonia DQ873592 DQ873592
Contumyces rosella Redhead 7501 – U66452 U66452
Cyphellostereum laeve JJ 020909 Sweden EU118621 EU118621
Exidia candida VS 8588 Russia KY801871 KY801896
Exidiopsis calcea MW 331 Canada AF291280 AF291326
Globulicium hiemale KHL 961221 Sweden EU118626 EU118626
G. hiemale Hjm 19007 Sweden DQ873595 DQ873595
Hyphoderma capitatum KHL 8464 Sweden DQ677491 DQ677491
H. orphanellum NH 12208 Russia DQ677500 DQ677500
Odonticium romellii KHL 1514b Norway DQ873639 DQ873639
Peniophorella praetermissa KHL 13164 Estonia DQ873597 DQ873597
P. tsugae NH 7473 Sweden – DQ677505
Repetobasidium conicum KHL 12338 USA DQ873647 DQ873647
Resinicium austroasianum LWZ 20180417-5 Malaysia MW414504 MW414450
R. bicolor Miettinen 14049 Finland MF319079 MF318936
R. chiricahuaense JLL-14605 Canada – DQ863692
R. confertum FP-102863 USA DQ826538 –
R. friabile CBS 126043 New Zealand MH864058 MH875513
R. grandisporum GGGUY13-008 French Guiana KY995325 –
R. lateastrocystidium LWZ 20180414-15 Malaysia MW414509 MW414455
R. monticola FP-150360 Jamaica DQ826552 DQ863697
R. mutabile FP-102989 Puerto Rico DQ826556 DQ863699
R. rimulosum FP-150328 Jamaica DQ826546 –
R. saccharicola FP-102754 Puerto Rico DQ826547 DQ863691
R. tenue FP-150354 Jamaica DQ826539 –
R. sp. LWZ 20171015-31 Vietnam MW414511 MW414457
Rickenella fibula P. Salo 1882 MF319088 –
R. mellea Lamoure 74 – U66438 U66438
Sidera americana Dai 19173 Canada MW198477* MW192005*
Dai 12730 USA MW198478* –
S. borealis Dai 22822 China OM974254* OM974246*
Dai 24120 China OQ134533* –
Cui 11216 China MW198485* –
Dai 23962 China OQ134534* –
Dai 23803 China OQ134535* –
Dai 24187 China OQ134536* OQ134528*
Dai 23960 China OQ134537* –
S. inflata Cui 13610 China MW198480 –
S. lenis Miettinen 11036 Finland FN907914 FN907914
Dai 22834 China OQ134538* OQ134529*
Dai 22854 China OQ134539* OQ134530*
S. lowei Miettinen X419 Venezuela FN907917 FN907917
Miettinen X426 New Zealand FN907919 FN907919
S. lunata JS 15063 Norway DQ873593 DQ873593
S. malaysiana Dai 18570 Malaysia MW198481 MW192007
S. minutipora Gates FF257 Australia FN907922 FN907922
Cui 16720 Australia MN621349 MN621348
S. minutissima Dai 19529 Sri Lanka MN621352 MN621350
Dai 22495 China OM974248 OM974240
Dai 18471A China MW198482 MW192008
S. parallela Dai 22038 China MW477793 MW474964
S. parallela Cui 10346 China MK346145 –
Cui 10361 China MK346144 –
Dai 22635 China OQ134540* OQ134531*
S. punctata Dai 22119 China MW418438 MW418437
S. roseo-bubalina Dai 11277 China MW198483 –
S. salmonea Dai 23343 China OM974249 OM974241
Dai 23354 China OM974250 OM974242
Dai 23428 China OM974251 OM974243
Dai 23612 China – OM974247
S. sp. Dollinger 922 USA KY264044 –
S. srilankensis Dai 19581 Sri Lanka MN621345 MN621347
Dai 19654 Sri Lanka MN621344 MN621346
S. tibetica Dai 23407 China OM974252 OM974244
Dai 23648 China OM974253 OM974245
Dai 21057 Belarus MW198484* MW192009*
Dai 22151 China MW477794* MW474965*
S. tenuis Dai 18697 Australia MK331865 MK331867
Dai 18698 Australia MK331866 MK331868
S. vesiculosa Dai 17835 Singapore MH636565 MH636567
Dai 17845 Singapore MH636564 MH636566
S. vulgaris Ryvarden 37198 New Zealand FN907918 FN907918
Skvortzovia dabieshanensis LWZ 20201012-22 China MW414512 MW414458
S. furfuracea KHL 11738 Finland DQ873648 DQ873648
S. furfurella KHL 10180 Puerto Rico DQ873649 DQ873649
S. georgica KHL 12019 Norway DQ873645 DQ873645
S. meridionalis FP-150236 – – AY293197
S. pinicola KHL 12224 USA DQ873637 DQ873637
S. qilianensis LWZ 20180904-16 China MW414518 MW414464
Skvortzoviella lenis LWZ 20180921-7 China MW414521 MW414467
LWZ 20180921-17 China MW414522 MW414468

