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Three new species of Cortinarius subgenus Telamonia (Cortinariaceae, Agaricales) from China
expand article infoMeng-Le Xie§, Tie-Zheng Wei|, Yong-Ping Fu§, Dan Li§, Liang-Liang Qi, Peng-Jie Xing§, Guo-Hui Cheng#§, Rui-Qing Ji§, Yu Li§
‡ Northeast Normal University, Changchun, China
§ Jilin Agricultural University, Changchun, China
| Institute of Microbiology, Beijing, China
¶ Guangxi Academy of Agriculture Sciences, Nanning, China
# Shenyang Agricultural University, Shenyang, China
Open Access

Abstract

Cortinarius is an important ectomycorrhizal genus that forms a symbiotic relationship with certain trees, shrubs and herbs. Recently, we began studying Cortinarius in China and here we describe three new species of Cortinarius subg. Telamonia based on morphological and ecological characteristics, together with phylogenetic analyses. Cortinarius laccariphyllus sp. nov. (section Colymbadini) is associated with broadleaf trees, with strongly hygrophanous basidiomata, special Laccaria-like lamellae and white and extremely sparse universal veil. Cortinarius neotorvus sp. nov. (section Telamonia) is associated with broadleaf trees and is easily confused with C. torvus, but can be distinguished by the colour of the fresh basidiomes and the stipe usually somewhat tapering towards the base. Cortinarius subfuscoperonatus sp. nov. (section Fuscoperonati) is associated with coniferous trees, with subglobose to broadly ellipsoid spores and is closely related to C. fuscoperonatus. A key to the new species and similar species in sections Colymbadini, Telamonia and Fuscoperonati is provided.

Keywords

Ectomycorrhizal fungi, morphology, phylogeny, taxonomy

Introduction

Cortinarius (Pers.) Gray is one of the most species-rich agaric genera, with reportedly more than 2250 species worldwide (He et al. 2019). While most of the Cortinarius species were described from Europe and North America, there are also some species described from Oceania (e.g. Bougher and Hilton 1989; Soop 2005; Gasparini and Soop 2008), South America (e.g. Valenzuela and Esteve-Raventos 1994; Garnica et al. 2003; San-Fabian et al. 2018) and Asia (e.g. Miyauchi 2001; Peintner et al. 2003; Xie et al. 2019). It was assumed that more than 900 species occur in northern European countries, based on phylogenetic studies (Niskanen et al. 2012). At least 500 Cortinarius species were reported in North America (Bessette et al. 1997). Only 229 Cortinarius species have been reported in China (Teng 1963; Tai 1979; Shao and Xiang 1997; Wei and Yao 2013; Li et al. 2015; Xie 2018; Xie et al. 2019; Cheng et al. 2019; Wei and Liu 2019). Recently, many new species have been described, based on the phylogenetic analyses, together with morphological and ecological data (e.g. Bojantchev and Davis 2011; Wei and Yao 2013; Harrower et al. 2015; Brandrud et al. 2018a). Many studies showed that nrDNA ITS barcodes are typically effective in distinguishing Cortinarius species (e.g. Liimatainen et al. 2014; Garnica et al. 2016; Schmidt-Stohn et al. 2017; Brandrud et al. 2018b).

Previously, phylogenetic studies of Cortinarius have shown that many traditional infrageneric groups are artificial (Høiland & Holst-Jensen 2000; Garnica et al. 2003; Garnica et al. 2005; Niskanen 2008; Harrower et al. 2011), based on ITS+LSU datasets or only ITS datasets. Cortinarius subg. Telamonia (Fr.) Trog sensu lato was a traditional subgenus, based on moist to dry, strongly to weakly hygrophanous and often brown coloured pileus (Brandrud et al. 1989; Bidaud et al. 1994). Some species in traditional subgenus Telamonia sensu lato were classified into other subgenera and several new sections in subgenus Telamonia sensu stricto, based on phylogenetic studies (Niskanen et al. 2015; Soop et al. 2019). Sections Colymbadini Melot, Fuscoperonati Liimat. & Niskanen and Telamonia (Fr.) Gillot & Lucand, all belonging to subgenus Telamonia sensu stricto, are included in this paper.

The diverse ecosystems in China provide a conducive environment for the growth of Cortinarius species. Research, dedicated to the phylogeny and taxonomy of Chinese Cortinarius, was initiated in recent years. During field trips in the past years, many specimens of Cortinarius were collected from China. However, only two new Cortinarius species have been described and reported, based on Chinese specimens until now (Wei and Yao 2013; Xie et al. 2019). There are still many species that have never been reported according to the phylogenetic analyses, based on our materials. Further efforts are necessary to describe these species and reveal the species diversity of Cortinarius in China. In this study, three new species of the subgenus Telamonia sensu stricto were described, based on morphological and ecological characteristics, as well as phylogenetic analyses. An identification key to the new species and similar species in sections Colymbadini, Telamonia and Fuscoperonati is provided.

Materials and methods

Sampling and morphological studies

We collected specimens from northeast China and northwest China, two important floristic areas of China. Fresh basidiomata were photographed and noted under daylight in the field, dried in an oven at about 50 °C and deposited in the Herbarium of Mycology, Jilin Agricultural University (HMJAU).

The macroscopic characters were described from fresh basidiomata. Colour codes were taken from Kornerup and Wanscher (1978). The microscopic characters were examined from dried specimens mounted in 5% aqueous potassium hydroxide (KOH) and Melzer’s reagent using a Zeiss AX10 light microscope with a high-resolution 100× objective. Twenty to thirty mature basidiospores were measured (excluding apiculus and ornamentation) from each collection. The length/width ratio (Q) was calculated for individual spores. `X and `Q refer to the average value of basidiospores of each specimen. The basidia (ten basidia per collection), sterile cells of lamellar edge (20 sterile cells per collection) and hyphae of the lamellar trama were examined and measured from the pieces of lamellae. The pileipellis structure was studied from radial sections half-way from the pileus centre. Basidiospores, lamellar margin cells of this new species were photographed.

