Research Article |
Corresponding author: Zai-Wei Ge ( zwge@mail.kib.ac.cn ) Academic editor: R. Henrik Nilsson
© 2020 Zai-Wei Ge, Jian-Yun Wu, Yan-Jia Hao, Qingying Zhang, Yi-Feng An, Martin Ryberg.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Ge Z-W, Wu J-Y, Hao Y-J, Zhang Q, An Y-F, Ryberg M (2020) The genus Catathelasma (Catathelasmataceae, Basidiomycota) in China. MycoKeys 62: 123-138. https://doi.org/10.3897/mycokeys.62.36633
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Two new species, Catathelasma laorentou and C. subalpinum, are described on the basis of morphological characters, phylogenetic evidence, host preferences and geographic distributions. A taxonomic key to the known species in China is also provided to facilitate identification. Based on samples from temperate Asia, Europe and North America, the phylogeny of Catathelasma was reconstructed using the internal transcribed spacer (ITS) region, the large subunit (LSU) of the ribosomal DNA and the translation elongation factor 1-α (TEF1).The phylogenetic results showed that Catathelasma contains two monophyletic clades: the /subalpinum clade and the /imperiale clade. The Asian species C. laorentou and C. subalpinum are closely related to the North American C. sp. (labelled as C. ventricosum in GenBank) in the /subalpinum clade, whereas C. imperiale and C. singeri are closely related in the /imperiale clade.
Catathelasmataceae, Biannulariaceae, Tricholomataceae, taxonomy, ectomycorrhizal fungi, new taxa
Catathelasma Lovejoy is the type genus of the mushroom family Catathelasmataceae Wasser (
Catathelasma has long been regarded a member of the Tricholomataceae (
Catathelasma contains four species: C. evanescens, C. imperiale, C. singeri and C. ventricosum (
Catathelasma specimens were collected in western and south-western China (Yunnan, Sichuan, Gansu and Tibet) and deposited in the Herbarium of Cryptogams, Kunming Institute of Botany, Chinese Academy of Sciences (
Taxa, vouchers, geographic origin and GenBank accession numbers of DNA sequences of Catathelasma and outgroups used in this study. New sequences generated in this study are given in bold. * indicates the type collection.
Taxon | Voucher | Geographic origin | GenBank accession number | ||
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ITS | LSU | TEF1 | |||
Catathelasma singeri |
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USA: Colorado | MK909090 | MK909109 | MK909079 |
C. singeri |
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USA: Colorado | MK909091 | MK909110 | MK909078 |
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USA: Colorado | MK909092 | MK909111 | MK909080 | |
C. singeri as ventricosum | PBM 2403 (AFTOL-ID 1488) | USA: Washington | DQ486686 | DQ089012 | N/A |
C. imperiale |
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China: Tibet | MK909094 | MK909112 | MK909081 |
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China: Sichuan | MK909096 | MK909113 | MK909083 | |
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China: Sichuan | MK909095 | MK909114 | MK909084 | |
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China: Gansu | MK909093 | MK909115 | MK909082 | |
TAA176551 | Canada: Newfoundland | N/A | AM946417 | N/A | |
UPS F-173429 | Sweden: Uppland | MK909097 | MK909116 | MK909085 | |
UPS F-120619 | Sweden: Hälsingland | MK909098 | N/A | N/A | |
TUB 011562 | N/A | DQ071743 DQ071835 | N/A | ||
LL_128 | KX008987 | N/A | N/A | ||
KM55154 | UK: England | GQ981498 | N/A | N/A | |
C. sp. as imperiale | DAOM225247 | KP255468 | AF261402 | KP255475 | |
11CA01A | USA: California | N/A | N/A | KC816900 | |
C. sp. as ventricosum | DAOM221514 | KP255469 | AF261401 | N/A | |
TRTC156545 | Canada: Quebec | JN020996 | N/A | N/A | |
Mat3 | Canada: Quebec | JN020995 | N/A | N/A | |
OSC 66879 | USA: Pacific Northwest | EU669305 | EU669331 | N/A | |
SMI349 | Canada: British Columbia | HQ650727 | N/A | N/A | |
TAA176473 | Canada: Newfoundland | N/A | AM946418 | N/A | |
C. laorentou |
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China: Yunnan | MK909106 | MK909117 | MK909086 |
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China: Yunnan | MK909103 | MK909118 | MK909087 | |
* |
China: Yunnan | MK909107 | N/A | N/A | |
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China: Yunnan | MK909105 | MK909119 | MK909088 | |
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China: Yunnan | MK909108 | MK909120 | N/A | |
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China: Sichuan | MK909102 | N/A | N/A | |
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China: Yunnan | MK909104 | N/A | N/A | |
C. subalpinum |
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China: Yunnan | MK909100 | MK909123 | MK909089 |
* |
China: Yunnan | MK909099 | MK909121 | N/A | |
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China: Yunnan | MK909101 | MK909122 | N/A | |
Outgroups | |||||
Callistosporium graminicolor | PBM 2341 (AFTOL-ID 978) | DQ484065 | AY745702 | GU187761 | |
Callistosporium luteoolivaceum | DUKE-JM99124 | N/A | AF261405 | KP255477 | |
MSM#004 | KJ101607 | N/A | N/A |
Morphological character descriptions were taken from field notes and colour images of the material, with colour names and codes following
Genomic DNA was extracted from dry specimens using the modified cetyltrimethylammonium bromide (CTAB) method (
PCR amplification was performed following
DNA sequences of ITS, LSU and TEF1 were independently aligned with MAFFT v6.8 (
Forty-six new ITS, LSU and TEF1 sequences were generated for Catathelasma species and deposited in GenBank (Table
Besides four Chinese collections that were confirmed to be conspecific with C. imperiale, sequences generated from other specimens collected in south-western China formed two monophyletic clades here described as C. laorentou and C. subalpinum, respectively (Fig.