Maximum Parsimony analysis was applied to the ITS + nLSU dataset sequences. The approaches to phylogenetic analysis utilized those conducted by Liu et al. (2022), and the tree was constructed using PAUP* version 4.0 beta 10 (Swofford 2002). All the characters were equally weighted, and gaps were treated as missing data. Trees were inferred using the heuristic search option with tree bisection and reconnection (TBR) branch swapping, and 1000 random sequence addition maxtrees were set to 5000. Branches of zero length were collapsed, and all the parsimonious trees were saved. Clade robustness was assessed using a bootstrap (BT) analysis with 1000 replicates (Felsenstein 1985). Descriptive tree statistics, including the Consistency Index (CI), Homoplasy Index (HI), Rescaled Consistency index (RC), Retention Index (RI), and tree length (TL), were calculated for each Maximum Parsimonious Tree (MPT) generated.

The research using ML was conducted using RAxML-HPC v.8.2.3 (Stamatakis 2014) and RAxML-HPC through the CIPRES Science Gateway V. 3.3 (Miller et al. 2010; http://www.phylo.org). Statistical support values (BS) were obtained using nonparametric bootstrapping with 1000 replicates. The BI analysis was performed with MrBayes 3.2.7a (Ronquist et al. 2012). Four Markov chains were run for two runs from random starting trees for 5 million generations until the split deviation frequency value < 0.01, and the trees were sampled at every 1000 generation. The first 25% of the sampled trees were discarded as burn-in, and the remaining ones were used to reconstruct a majority rule consensus tree and calculate the Bayesian Posterior Probabilities (BPP) of the clades.

A total of 24 models of evolution was scored using PAUP* version 4.0 beta 10 (Swofford 2002). Optimal substitution models for the combined dataset were then determined using the Akaike Information Criterion (AIC) implemented in MrModeltest 2.3 (Posada and Crandall 1998; Nylander 2004). The model GTR + I + G was selected for use in the Maximum Likelihood (ML) and Bayesian Inference (BI) analyses.

Branches that received bootstrap support for Maximum Likelihood (BS), Maximum Parsimony (BP), and Bayesian Posterior Probabilities (BPP) > 70% (BS), 50% (BP), and 0.95 (BPP) were considered to be significantly supported. In addition, the ML analysis resulted in the best tree, and only the ML tree is shown along with the support values from the MP and BI analyses. FigTree v1.4.4 (Rambaut 2018) was used to visualize the resulting tree.

Results

The concatenated ITS+nLSU dataset contained sequences from 81 fungal specimens representing 18 Sidera taxa (Table 2). The dataset had an aligned length of 2313 characters, of which 1218 were constant, 269 were variable but parsimony-uninformative, and 826 were parsimony-informative. MP analysis yielded three equally parsimonious trees (TL = 5471, CI = 0.369, RI = 0.694, RC = 0.256, HI = 0.631). And the average standard deviation of split frequencies was 0.009886 (BI).

The phylogeny (Fig. 1) inferred from the ITS + nLSU sequences confirmed the taxonomic position of Sidera (Fig. 1B), Resinicium (Fig. 1C), and Skvortzovia (Fig. 1D) within the Rickenella clade (Fig. 1A) of Hymenochaetales. Species in Sidera clustered together with strong support (98% BS, 96% BP, 1.00 BPP) and new species Sidera americana and S. borealis clustered in the Sidera clade. S. americana grouped with S. parallela with strong support (98% BS, 100% BP, 1.00 BPP). S. borealis grouped with S. vulgaris with strong support (100% BS, 100% BP, 1.00 BPP).