DNA extraction, PCR amplification and sequencing

We extracted the DNA from fresh tissue dried in silica gel by the NuClean PlantGen DNA Kit (CWBIO, China) and amplified the ITS region with primers ITS1F and ITS4 (White et al. 1990; Gardes and Bruns 1993).The PCR amplification progress followed Xie et al. (2019) and was sequenced by Sangon Biotech (Shanghai) Co. Ltd. The newly generated ITS sequences have been submitted to GenBank.

Data analysis

BLAST searches with the newly-generated ITS sequences were performed against NCBI (https://www.ncbi.nlm.nih.gov/) and UNITE (https://unite.ut.ee/) databases to retrieve similar sequences for the phylogenetic analyses (Table 1). C. armillatus (Fr.: Fr.) Fr. and C. paragaudis Fr. of section Armillati Kühner & Romagn. ex M.M. Moser, Schweiz. Z. Pilzk. were chosen as outgroup. Section Armillati belongs to subgenus Telamonia sensu stricto and is separated from other sections (Niskanen 2008; Niskanen et al. 2011).

Table 1.

ITS sequences used in the phylogenetic analysis. New species in bold.

Species Voucher GenBank accession No. Locality Reference
C. agathosmus TYPE CFP536 KC608590 Sweden Niskanen et al. (2013a)
C. ahsii TYPE MM19650703 (IB) KX882644 USA Ammirati et al. (2017)
C. ahsii JFA10303 (WTU) KX882649 USA Ammirati et al. (2017)
C. alboviolaceus HMJAU44214 MK552393 China This study
C. alboviolaceus HMJAU44245 MK234572 China Xie et al. (2019)
C. alboviolaceus HMJAU44347 MK552392 China This study
C. alboviolaceus F15809 FJ157005 Canada Harrower et al. (2011)
C. armeniacus HMJAU44408 MK552394 China This study
C. armeniacus F16352 FJ039573 Canada Harrower et al. (2011)
C. armillatus TYPE F256861 (S) NR131891 Sweden Kytövuori et al. (2005)
C. bulliardii CFP499 (S) JX114942 Sweden Ammirati et al. (2013)
C. caesioarmeniacus TYPE H7000901 KP137498 Canada Liimatainen (2014)
C. caesioarmeniacus HMJAU44409 MK552396 China This study
C. caesioarmeniacus HMJAU44403 MK552395 China This study
C. cinnabarinus IK85-1517 (H) JX114943 Finland Ammirati et al. (2013)
C. cinnabarinus TYPE CFP379 (S) JX114944 Sweden Ammirati et al. (2013)
C. coccineus TYPE 435745 (GK) JX114945 France Ammirati et al. (2013)
C. colynbadinus CFP1130 (S) JX127302 Sweden Ammirati et al. (2013)
C. colynbadinus TYPE F248443 (S) NR131819 Sweden Ammirati et al. (2013)
C. fructuodorus TN09-113 KC608582 USA Niskanen et al. (2013a)
C. fructuodorus TYPE H7001104 NR131827 USA Niskanen et al. (2013a)
C. fuscoperonatus SSt16-046 MF139754 Sweden Schmidt-Stohn et al. (2017)
C. fuscoperonatus CFP1470 JX407330 France Niskanen et al. (2013b)
C. fuscoperonatus CFP505 EU433390 Sweden GenBank/Liimatainen
C. laccariphyllus HMJAU44449 MK552380 China This study
C. laccariphyllus HMJAU44450 MK552381 China This study
C. millaresensis XC2011-200 MH784748 France Bidaud et al. (2017)
C. millaresensis XC2013-163 MH784752 France Bidaud et al. (2017)
C. nolaneiformis DB886 (BP) KJ206487 Hungary Dima et al. (2014)
C. nolaneiformis TYPE PRM857042 NR131833 Czech Republic Dima et al. (2014)
C. paragaudis TYPE F256858 (S) NR131814 Norway Niskanen et al. (2011)
C. privignofulvus TYPE AB00-10-128 (PC) MH784703 France Bidaud et al. (2017)
C. privignofulvus AB04-09-192 MH784714 France Bidaud et al. (2017)
C. neotorvus HMJAU44438 MK552383 China This study
C. neotorvus HMJAU44441 MK552384 China This study
C. neotorvus HMJAU44442 MK552385 China This study
C. neotorvus HMJAU44443 MK552386 China This study
C. neotorvus HMJAU44437 MK552382 China This study
C. rigidipes TYPE MM1962/0062 (IB) KJ206504 Switzerland Dima et al. (2014)
C. rigidipes IK95-1873 (H) KJ206506 Germany Dima et al. (2014)
C. subargyronotus TYPE H7018127 KP137494 Sweden Liimatainen (2014)
C. subfuscoperonatus HMJAU44446 MK552389 China This study
C. subfuscoperonatus HMJAU44447 MK552390 China This study
C. subfuscoperonatus HMJAU44445 MK552388 China This study
C. subfuscoperonatus HMJAU44444 MK552387 China This study
C. subfuscoperonatus HMJAU44448 MK552391 China This study
C. torvus TUB 011515 AY669668 Germany Garnica et al. (2005)
C. torvus IK98-1973 JX407337 Denmark Niskanen et al. (2013b)
C. torvus TF01-035 AJ889977 Denmark GenBank/Kjoller
C. turgidoides AB15-09-37 MH784723 France Bidaud et al. (2017)
C. turgidoides AB07-09-121 MH784717 France Bidaud et al. (2017)
C. uraceomajalis DB2291 (BP) KJ206511 Hungary Dima et al. (2014)
C. uraceomajalis DB2283 (BP) KJ206510 Hungary Dima et al. (2014)
C. uraceomajalis TYPE DB1623 (BP) NR131835 Hungary Dima et al. (2014)
C. uraceonemoralis ORS-ERDO99-15-1 (BP) KJ206520 Hungary Dima et al. (2014)
C. uraceonemoralis TYPE H7017739 NR131836 Italy Dima et al. (2014)
C. uraceus TYPE TN04-872 (H) NR131837 Finland Dima et al. (2014)
C. uraceus IK98-1607 (H) KJ206525 Finland Dima et al. (2014)
C. vernalisierraensis TYPE DBB33386 (UC) KX882652 USA Ammirati et al. (2017)
C. vernalisierraensis DBB15144 (UC) KX882653 USA Ammirati et al. (2017)