As revealed by the analyses of the different genetic markers and concatenated dataset (ITS, LSU, TEF1 and the combined dataset), the genus Catathelasma comprises two monophyletic clades: the /imperiale clade and /subalpinum clade (Fig.
The /imperiale clade included the northern-temperate-region distributed C. imperiale and the North American species C. singeri. The ITS, TEF1 and concatenated sequences suggest that C. singeri represents a monophyletic clade within or close to C. imperiale (Fig.
Considering the strong statistical support as monophyletic groups and the morphological differences, as well as their host preferences (see below), C. laorentou and C. subalpinum are described as new species.
Pileus 8–15 cm broad, hemispherical, convex to plano-convex, later expanded with decurved margin, sometimes depressed to funnel-shaped, smooth, dry to slightly viscid, greyish-brown, reddish-brownish or brown. Lamellae adnate to slightly decurrent, white to off-white when young, whitish to cream when mature, thick, 7–15 mm in height, with 1–2 series of lamellulae; edge smooth, grey to dark brown. Stipe 5–10 × 1.8–3.0 cm, fusiform, attenuate downwards, straight or curved, firm, with double annulus in which the lower annulus is often gelatinous and the upper annulus is membranous, with white to whitish upper surface and grey to brown lower surface. Context firm, white, not changing colour when cut; smell and taste farinaceous. Spore print white.
Basidiospores [60/3/3] 10–14.5 × 4.5–6 μm, hyaline in KOH, amyloid, congophilous, smooth, oblong to subcylindrical in frontal view, subcylindrical to somewhat inequateral in side view, thin-walled, without germ pore. Basidia 35–48 × 7–10 μm, 4-spored, narrowly clavate, hyaline; sterigmata up to 5 μm long. Cheilocystidia basidiole-like, with yellow to brown contents. Pleurocystidia absent. Lamella trama bilateral, composed of more or less parallel to interwoven hyphae. Oleiferous hyphae present in both lamella and pileus trama. Pileipellis a thick ixocutis of loosely interwoven cylindrical, 2–8 μm wide gelatinised hyphae, interspersed with oleiferous hyphae. Clamp connections present, common.
Ectomycorrhizal, solitary or scattered, in forests dominated by Picea spp. or Abies spp.
China. Gansu Province: Gannan city, Diebu, Wabagou, alt. 2700 m, 12 August 2012, X. T. Zhu 662 (
This species is distinguished from C. ventricosum (Peck) Singer by having pale yellow to greyish-yellow basidiomes, longer stipes, abundant clamp connections and associations with Pinus yunnanensis Mast. and Keteleeria evelyniana Franchet in south-western China.
China. Yunnan Province: Chuxiong, Zixi Mountain, alt. 1950 m, in forest dominated by K. evelyniana Mast. and P. yunnanensis Franchet, 26 August 2017, Z. W. Ge 4070 (Holotype:
Pileus 10–24 cm broad, hemispherical to convex at first, expanding to convex to broadly convex with age; surface initially white, then yellowish-white (1A2) to pale yellow (1A3), greyish-yellow (2B3) with age, smooth at first, irregularly depressed, margin more or less incurved, slightly viscid to viscid when wet, occasionally with whitish veil remnants. Lamellae decurrent, white to off-white when young, whitish when mature, thick, 7–15 mm in height, with 1–2 series of lamellulae, edge smooth. Stipe 6–24 × 1.5–8 cm, fusiform, attenuate downwards, straight or curved, firm, with double annulus in which the lower annulus is flimsy and the upper annulus is membranous to leathery, yellowish-white, often split into several pedals. Context white, 2.1–4.5 cm thick in pileus, white in pileus and stipe, not changing colour when cut; smell and taste farinaceous. Spore print white.