Figure 1. 

Phylogeny of Sidera and other genera in the Rickenella clade generated by ML analyses based on combined ITS+nLSU sequences A the Rickenella clade B the genus Sidera in modena C the genus Resinicium in purple D the genus Skvortzovia in red. Branches are labelled with Maximum Likelihood bootstrap > 70%, parsimony bootstrap proportions > 50%, and Bayesian Posterior Probabilities > 0.95, respectively. New species are indicated in bold. * Newly generated sequences for this study.

Besides, we collected two Sidera lenis on rotten wood of Picea in Yunnan Province, China: Dai 22834 (BJFC 037407) and Dai 22854 (BJFC 037427). This is the first time the species has been reported in China. We have uploaded ITS and nLSU sequences of the two specimens to GenBank (https://www.ncbi.nlm.nih.gov/genbank/) and added them to our phylogenetic analysis (Fig. 1).

Taxonomy

Sidera americana Z.B. Liu & Yuan Yuan, sp. nov.

MycoBank No: MycoBank No: 838379
Figs 2, 3

Diagnosis

Sidera americana is characterized by annual, resupinate basidiomata with silk sheen when dry, round pores (9–11 per mm), a dimitic hyphal system, and allantoid basidiospores measuring 3.5–4.2 × 1 μm.

Figure 2. 

Basidiomata of Sidera americana (Holotype, Dai 12730). Photo by: Zhan-Bo Liu.

Holotype

USA. Connecticut, New Haven, West Rock Park, on rotten stump of Pinus, 15.VII.2012, Dai 12730 (BJFC 013037, isotype in CFMR).

Figure 3. 

Microscopic structures of Sidera americana (Holotype, Dai 12730) a basidiospores b basidia and basidioles c cystidioles d hyphae from subiculum e hyphae from trama f hyphae at dissepiment edge. Drawings by: Hong-Min Zhou.

Etymology

Americana (Lat.): referring to the species occurring in North America.

Basidiomata

Annual, resupinate, soft and without odor or taste when fresh, soft corky when dry, up to 14 cm long, 6 cm wide, and approximately 2 mm thick at center; pore surface white when fresh, becoming cream to buff with silk sheen when dry; sterile margin indistinct; pores round, 9–11 per mm; dissepiments thin, lacerate; subiculum very thin to almost absent; tubes concolorous with poroid surface, up to 2 mm long.

Hyphal structure

Hyphal system dimitic; generative hyphae with clamp connections; skeletal hyphae dominant; all hyphae IKI–, CB–; tissue unchanged in KOH.

Subiculum

Generative hyphae hyaline, thin-walled, unbranched, 1–2.5 μm in diam; skeletal hyphae dominant, thick-walled with a wide lumen, frequently branched, flexuous, interwoven, 2–3 μm diam.

Tubes

Generative hyphae hyaline, thin-walled, unbranched, 1–2 μm in diam, dominating at dissepiment edges; skeletal hyphae dominant in tube trama except dissepiment edges, thick-walled with a wide lumen, unbranched, flexuous, interwoven, 2–3 μm diam; rosette-like crystals abundant, 3–12.5 μm in diam; cystidia absent; cystidioles present, fusoid, hyaline, thin-walled, basally swollen, with a sharp or often hyphoid neck, 13.4–15 × 3.2–4 μm; basidia barrel-shaped, hyaline, bearing four sterigmata and with a basal clamp connection, 6–7 × 3–4.2 μm; basidioles in shape similar to basidia, but slightly shorter.

Spores

Basidiospores allantoid, hyaline, thin-walled, smooth, occasionally with one or two guttules, IKI–, CB–, (3.2–)3.5–4.2(–5) × 1(–1.3) μm, L = 4 μm, W = 1.04 μm, Q = 3.74–3.96 (n = 60/2).