All ITS sequences were aligned and edited with BioEdit 7.0.9 (Hall 1999). ITS1 and ITS2 were delimited by comparison with the sequence KC608590, which is fully annotated in GenBank. For phylogenetic analyses, both Bayesian Inference (BI) and Maximum Likelihood (ML) methods were used. The analyses were performed with two partitions, one including ITS1 and ITS2, the other including coding sequences (SSU, 5.8S and LSU). The two partitions alignments were concatenated using Phyutility 2.2 (Smith and Dunn 2008). Exactly identical sequences were removed from the data matrix (Vadthanarat et al. 2017). For BI analysis, the best-fit model for each partition was determined using the Akaike Information Criterion (AIC), implemented in MrModeltest 2.3 (Nylander 2004). BI analysis was performed with MrBayes 3.2.6 (Ronquist and Huelsenbeck 2003). Markov Chain Monte Carlo (MCMC) chains were run for 200,000 generations, sampling every 100th generation at which point the average standard deviation of split frequencies was 0.00594. The first 25% of trees were discarded to build the 50% majority rule consensus tree. ML analysis was performed with RAxML (Stamatakis 2014) and implemented in raxmlGUI (Silvestro and Michalak 2012). All parameters in the ML analysis were kept as defaults, except for choosing GTRGAMMAI as the model of sequence evolution. For testing the support of the branches, rapid bootstrap analysis with 1,000 replicates was chosen. The resulting phylogenies were visualised in FigTree 1.4.3 (http://tree.bio.ed.ac.uk/software/figtree/).

Results

Phylogenetic analyses

The dataset for phylogenetic analyses contained 60 ITS sequences, representing 27 species (Table 1). The combined matrix of 33 samples with 583 nucleotide sites (including 366 informative sites) is available from TreeBASE under S26123 (study accession URL: http://purl.org/phylo/treebase/phylows/study/TB2:S26123). GTR+G and JC were chosen as the best-fit model for ITS1+ITS2 partition and SSU+5.8S+LSU partition, respectively. The BI and ML trees showed similar topologies with high statistical support values. The ML tree was selected as the representative phylogeny (Fig. 1). The Bayesian posterior probabilities (BPP) ≥ 0.95 and ML bootstrap values (ML) ≥ 75% are shown on the branches.

Figure 1. 

Maximum Likelihood tree inferred from ITS sequences. The tree is rooted with section Armillati. Bayesian posterior probabilities (≥ 0.95) and ML bootstrap values (≥ 75%) are shown on each branch (BPP / ML). New species in bold.

The phylogenetic analyses recovered seven sections, including outgroup (Fig. 1). Three new species were separated into individual lineages with high statistical support values and were distinct from their closest taxa, respectively. Cortinarius laccariphyllus had a distinct position with other species in section Colymbadini (BPP = 1.00, MLBS = 86%). The five collections of C. neotorvus (BPP = 0.96, MLBS = 98%) formed a sister relationship (BPP = 1.00, MLBS = 95%) with C. torvus (Fr.) Fr. in section Telamonia. Cortinarius subfuscoperonatus (BPP = 1.00, MLBS = 100%) formed a sister relationship (BPP = 1.00, MLBS = 99%) with C. fuscoperonatus Kühner in section Fuscoperonati.

Taxonomy

Cortinarius laccariphyllus Y. Li & M.L. Xie, sp. nov.

MycoBank No: 830780
Figures 2a, b, 3a, 4a

Diagnosis

Pileus 2.2–6.6 cm in diam., strongly hygrophanous, translucently striate. Lamellae distant, Laccaria-like when young. Universal veil white, extremely sparse. Basidiospores 7.7–9.7 × 4.5–5.8 μm. The ITS sequences differ from the sequences of other species of section Colymbadini by at least fifteen substitutions and eight indel positions.

Holotype

China. Jilin Province: Antu County, Liangjiang Town, Dongfanghong Village, broadleaf forest (Quercus mongolica dominated forest with some Juglans and Acer), 42°42'51"N, 128°01'10"E, alt. 640 m, 5 August 2017, M.L. Xie, HMJAU44449, GenBank No. (ITS) MK552380.

Etymology

The name refers to the Laccaria-like lamellae when young.

Description

Pileus 2.2–6.6 cm in diam., conical when young, then convex, strongly hygrophanous, reddish-brown (9E6–8), dark brown at the centre (8F6–8), margin to half-way translucently striate, rarely fibrillose, margin thin and wavy. Lamellae subadnate to emarginated, distant, Laccaria-like (Laccaria laccata (Scop.) Cooke) when young, reddish-brown (9E6–8) to rusty brown (6E8), edge slightly serrate. Stipe 4.2–6.6 cm long, 0.4–0.8 cm thick at apex, 0.2–0.5 cm thick at base, cylindrical to tapering towards base, dark brown (7F6) to black brown (7F3), surface with white fibrillose when young, these disappearing with age (excluding the base of stipe). Universal veil white, extremely sparse, soon disappearing. Context dark brown (7F6–8), strongly hygrophanous (pileus and stipe). Odour indistinct. Exsiccata brown (5F8) to black brown (7F5). UV fluorescence yellow on stipe, pileus and lamellar edge, strong at stipe base.