Basidiospores [70/3/3] (8) 9–12(15) × (4) 5–6.5 (7) μm (mean 9.9 ± 1.3 × 5.8 ± 0.5 μm), Q = (1.23) 1.33–2.2 (2.75), Qav = 1.72 ± 0.30, ellipsoid, oblong to subcylindrical in frontal view, subcylindrical to somewhat inequateral in side view, hyaline in KOH, amyloid, congophilous, smooth, thin walled, without germ pore. Basidia 38–50 × 8–10 μm, narrowly clavate, 4-spored, hyaline; sterigmata up to 6 μm long. Cheilocystidia basidiole-like, hyalinous. Pleurocystidia absent. Lamella trama subregular, somewhat bilateral towards lamella edge, made up of more or less parallel to interwoven hyphae. Oleiferous hyphae present in both lamella and pileus trama. Pileipellis a thick ixocutis (850–1000 μm thick) of loosely interwoven cylindrical, gelatinised hyphae 2–10 μm in width, interspersed with oleiferous hyphae. Clamp connections present, common.
Known from Sichuan and Yunnan provinces in south-western China.
Presumably ectomycorrhizal, solitary or scattered, rarely in small clusters of 2–5 basidiomes in Pinus or Keteleeria forests.
From ‘lao ren tou jun’, a transliteration of the Chinese name “老人头菌” which is a local common name used in the wild mushroom markets in Yunnan, China. The literal translation is “fungus that looks like the shiny bald pate of The God of Longevity”.
China. Yunnan Province, Chuxiong, Nanhua, wild mushroom market, 12 August 2014, Z. W. Ge 3620 (
Catathelasma laorentou is morphologically similar to C. ventricosum (Peck) Singer, a species originally described from North America. Both species have ellipsoid basidiospores, large-sized hemispherical pilei and a pileipellis composed of an ixocutis layer. However, C. laorentou has abundant clamp connections, smaller basidiospores (9–11 × 5–6 μm), larger basidia (38–50 × 8–10 μm) and is found in coniferous forest dominated by P. yunnanensis and K. evelyniana from south-western China, while C. ventricosum is found alongside hardwood (
Catathelasma singeri Mitchel & A.H. Sm. from the USA is morphologically similar to C. laorentou, but the former differs by its dull pale ochraceous to dingy olive buff pileus which is slimy viscid and shows similarities to Hygrophorus Fr., smaller basidiomes (pileus around 6 cm, stipe 4 × 1.2 cm), bearing basidiole-like or narrower cheilocystidia. Catathelasma singeri was collected from the aspen zone, which was dominated by Populus tremuloides and Pinaceae species, although the specific host tree was not mentioned (
Catathelasma imperiale, originally described from Europe, is distinguished by its greyish-brown, reddish-brownish or brown basidiomes (Fig.
Catathelasma subalpinum is distinguished from C. laorentou by having greyish-yellow to grey pilei, higher elevation (alt. 2600–3500 m) occurrence and association with Pinus densata Mast.
Pileus 3.5–15 cm broad, hemispherical at early stage, expanding to broadly convex with age, shallowly depressed at centre, white to dirty white at first, then greyish-white (1B1) to greyish-yellow (4C4), grey (8B1) when mature, with incurved margin, viscid when wet, sometimes irregularly cracked. Lamellae slightly decurrent, crowded, whitish, thick, 8 mm in height, with 2–3 tiers of lamellulae, with smooth edge, covered by a white, well developed, thick membranous veil in early stage. Stipe 11–14 × 3–5.5 cm, fusiform, attenuated downwards, whitish to yellowish-white, firm, with double annulus in which the lower annulus is flimsy and the upper one is membranous, thick, around 2.5 cm away from the stipe apex; with white inner side and greyish-yellow outer side. Context white in pileus and stipe, not changing colour when cut, 3.5 cm thick in pileus; smell and taste farinaceous. Spore print white.
Basidiospores [43/2/2] (9) 10–12 × 5–6 μm (mean 10.7 ± 0.8 × 5.4 ± 0.5 μm), Q = (1.67) 1.80–2.20 (2.40), Qm = 1.99 ± 0.18, subcylindrical in frontal view, subcylindrical to somewhat inequilateral in side view, hyaline in KOH, amyloid, smooth, thin-walled. Basidia 35–45 × 8–9 μm, narrowly clavate, 4-spored; sterigmata up to 5 μm long. Pleurocystidia none. Cheilocystidia basidiole-like, hyalinous. Lamella trama subregular, somewhat bilateral towards lamella edge, made up of more or less parallel to interwoven hyphae. Oleiferous hyphae present in both lamella and pileus trama. Pileipellis a thick ixolattice (500–650 μm thick) of 1.5–10 μm wide hyphae which gelatinise and collapse, occasionally interspersed with oleiferous hyphae; the layer grading gradually into pileal trama. Clamp connections abundant in all tissues.