Additional specimen examined

Canada, Ontario, Hamilton, McMaster University, Botanical Garden, on rotten angiosperm wood, 18–20.VII.2017, Dai 19173 (BJFC 027641).

Sidera borealis Z.B. Liu & Yuan Yuan, sp. nov.

MycoBank No: MycoBank No: 838385
Figs 4, 5

Diagnosis

Sidera borealis is characterized by annual, resupinate basidiomata with cream to pinkish buff dry pore surface, angular pores (6–7 per mm), a dimitic hyphal system, and allantoid basidiospores measuring 3.9–4.1 × 1–1.1 μm.

Figure 4. 

Basidiomata of Sidera borealis (Paratypes) A Dai 24120 B Dai 22822 C Dai 23960 D Dai 24187. Photo by: Yu-Cheng Dai.

Holotype

China, Shannxi Province, Zhashui County, Niubeiliang Forest Park, on fallen angiosperm trunk, 16.IX.2013, Cui 11216 (BJFC 015331).

Figure 5. 

Microscopic structures of Sidera borealis (Holotype, Cui 11216) a basidiospores b basidia and basidioles c cystidioles d hyphae from subiculum e hyphae from trama f hyphae at dissepiment edge. Drawings by: Hong-Min Zhou.

Etymology

Borealis (Lat.): referring to the species occurring in boreal areas of China.

Basidiomata

Annual, resupinate, soft corky and without odor or taste when fresh, corky when dry, up to 5 cm long, 2 cm wide, and less than 1 mm thick at center; pore surface white to cream or pale buff when fresh, becoming cream to pinkish buff when dry; sterile margin indistinct, white, cottony, thinning out; pores angular, 6–7 per mm; dissepiments thin, entire; subiculum very thin to almost absent; tubes concolorous with poroid surface, less than 1 mm long.

Hyphal structure

Hyphal system dimitic; generative hyphae with clamp connections; skeletal hyphae dominant; all hyphae IKI–, CB–; tissue unchanged in KOH.

Subiculum

Generative hyphae hyaline infrequent, thin-walled, occasionally branched, 1–2 μm in diam; skeletal hyphae dominant, thick-walled with a narrow to medium lumen, occasionally branched, flexuous, interwoven, 1–3 μm diam.

Tubes

Generative hyphae hyaline occasionally present, thin-walled, rarely branched, 1–2 μm in diam, dominating at dissepiment edges; skeletal hyphae thick-walled with a narrow to wide lumen, occasionally branched, flexuous, interwoven, 1–3 μm diam; rosette-like crystals present, 3–6 μm in diam; cystidia absent; cystidioles present, fusoid, hyaline, thin-walled, basally swollen, with a sharp or often hyphoid neck, 17–19 × 2.5–3 μm; basidia barrel-shaped, hyaline, bearing four sterigmata and with a basal clamp connection, 7–8 × 3.5–4 μm; basidioles in shape similar to basidia, but slightly shorter.

Spores

Basidiospores allantoid, hyaline, thin-walled, smooth, occasionally with one or two guttules, IKI–, CB–, (3.5–)3.9–4.1(–4.2) × (0.8–)1–1.1(–1.4) μm, L = 4.01 μm, W = 1.06 μm, Q = 3.78 (n = 60/1).

Additional specimens examined

China, Gansu Province, Zhuoni County, Yaohe Nature Reserve, on rotten wood of Abies, 19.VIII.2022, Dai 24187 (BJFC 039430); on rotten wood of Picea, 18.VIII.2022, Dai 24120 (BJFC 039364); Jilin Province, Antu County, Dongfanghong Forest Farm, on rotten wood of Pinus, 25.VII.2022, Dai 23803 (BJFC 039047); Qinghai Province, Nangqian County, Baizha Forest Farm, on rotten wood of Picea, 7.VIII.2022, Dai 23960 (BJFC 039204); Dai 23962 (BJFC 039206); Yunnan Province, Deqin County, Baimaxueshan Nature Reserve, on rotten wood of Picea, 5.IX.2021, Dai 22822 (BJFC 037395).