Figure 2. 

Basidiocarps of three newly-described species. a, b Cortinarius laccariphyllus (a, b HMJAU44449, holotype); c, d Cortinarius neotorvus (c HMJAU44441, holotype; d HMJAU44439); e, f Cortinarius subfuscoperonatus (e HMJAU44444, holotype; f HMJAU44445). Scale bars: 2 cm (a, b, d–f). Photographs by Meng-Le Xie.

Basidiospores 7.7–9.7 × 4.5–5.8 μm, Q = 1.43–1.84, `X = 8.0–8.5 × 4.8–5.2 μm, `Q = 1.66–1.70 (60 spores, 2 specimens), ellipsoid to amygdaloid, moderately and sharply verrucose, moderately dextrinoid. Basidia 4-spored, clavate, 23–39 × 7–9 μm, thin-walled, hyaline to olivaceous brown in 5% KOH. Lamellar edge fertile, with cylindrical-clavate sterile cells, 14–41 × 7–17 μm, thin-walled, hyaline in 5% KOH. Lamellar trama hyphae regular, pale olivaceous to olivaceous brown in 5% KOH, finely and densely encrusted. Pileipellis: epicutis hyphae cylindrical, 4–9.5 μm wide, dark olivaceous brown in 5% KOH, encrusted; hypocutis well developed, hyphae 11.5–53 μm wide, sub-cellular to cylindrical, slightly olivaceous in 5% KOH, finely encrusted. Pileus trama hyphae thin-walled, hyaline to slightly olivaceous in 5% KOH, smooth to finely encrusted. Clamp connections present.

ITS sequence

The ITS sequences of two specimens are 534 bp long and 100% identical. They differ from the sequences of other species of section Colymbadini (Niskanen et al. 2013a; Dima et al. 2014; Ammirati et al. 2017) by at least fifteen substitutions and eight indel positions.

Ecology and distribution

In broadleaf forest (Quercus mongolica dominated forest). Gregarious. Known from Jilin Province, China.

Additional specimens examined

China. Jilin Province: Antu County, Liangjiang Town, Dongfanghong Village, broadleaf forest (Quercus mongolica dominated forest with some Juglans and Acer), 42°42'51"N, 128°01'10"E, alt. 640 m, 5 August 2017, M.L. Xie, HMJAU44450, GenBank No. (ITS) MK552381.

Comments

Cortinarius laccariphyllus has strongly hygrophanous basidiomata, Laccaria-like (when young), with distantly-spaced lamellae and an extremely sparse, white veil. Morphologically, C. nolaneiformis (Velen.) Dima, Niskanen & Liimat. is similar to C. laccariphyllus due to the strongly hygrophanous pileus, similar colouration and similar size of spores. Cortinarius uraceomajalis Dima, Liimat., Niskanen & Bojantchev is also similar to C. laccariphyllus because of the black brown stipe and the striate pileus. However, both C. nolaneiformis and C. uraceomajalis have a yellowish veil and medium-spaced lamellae and lamellae not Laccaria-like. Furthermore, C. nolaneiformis is associated with broadleaf trees and also occurs in coniferous forest; C. uraceomajalis has a somewhat lighter brown pileus as well as generally smaller (av. 7.8–8.1 × 4.6–4.7 μm) and narrower (Qav. > 1.7) spores (Dima et al. 2014). In the phylogenetic analyses, C. laccariphyllus was well separated from other species in section Colymbadini.

Cortinarius neotorvus Y. Li, M.L. Xie & T.Z. Wei, sp. nov.

MycoBank No: 835346
Figures 2c, d, 3b, 4b

Diagnosis

Pileus 2–4.4 cm in diam., weakly hygrophanous, orange grey. Lamellae greyish-red when young. Stipe cylindrical to somewhat tapering towards base. Universal veil greyish-yellow. Context white, sometimes with violet tinge at the stipe apex. Basidiospores 8.5–10.2 × 5.8–6.9 μm. Lamellar edge sterile. The ITS sequence of the holotype differs from the sequences of other species in section Telamonia by at least six substitutions and five indels.

Holotype

China. Jilin Province: Antu County, Liangjiang Town, Dongfanghong Village, broadleaf forest (Quercus mongolica dominated forest with some Juglans and Acer), 42°42'51"N, 128°01'10"E, alt. 640 m, 5 August 2017, M.L. Xie, HMJAU44441, GenBank No. (ITS) MK552384.

Etymology

The name refers to Cortinarius torvus.

Description

Pileus 2–4.4 cm in diam., hemispherical when young, then convex to almost plane with a low, broad umbo, weakly hygrophanous, orange grey (5B2), paler at the margin, surface with greyish-white fibrillose. Lamellae emarginate, medium-spaced, yellowish-grey (4B2), greyish-red (9B4–6) when young, sometimes with violet tinge when young, margin paler, slightly serrate. Stipe 4.1–10.5 cm long, 0.5–0.7 cm thick at apex, 0.3–0.5 cm thick at base, cylindrical to somewhat tapering towards base, orange grey (5B2) when moist, sometimes with violet tinge at the apex when young, surface with richly whitish fibrillose. Universal veil greyish-yellow (4B3), copious, usually forming a girdle on the upper stipe, cortina white. Context white (A1), marbled watery when moist, sometimes with violet tinge at the apex of the stipe. Odour indistinct. Exsiccata brown (6E5) to dark brown (6F6).