Known from Yunnan Province, south-western China.
Presumably ectomycorrhizal, in Pinus densata forests distributed at around alt. 2600–3500 m. Solitary to scattered, terrestrial.
The epithet "subalpinum" refers to the distribution range of the species.
China. Yunnan Province: Lijiang, Elephant Hill, 1 August 2011, Q. Cai 495 (
Catathelasma subalpinum is closely related to C. laorentou, which is also from south-western China. However, C. subalpinum differs by its higher elevation distribution and its association with Pinus densata, while C. laorentou has pale yellow to greyish-yellow basidiomes, associations with P. yunnanensis and Keteleeria evelyniana forests and is comparatively more common than C. subalpinum. Besides, C. subalpinum has much fewer oleiferous hyphae in the pileipellis. In addition, phylogenetic trees, reconstructed from ITS, 28S, TEF1 and concatenated ITS-LSU-TEF1, support the separation of C. subalpinum from C. laorentou.
Catathelasma subalpinum is also morphologically similar to C. ventricosum Peck) Singer in general appearance. However, C. subalpinum is found in coniferous forest dominated by Pinus densata in south-western China, while C. ventricosum is associated with hardwood trees in south-eastern North America (
Catathelasma singeri from USA is morphologically somewhat similar to C. subalpinum. However, C. singeri has a slimy viscid pileus that is more similar to species within the genus Hygrophorus Fr. (
Catathelasma evanescens, which was described from Wyoming (USA), is similar in general appearance and also has a high elevation distribution. However, C. evanescens has obvious distant lamellae, a hollow stipe, a volva-like veil around the base of the stipe and longer but narrower basidiospores measuring 14–17.5 × 3–5 μm, according to
1 | Pileus overall ochraceous, greyish-brown or reddish-brownish, lamellae with cylindrical or basidiole-like, yellow to brown cheilocystidia, under Pinus, Picea abies, Picea spp. or Abies spp | C. imperiale |
– | Pileus overall whitish, greyish-white, greyish-yellow or grey with age and sun exposure, sometimes brown in the centre, cheilocystidia basidiole-like, hyalinous, associated with Pinus spp. or Keteleeria spp | 2 |
2 | Pileus pale yellow to greyish-yellow, in forest dominated by Pinus yunnanensis or Keteleeria evelyniana in lower elevation (alt. 700–2900 m) | C. laorentou |
– | Pileus greyish-yellow to grey, in forest dominated by Pinus densata Mast. in higher elevation (alt. 2600–3500 m) | C. subalpinum |
Most of the characters used to identify fungal species are based on the morphology of basidiomes. However, the use of morphological characters to delimit species boundaries may be inadequate due to the paucity of measurable characters as basidiomes only represent a single and transient part of the fungal life cycle (
Based on stable isotope evidence, Catathelasma is ectomycorrhizal (
In China, Catathelasma imperiale is distributed in alpine regions in western and south-western provinces, associated with Picea such as Picea asperata or Abies spp. The finding of two new Catathelasma species in China viz., C. subalpinum associated with P. densata and C. laorentou associated with P. yunnanensis and/or K. evelyniana, demonstrated that species in Catathelasma probably possess host tree preferences, indicating a much narrower distribution than previously thought (e.g. the idea that C. imperiale and C. ventricosum are widely distributed in the Northern hemisphere). Thus, in addition to morphological characters, host tree species and geographic distribution can be of help in delimiting species within ectomycorrhizal genera such as Catathelasma. Indeed, mycorrhizal host association and geographic separation could contribute to fungal speciation as host-shift events can provide ecological opportunities for the diversification of ectomycorrhizal fungi (
Our study revealed that the geographical distribution differs amongst species of the genus: the previous records of C. ventricosum from China were based on incorrect identifications of C. laorentou or C. subalpinum, whereas C. imperiale, originally described from Europe, is indeed present in East Asia. Catathelasma laorentou and C. subalpinum seem to be endemic to south-western China (possibly East Asia), while C. ventricosum, C. evanescens, C. singeri and C. sp. seem to be endemic to North America, but more sampling is needed to confirm these assumptions.
The phylogeny of Catathelasma in this study, inferred from ITS, LSU and TEF1 data, revealed that this genus contains two major clades: the /subalpinum clade and the /imperiale clade (Fig.
Catathelasma evanescens is considered rare and has seldom been collected since it was described. Although efforts have been made to include C. evanescens in the present study by sequencing the specimens identified as C. evanescens (
We are very grateful to Drs Melissa Islam and Andrew Wilson of Denver Botanic Gardens (