Sidera tibetica Z.B. Liu, Jian Yu & F. Wu, Journal of Fungi 8: 7 (2022)

Fig. 6

Description

See Liu et al. (2022). Liu et al. (2022) described Sidera tibetica as a new species based on Tibetan specimens and a photo of holotype. Subsequently, more specimens of the species from Belarus and China (Guangxi, Yunnan and Zhejiang) were collected and we took many photos of the fungus at different stages of growth on different hosts to make it easier for taxonomists to recognize the fungus in the field.

Figure 6. 

Basidiomata of Sidera tibetica A Dai 22321 B Dai 22639 C Dai 22663 D Dai 22151 E Dai 20342 F Dai 23407 G Dai 23486 H Dai 23648 (Holotype) I Dai 21057. Photo by: Yu-Cheng Dai.

Materials studied

Belarus, Brestskaya Voblasts, Belavezhskaya Pushcha National Park, on rotten wood of Picea, 19.X.2019, Dai 21057 (BJFC 032716, paratype). China, Guangxi, Guiping County, Xishan Forest Park, on rotten wood of Pinus, 25.XII.2020, Dai 22151 (BJFC 036043, paratype); Xizang, Bomi County, Gangcun Spruce Park, on a rotten branch of Pinus armandii, 27.X.2021, Dai 23648 (BJFC 038220, holotype); Yigong, on a rotten branch of Pinus armandii, 24.X.2021, Dai 23407 (BJFC 037979, paratype); on rotten wood of Pinus yunnanensis, 24.X.2021, Dai 23486 (BJFC 038058, paratype); Yunnan Province, Jianchuan County, Yinhe Mountain, on fallen trunk of Pinus, 27.IX.2021, Dai 23097 (BJFC 037668, paratype), 28.IX.2021, Dai 23121 (BJFC037692, paratype); on fallen branch of Pinus, 27.IX.2021, Dai 23106 (BJFC037677, paratype). Mouding County, Huafoshan Nature Reserve, on rotten wood of Pinus yunnanensis, 31.VIII.2021, Dai 22639 (BJFC 037213, paratype); Dai 22663 (BJFC 037237, paratype); on rotten wood of Pinus, 31.VIII.2021, Dai 22667 (BJFC 037241, paratype). Wuding County, Shizishan Nature Reserve, on fallen angiosperm trunk, 15.VIII.2019, Dai 20326 (BJFC 031994, paratype); on rotten wood of Pinus, 15.VIII.2019, Dai 20342 (BJFC 032010, paratype); Zhejiang Province, Pingyang County, Nanyandangshan Forest Park, on rotten wood of Pinus, 3.VI.2021, Dai 22321 (BJFC 036909, paratype).

A key to accepted species of Sidera in worldwide

1 Hymenium grandinioid to odontioid S. lunata
– Hymenium poroid 2
2 Hyphal system monomitic 3
– Hyphal system dimitic 6
3 Basidiospores mostly < 1 μm in width 4
– Basidiospores mostly > 1 μm in width 5
4 Pores 7–9 per mm; basidiospores 2.9–3.7 μm long S. vesiculosa
– Pores 6–7 per mm; basidiospores 3.9–4.5 μm long S. roseo-bubalina
5 Pores 6–8 per mm; cystidioles present, some branched S. lowei
– Pores 8–9 per mm; cystidioles absent S. punctata
6 Basidiospores > 1.5 μm in width S. lenis
– Basidiospores < 1.5 μm in width 7
7 Skeletal hyphae becoming swollen in KOH 8
– Skeletal hyphae almost unchanged in KOH 10
8 Pores 5–7 per mm; basidiospores 3.7–4.3 μm long S. minutipora
– Pores 9–11 per mm; basidiospores 2.9–3.3 μm long 9
9 Basidiospores allantoid, skeletal hyphae distinctly swollen in KOH S. inflata
– Basidiospores lunate, skeletal hyphae slightly swollen in KOH S. malaysiana
10 Tramal hyphae parallel along the tubes S. parallela
– Tramal hyphae interwoven 11
11 Generative hyphae at dissepiments even 12
– Generative hyphae at dissepiments with swollen tips 16
12 Basidiospores > 3.5 μm long 13
– Basidiospores < 3.5 μm long 15
13 Pores < 9 per mm S. americana
– Pores > 9 per mm 14
14 Skeletal hyphae occasionally branched in subiculum and tube trama S. borealis
– Skeletal hyphae unbranched in subiculum and tube trama S. srilankensis
15 Sterile margin distinct, white; basidiospore length/width > 3 S. salmonea
– Sterile margin indistinct to almost absent; basidiospore length/width < 3 S. tibetica
16 Basidiospores < 3.6 μm long S. vulgaris
– Basidiospores > 3.8 μm long 17
17 Sterile margin distinct, fimbriate; basidiospore length/width < 4 S. minutissima
– Sterile margin indistinct to almost absent; basidiospore length/width > 4 S. tenuis