Basidiospores 8.5–10.2 × 5.8–6.9 μm, Q = 1.31–1.67, `X = 9.0–9.9 × 6.1–6.5 μm, `Q = 1.45–1.61 (130 spores, 6 collections), ellipsoid, moderately verrucose, moderately dextrinoid. Basidia 4-spored, cylindrical to clavate, 27–53 × 7–12 μm, thin-walled, hyaline to olivaceous brown in 5% KOH. Lamellar edge sterile, sterile cells cylindrical-clavate, 11–26 × 3–9 μm, thin-walled, hyaline in 5% KOH. Lamellar trama hyphae regular, pale olivaceous in 5% KOH, smooth. Universal veil hyphae thin-walled, hyaline to pale olivaceous yellow in 5% KOH. Pileipellis: epicutis hyphae cylindrical, 2–6 μm wide, olivaceous brown in 5% KOH, smooth; hypocutis well developed, hyphae 15–38 μm wide, sub-cellular, thin-walled, hyaline in 5% KOH, smooth. Pileus trama hyphae thin-walled, hyaline to slightly olivaceous in 5% KOH, smooth. Clamp connections present.

Figure 3. 

Basidiospores of three newly-described species. a Cortinarius laccariphyllus (HMJAU44449, holotype); b Cortinarius neotorvus (HMJAU44441, holotype); c Cortinarius subfuscoperonatus (HMJAU44444, holotype). Photographs by Meng-Le Xie.

ITS sequence

The ITS sequences of C. neotorvus are 513–515 bp long (5 collections, Table 1). All four sequences (MK552384 holotype, MK552385, MK552386 and MK552382) are identical and only MK552383 has 2 bp indels. The ITS sequence of C. neotorvus (MK552384, holotype) differs from the sequences of other species in section Telamonia by at least six substitutions and five indels.

Ecology and distribution

In broadleaf forest (Quercus mongolica dominated forest). Solitary or gregarious. Known from Jilin and Heilongjiang Province, China.

Additional specimens examined

China. Heilongjiang Province: Heihe City, Wudalianchi Scenic Area, broadleaf forest (Quercus mongolica), 48°39'15"N, 126°28'18"E, alt. 290 m, 16 August 2017, M.L. Xie, HMJAU44442, GenBank No. (ITS) MK552385; 12 August 2018, P.J. Xing, HMJAU44440; Heihe City, Shengshan National Nature Reserve, broadleaf forest (Quercus mongolica dominated forest with some Tilia and Alnus), 49°30’N, 126°43’E, alt. 300 m, 11 September 2017, G.H. Cheng, HMJAU44443, GenBank No. (ITS) MK552386. Jilin Province: Yanji City, Sandaowan Town, broadleaf forest (Quercus mongolica), 43°16'10"N, 129°07'19"E, alt. 580 m, 8 September 2018, M.L. Xie, HMJAU44437, GenBank No. (ITS) MK552382, HMJAU44438, GenBank No. (ITS) MK552383, HMJAU44439.

Comments

Cortinarius neotorvus is easily confused with C. torvus due to highly similar morphology. Morphologically, the lamellae of C. torvus are adnate to subdecurrent and distant (Bidaud et al. 1999; Breitenbach and Kränzlin 2000; Soop 2014) and the pileus colour of C. torvus is usually darker and with a violet tinge, as well as the stipe usually being bulbous at the base (Consiglio et al. 2003). In molecular data, the ITS sequence of C. neotorvus (MK552384, holotype) differ from the sequences of C. torvus (AY669668, JX407337) by six substitutions and five indels. In the phylogenetic analyses, the five specimens of C. neotorvus were placed in separate monophyletic lineages (BPP = 0.96, MLBS = 90%) and formed a sister relationship with C. torvus.

Cortinarius subfuscoperonatus Y. Li & M.L. Xie, sp. nov.

MycoBank No: 830782
Figures 2e, f, 3c, 4c

Diagnosis

Pileus 1.6–4.4 cm in diam. Context white, greyish-brown when moist. Basidiospores 9.5–12.1 × 7.9–9.7 μm. The ITS sequence of the holotype differs from other species in section Fuscoperonati by at least six substitutions and six indels.

Holotype

China. Gansu Province: Zhangye City, Minle County, Gansu Qilianshan National Nature Reserve, coniferous forest (Picea crassifolia), 38°17'55"N, 100°45'54"E, alt. 2860 m, 9 August 2018, M.L. Xie, HMJAU44444, GenBank No. (ITS) MK552387.

Etymology

The name refers to its affinity to Cortinarius fuscoperonatus.

Description

Pileus 1.6–4.4 cm in diam., hemispherical when young, then low convex, weakly hygrophanous, pale greyish-brown (6C3), sometimes reddish-brown (9E5–9E6) to dark brown (6F6–6F8), surface with greyish-brown fibrillose, margin wavy with age. Lamellae emarginate, medium-spaced, reddish-brown to rusty brown (7D6–7E7), margin even when young, then slightly serrate. Stipe 2.3–7.5 cm long, 0.8–1.3 cm thick at apex, 1.5–2.5 cm thick at base, clavate, white to pale grey (E2), mycelium white at the base. Universal veil greyish-brown (6C2), rich, usually forming an annular band on the middle part and distinct belts or zones lower down. Context white (A1), greyish-brown (7F8) and marbled watery when moist, strongly hygrophanous near pileus and lamellae. Odour somewhat radish-like. Chemical reaction: pileus and context (fresh basidiomata) are dark black brown (8F3) with 10% KOH. Exsiccata brown (6E5) to dark brown (6F5).

Figure 4. 

