Research Article |
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
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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.
Phylogenetic analysis, polypore, wood-rotting fungi
Sidera, a genus with mostly poroid hymenophore of wood-inhabiting fungi distributed in most continents except Africa (
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 (
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
The main characteristics of Sidera species. Pore and basidiospore sizes mainly from
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 |
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
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 (
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 (
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
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
The research using ML was conducted using RAxML-HPC v.8.2.3 (
A total of 24 models of evolution was scored using PAUP* version 4.0 beta 10 (
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 (
The concatenated ITS+nLSU dataset contained sequences from 81 fungal specimens representing 18 Sidera taxa (Table
The phylogeny (Fig.
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 (
USA. Connecticut, New Haven, West Rock Park, on rotten stump of Pinus, 15.VII.2012, Dai 12730 (
Americana (Lat.): referring to the species occurring in North America.
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 system dimitic; generative hyphae with clamp connections; skeletal hyphae dominant; all hyphae IKI–, CB–; tissue unchanged in KOH.
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.
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.
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).
Canada, Ontario, Hamilton, McMaster University, Botanical Garden, on rotten angiosperm wood, 18–20.VII.2017, Dai 19173 (
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.
China, Shannxi Province, Zhashui County, Niubeiliang Forest Park, on fallen angiosperm trunk, 16.IX.2013, Cui 11216 (
Borealis (Lat.): referring to the species occurring in boreal areas of China.
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 system dimitic; generative hyphae with clamp connections; skeletal hyphae dominant; all hyphae IKI–, CB–; tissue unchanged in KOH.
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.
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.
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).
China, Gansu Province, Zhuoni County, Yaohe Nature Reserve, on rotten wood of Abies, 19.VIII.2022, Dai 24187 (
See
Belarus, Brestskaya Voblasts, Belavezhskaya Pushcha National Park, on rotten wood of Picea, 19.X.2019, Dai 21057 (
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 |
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.
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.
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 (
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.