Discussion

Sidera americana is discovered in USA and Canada, and the species is characterized by annual, resupinate basidiomata with silk sheen when dry, round pores (9–11 per mm), a dimitic hyphal system, and allantoid basidiospores measuring 3.5–4.2 × 1 μm. In our phylogeny, two specimens of S. americana form a lineage with strong support (99% BS, 100% BP, 1.00 BPP, Fig. 1). S. americana is closely related to S. parallela (98% BS, 100% BP, 1.00 BPP, Fig. 1), but basidiospores are longer in S. americana than in S. parallela (3.5–4.2 μm vs. 2.8–3.3 μm, Du et al. 2020). In addition, S. parallela has parallel tramal hyphae, while they are interwoven in S. americana.

Sidera borealis is discovered in boreal areas of China, including Gansu, Jilin, Qinghai, Shannxi, and Yunnan. The species is characterized by annual, resupinate basidiomata with cream to pinkish buff dry pore surface, angular pores (6–7 per mm), a dimitic hyphal system, and allantoid basidiospores measuring 3.9–4.1 × 1–1.1 μm. Phylogenetically, S. borealis clustered together with S. vulgaris with strong support (100% BS, 100% BP, 1.00 BPP, Fig. 1). Morphologically, S. vulgaris is different from S. borealis by the presence of capitate hyphal ends and “halocystidia” in tube mouths. Besides, basidiospores are longer in S. borealis than in S. vulgaris (3.9–4.1 μm vs. 2.9–3.6 μm, Niemelä and Dai 1997). S. borealis resembles S. minutipora by cream to buff fresh pores and similar pores (6–7 per mm vs. 5–7 per mm, Du et al. 2020). However, skeletal hyphae of S. minutipora become swollen in KOH, while they are unchanged in KOH in S. borealis. Besides, both species are distantly related (Fig. 1).

Sidera americana and S. borealis are described from North China and North America; like most other species of Sidera, the two new species grow mostly on gymnosperm wood in temperate or boreal forests, but they are distinguished from existing species in the genus by morphology, geographic distribution and DNA sequences.

Boreal areas of China have the most important virgin forests in the country, and such forests provide favorable environments for some special wood-decaying fungi, e.g. Heterobasidion Bref., Skeletocutis Kotl. & Pouzar and Sidera, because fewer morphological characteristics existed among different species of each genus, and many species in the traditional definition are, in fact, the species complex. In recent years, the introduction of molecular systematics has greatly improved our understanding of the diversity of wood-rotting fungi in the boreal forests. Numerous new species have been found there (Dai et al. 2007, 2021; Yuan and Dai 2008; Tian et al. 2013; Li et al. 2014; Chen et al. 2015, 2016; Cui et al. 2019; Wang et al. 2021; Wu et al. 2021, 2022b), and we believe that more boreal new species will be found in the future.

Acknowledgements

The research is supported by the National Natural Science Foundation of China (Project No. 32161143013) and the Second Tibetan Plateau Scientific Expedition and Research Program (STEP, Grant No. 2019QZKK0503). Special thanks are due to Prof. Yu-Cheng Dai (Beijing Forestry University, China) for forwarding his specimens and photos for our study.