Margin cells of three newly-described species. a Cortinarius laccariphyllus (HMJAU44449, holotype); b Cortinarius neotorvus (HMJAU44441, holotype); c Cortinarius subfuscoperonatus (HMJAU44444, holotype). Photographs by Meng-Le Xie.

Basidiospores 9.5–12.1 × 7.9–9.7 μm, Q = 1.10–1.45, `X = 10.3–11.2 × 8.0–8.6 μm, `Q = 1.24–1.33 (135 spores, 5 collections), subglobose to broadly ellipsoid, moderately to strongly verrucose, strongly dextrinoid. Basidia 4-spored, clavate, 35–58 × 10–13 μm, thin-walled, hyaline to olivaceous brown in 5% KOH. Lamellar edge fertile, with cylindrical-clavate sterile cells, 13–27 × 6–11 μm, thin-walled, hyaline to slightly olivaceous yellow in 5% KOH. Lamellar trama hyphae regular, pale olivaceous to olivaceous brown in 5% KOH, smooth. Pileipellis: epicutis hyphae cylindrical, 4–12 μm wide, slightly olivaceous brown to olivaceous brown in 5% KOH, some hyphae finely encrusted; hypocutis well developed, hyphae 24–89 × 15–29 μm, sub-cellular to sub-cylindrical, thin-walled, hyaline to slightly olivaceous brown in 5% KOH, smooth. Pileus trama hyphae almost thin-walled, hyaline in 5% KOH, smooth. Clamp connections present.

ITS sequence

The ITS sequences of C. subfuscoperonatus are 524–525 bp long (5 collections, Table 1) and distinct from other members of section Fuscoperonatus. The ITS sequence of C. subfuscoperonatus (MK552387, holotype) differs from C. fuscoperonatus by six substitutions and six indels.

Ecology and distribution

In coniferous forest (Picea crassifolia dominated forest). Solitary or gregarious. Known from Gansu Province, China.

Additional specimens examined

China. Gansu Province: Zhangye City, Minle County, Gansu Qilianshan National Nature Reserve, coniferous forest (Picea crassifolia), 38°17'55"N, 100°45'54"E, alt. 2860 m, 9 August 2018, M.L. Xie, HMJAU44445, GenBank No. (ITS) MK552388; Zhangye city, Su’nan Yugu Autonomous County, Gansu Qilianshan National Nature Reserve, coniferous forest (Picea crassifolia dominated forest, occasionally with Juniperus), 38°44'57"N, 99°47'56"E, alt. 3010 m, 10 August 2018, M.L. Xie, HMJAU44446, GenBank No. (ITS) MK552389, HMJAU44447, GenBank No. (ITS) MK552390; Zhangye city, Su’nan Yugu Autonomous County, Gansu Qilianshan National Nature Reserve, coniferous forest (Picea crassifolia dominated forest, occasionally with Juniperus), 38°33'13"N, 100°41'75"E, alt. 2700 m, 11 August 2018, M.L. Xie, HMJAU44448, GenBank No. (ITS) MK552391.

Comments

Cortinarius subfuscoperonatus corresponds well to the characteristics of section Fuscoperonati, with weak hygrophanous pileus, an annular band on the middle stipe and distinct belts or zones lower down, large spores (> 10 µm long) and grow in coniferous forests. Cortinarius fuscoperonatus was previously placed in section Bovini M.M. Moser (Bidaud et al. 2009; Soop 2014) and Armillati (Brandrud et al. 1992), until Niskanen et al. (2015) placed it in section Fuscoperonati. Cortinarius subfuscoperonatus has remarkably similar morphological characteristics to C. fuscoperonatus, apart from the spores of C. fuscoperonatus being narrower (9.7–11.6 × 6.6–7.7 µm), the pileus being chocolate brown to blackish-brown and being fine fibrous to fine scaly (Schmidt-Stohn et al. 2017). In addition, C. subfuscoperonatus formed a sister relationship with C. fuscoperonatus and was well separated according to the phylogenetic analyses. C. subfuscoperonatus could be considered as the second species in section Fuscoperonati.

Key to new species and morphologically-similar species in sections Colymbadini, Telamonia and Fuscoperonati