References

  • Chen JJ, Cui BK, Zhou LW, Korhonen K, Dai YC (2015) Phylogeny, divergence time estimation, and biogeography of the genus Heterobasidion (Basidiomycota, Russulales). Fungal Diversity 71(1): 185–200. https://doi.org/10.1007/s13225-014-0317-2
  • Chen H, Zhou JL, Cui BK (2016) Two new species of Fomitiporia (Hymenochaetales, Basidiomycota) from Tibet, southwest China. Mycologia 108(5): 1010–1017. https://doi.org/10.3852/16-011
  • Cui BK, Li HJ, Ji X, Zhou JL, Song J, Si J, Dai YC (2019) Species diversity, taxonomy and phylogeny of Polyporaceae (Basidiomycota) in China. Fungal Diversity 97(1): 137–302. https://doi.org/10.1007/s13225-019-00427-4
  • Dai YC, Yu CJ, Wang HC (2007) Polypores from eastern Xizang (Tibet), western China. Annales Botanici Fennici 44: 135–145.
  • Dai YC, Yang ZL, Cui BK, Wu G, Yuan HS, Zhou LW, He SH, Ge ZW, Wu F, Wei YL, Yuan Y, Si J (2021) Diversity and systematics of the important macrofungi in Chinese forests. Mycosystema 40: 770–805. https://doi.org/10.13346/j.mycosystema.210036
  • Du R, Wu F, Gate GM, Dai YC, Tian XM (2020) Taxonomy and phylogeny of Sidera (Hymenochaetales, Basidiomycota): Four new species and keys to species of the genus. MycoKeys 68: 115–135. https://doi.org/10.3897/mycokeys.68.53561
  • Felsenstein J (1985) Confidence intervals on phylogenetics: An approach using bootstrap. Evolution; International Journal of Organic Evolution 39(4): 783–791. https://doi.org/10.2307/2408678
  • Hall TA (1999) Bioedit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
  • 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
  • Liu ZB, Zhou M, Yuan Y, Dai YC (2021) Global diversity and taxonomy of Sidera (Hymenochaetales, Basidiomycota): Four new species and keys to species of the genus. Journal of Fungi 7(4): e251. https://doi.org/10.3390/jof7040251
  • Liu ZB, Zhou M, Wu F, Yu J (2022) Two new species of Sidera (Hymenochaetales, Basidiomycota) from Southwest China. Journal of Fungi 8(4): e385. https://doi.org/10.3390/jof8040385
  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, 8 pp. https://doi.org/10.1109/GCE.2010.5676129
  • Niemelä T, Dai YC (1997) Polypore Skeletocutis lenis and its sib S. vulgaris. Annales Botanici Fennici 34: 133–140.
  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
  • Petersen JH (1996) The Danish Mycological Society’s colour-chart. Foreningen til Svampekundskabens Fremme, Greve.
  • Ronquist F, Teslenko M, Mark P, Ayres DL, Darling A, Höhna 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
  • Thiers B (2018) Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium, New York. http://sweetgum.nybg.org/science/ih/
  • Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
  • Wang K, Chen SL, Dai YC, Jia ZF, Li TH, Liu TZ, Phurbu D, Mamut R, Sun GY, Bau T, Wei SL, Yang ZL, Yuan HL, Zhang XG, Cai L (2021) Overview of China’s nomenclature novelties of fungi in the new century (2000–2020). Mycosystema 40: 822–833. https://doi.org/10.13346/j.mycosystema.210064
  • 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, 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
  • Wu F, Tohtirjap A, Fan LF, Zhou LW, Alvarenga RLM, Gibertoni TB, Dai YC (2021) Global diversity and updated phylogeny of Auricularia (Auriculariales, Basidiomycota). Journal of Fungi 7(11): e933. https://doi.org/10.3390/jof7110933
  • Wu F, Man XW, Tohtirjap A, Dai YC (2022a) A comparison of polypore funga and species composition in forest ecosystems of China, North America, and Europe. Forest Ecosystems 9: e100051. https://doi.org/10.1016/j.fecs.2022.100051
  • Yu J, Wang XW, Liu SL, Shen S, Zhou LY (2021) Taxonomy and phylogeny of Resinicium sensu lato from Asia-Pacific revealing a new genus and five new species (Hymenochaetales, Basidiomycota). IMA Fungus 12(1): 1–19. https://doi.org/10.1186/s43008-021-00071-1
  • Yuan HS, Dai YC (2008) Polypores from northern and central Yunnan Province, Southwestern China. Sydowia 60: 147–159.
login to comment