1 Basidiomata medium. Pileus more or less brown, strongly hygrophanous. Stipe usually cylindrical. Universal veil sparse. With positive yellow UV reaction. Associated with coniferous and/or broadleaf trees. Spores ellipsoid to amygdaloid (section Colymbadini) 2
Basidiomata medium to large. Pileus more or less brown and hygrophanous. Stipe cylindrical to clavate. Universal veil white to greyish-yellow, sometimes with violet tinge, usually forming a ring at the middle stipe. Associated with coniferous and/or broadleaf trees (section Telamonia) 3
Basidiomata medium to large. Pileus brown and weakly hygrophanous. Stipe clavate to slightly bulbous. Universal veil greyish-brown to blackish-brown. Associated with coniferous trees. Spores subglobose to ellipsoid, moderately to strongly verrucose (section Fuscoperonati) 4
2 Pileus strongly hygrophanous, reddish-brown to dark brown, surface translucently striate. Lamellae distant, Laccaria-like when young. Stipe cylindrical to tapering towards base, hollow. Universal veil white, extremely sparse. Odour indistinct. Positively yellow UV fluorescence (exsiccata). Associated with broadleaf trees. Spores ellipsoid to amygdaloid, on average 8.0–8.5 × 4.8–5.2 μm. C. laccariphyllus
Pileus strongly hygrophanous, yellowish-brown to brown, margin striate. Lamellae medium-spaced. Stipe cylindrical to tapering towards base, not hollow. Universal veil yellow, very sparse. Odour similar to raw vegetables. Usually yellow UV fluorescence at stipe. Associated with broadleaf trees. Spores amygdaloid to narrowly amygdaloid, on average 7.8–8.1 × 4.6–4.7 μm C. uraceomajalis
Pileus strongly hygrophanous, dark greyish-brown to dark brown, margin slightly striate. Lamellae medium-spaced to fairly distant, margin whitish when young. Stipe cylindrical to clavate, sometimes tapering downwards, sometimes hollow. Universal veil yellow. Strong yellow UV fluorescence at stipe, dull yellowish-brown at pileus, lamellae and context. Associated with coniferous and broadleaf trees. Spores amygdaloid to weakly ellipsoid, on average 8.1–8.6 × 4.8–5.1 μm C. nolaneiformis
3 Pileus pale greyish-yellow, paler at the margin, weakly hygrophanous. Lamellae emarginate, medium-spaced, greyish-red when young, sometimes with violet tinge. Stipe cylindrical to somewhat tapering towards base, pale greyish-yellow. Odour indistinct. Spores ellipsoid, on average 9.0–9.9 × 6.1–6.5 μm C. neotorvus
Pileus greyish-brown to chestnut brown, usually with violet tinge at the margin, weakly hygrophanous. Lamellae adnate, subdecurrent to distant, greyish-brown, with violet tinge. Stipe clavate, usually bulb at the base. Odour acidulous. Spores ellipsoid, 8–10.5 × 6–7 μm C. torvus
4 Pileus pale greyish-brown, sometimes reddish-brown to dark brown, margin wavy with age, with greyish-brown fibrillose. Stipe clavate. Spores subglobose to broadly ellipsoid, on average 10.3–11.2 × 8.0–8.6 μm C. subfuscoperonatus
Pileus chocolate brown to blackish-brown, pale greyish-brown at the edge, fine fibrous to fine scaly. Stipe clavate, with a bulb at the base. Spores ellipsoid to broadly ellipsoid, 9.7–11.6 × 6.6–7.7 μm C. fuscoperonatus

Discussion

Cortinarius is the most species-rich genus of Agaricales, with most of the described species distributed in the Northern Hemisphere. However, so far, little has been done on Cortinarius taxonomy in north-eastern Asia or even in the whole of Asia, leaving an important gap in our knowledge of this genus (Horak 1983). The flora of northern China has a strong affinity shared with the circumboreal areas of Europe and western North America but also harbours some floristic elements with a tropical and subtropical affinity (Wu 1979). Some Cortinarius species in northern China are the same as those in Europe and western North America (e.g. Xie 2018; Cheng et al. 2019; Wei and Liu 2019). However, there are also some endemic species in China (Wei and Yao 2015; Xie et al. 2019). Thus far, only 229 Cortinarius species (about 10% in the world) have been reported in China. Therefore, studies focusing on Chinese Cortinarius are needed.

In this study, we described the phylogenetic relationships amongst the three new species and other species, based on the ITS sequences. However, multiple genes should be used in future studies to describe more complex phylogenetic relationships in Cortinarius, which some mycologists have conducted. Peintner et al. (2002) assessed the phylogenetic relationships of Rozites, Cuphocybe and Rapacea by molecular phylogenetic approaches, based on ITS and LSU. Frøslev et al. (2005) analysed the phylogeny of Cortinarius subgenus Phlegmacium, a taxonomically difficult group, based on ITS, RPB1 and RPB2. They speculated that the sequences from RNA polymerase II genes have the potential for resolving the phylogenetic problems of Cortinarius. Later, the study of Frøslev et al. (2007) showed that the delimitation of species, based on ITS sequences, is more consistent with a conservative morphological species concept and there is considerable potential for using ITS sequence data as a barcode for section Calochroi. Soop et al. (2019) studied the global supraspecific taxonomy of Cortinarius by the phylogenetic approach, based on ITS, LSU, RPB1 and RPB2. Both ITS and LSU datasets and ITS, LSU, RPB1 and RPB2 datasets showed satisfactory results. Although phylogenetic analyses of Cortinarius have made significant progress in Europe, North America and even in Australasia, few phylogenetic analyses of Cortinarius, based on Chinese materials have been carried out. According to our analysis of ITS data, there are presently less than 200 accessions (excluding sequences obtained from mycorrhiza) from China in GenBank. Thus, the dedicated collection of specimens and studying the phylogeny of Cortinarius, based on the ITS or, preferably, multiple genes, are important contributions to the global phylogenetic framework of Cortinarius.

Acknowledgements

The study was supported by China Agriculture Research System (No. CARS20), Special Fund for Agro-scientific Research in the Public Interest (No. 201503137), Overseas Expertise Introduction Project for Discipline Innovation (111 Center) (No. D17014), National Natural Science Foundation of China (No. 31270072), the Special Funds for the Young Scholars of Taxonomy of the Chinese Academy of Sciences (No. ZSBR-001). We would like to express our gratitude to the people in the Engineering Research Center of Edible and Medicinal Fungi, Ministry of Education, Jilin Agricultural University, including Dr. Bo Zhang for her suggestions to improve our work, Ms. Yang Yang and Ms. Yu-Xiu Guo for their help during molecular experiments, Mr. Yang Wang, Mr. Zhu-Shan Liu and Mr. Zhi-Hui Luo for their help during the field trips in Jilin and Heilongjiang, as well as Prof. Sheng-Long Wei and Ms. Qian-Qian Liang (Gansu Engineering Laboratory of Applied Mycology, Hexi University, China) for their kind help during the field trips in Gansu. We thank Dr. Frederick Leo Sossah for his kind-hearted and excellent technical assistance with the English language correction. We also thank the reviewers, Bálint Dima, Joseph F. Ammirati and Jerry Adrian Cooper, for their suggestions and corrections to improve our work.

References

  • Ammirati JF, Hughes KW, Liimatainen K, Niskanen T, Matheny PB (2013) Cortinarius hesleri from eastern North America and related species from Europe and western North America. Botany 91: 91–98. https://doi.org/10.1139/cjb-2012-0154
  • Ammirati JF, Niskanen T, Liimatainen K, Bojantchev D, Peintner U, Kuhnert-Finkernagel R, Cripps C (2017) Spring and early summer species of Cortinarius, subgenus Telamonia, section Colymbadini and /Flavobasilis, in the mountains of western North America. Mycologia 109(3): 443–458. https://doi.org/10.1080/00275514.2017.1349468
  • Bessette A, Bessette AR, Fischer DW (1997) Mushrooms of northeastern North America. Syracuse University Press, Syracuse.
  • Bidaud A, Bellanger JM, Carteret X, Reumaux P, Moënne-Loccoz P (2017) Atlas des Cortinaires XXVI. Éditions Fédération Mycologique Dauphiné-Savoie, Meyzieu.
  • Bidaud A, Moënne-Loccoz P, Reumaux P (1994) Atlas des Cortinaires. Clé générale des sous-genres, sections, sous-sections et séries. Éditions Fédération Mycologique Dauphiné-Savoie, Meyzieu.
  • Bidaud A, Moënne-Loccoz P, Reumaux P, Carteret X (2009) Atlas des Cortinaires XVIII. Éditions Fédération Mycologique Dauphiné-Savoie, Meyzieu.
  • Bidaud A, Moënne-Loccoz P, Reumaux P, Henry R (1999) Atlas des Cortinaires IX. Éditions Fédération Mycologique Dauphiné-Savoie, Meyzieu.
  • Bojantchev D, Davis RM (2011) Cortinarius callimorphus, a new species from northern California. Mycotaxon 117(1): 1–8. https://doi.org/10.5248/117.1
  • Brandrud TE, Frøslev TG, Dima B (2018b) Rare, whitish-pale ochre Cortinarius species of section Calochroi from calcareous Tilia forests in South East Norway. Agarica 38: 3–20.
  • Brandrud TE, Lindström H, Marklund H, Melot J, Muskos S (1989) Cortinarius flora Photographica I. Cortinarius HB, Matfors.
  • Brandrud TE, Lindström H, Marklund H, Melot J, Muskos S (1992) Cortinarius Flora Photographica II. Cortinarius HB, Matfors.
  • Brandrud TE, Schmidt-Stohn G, Liimatainen K, Niskanen T, Frøslev TG, Soop K, Bojantchev D, Kytövuori I, Jeppesen TS, Bellù F, Saar G, Oertel B, Ali T, Thines M, Dima B (2018a) Cortinarius section Riederi: taxonomy and phylogeny of the new section with European and North American distribution. Mycological Progress 17(12): 1323–1354. https://doi.org/10.1007/s11557-018-1443-0
  • Breitenbach J, Kränzlin F (2000) Fungi of Switzerland. Vol. 5 Agarics (3rd part) Cortinariaceae. Mycologia Luzern, Lucerna.
  • Cheng GH, An XY, Xie ML, Li Y (2019) New records of Cortinarius species collected from Heilongjiang Province in China. Journal of Fungal Research 17(2): 67–73.
  • Consiglio G, Antonini D, Antonini M (2003) Il Genere Cortinarius in Italia (Parte prima). Associazione Micologica Bresadola, Luglio.
  • Dima B, Liimatainen K, Niskanen T, Kytövuori I, Bojantchev D (2014) Two new species of Cortinarius, subgenus Telamonia, sections Colymbadini and Uracei, from Europe. Mycological Progress 13(3): 867–879. https://doi.org/10.1007/s11557-014-0970-6
  • Garnica S, Schön ME, Abarenkov K, Riess K, Liimatainen K, Niskanen T, Dima B, Soop K, Frøslev TG, Jeppesen TS, Peintner U, Kuhnert-Finkernagel R, Brandrud TE, Saar G, Oertel B, Ammirati JF (2016) Determining threshold values for barcoding fungi: lessons from Cortinarius (Basidiomycota), a highly diverse and widespread ectomycorrhizal genus. FEMS Microbiology Ecology 92(4): fiw045. https://doi.org/10.1093/femsec/fiw045
  • Garnica S, Weiß M, Oberwinkler F (2003) Morphological and molecular phylogenetic studies in South American Cortinarius species. Mycological Research 107(10): 1143–1156. https://doi.org/10.1017/S0953756203008414
  • Garnica S, Weiß M, Oertel B, Oberwinkler F (2005) A framework for a phylogenetic classification in the genus Cortinarius (Basidiomycota, Agaricales) derived from morphological and molecular data. Botany 83(11): 1457–1477. https://doi.org/10.1139/b05-107
  • Gasparini B, Soop K (2008) Contribution to the knowledge of Cortinarius (Agaricales, Cortinariaceae) of Tasmania (Australia) and New Zealand. Australasian Mycologist 27(3): 173–203.
  • Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41(41): 95–98.
  • Harrower E, Ammirati JF, Cappuccino AA, Ceska O, Kranabetter JM, Kroeger P, Lim S, Taylor T, Berbee ML (2011) Cortinarius species diversity in British Columbia and molecular phylogenetic comparison with European specimen sequences. Botany 89(11): 799–810. https://doi.org/10.1139/b11-065
  • Harrower E, Bougher NL, Winterbottom C, Henkel TW, Horak E, Matheny PB (2015) New species in Cortinarius section Cortinarius (Agaricales) from the Americas and Australasia. MycoKeys 11: 1–21. https://doi.org/10.3897/mycokeys.11.5409
  • He MQ, Zhao RL, Hyde KD, Begerow D, Kemler M, Yurkov A, McKenzie EHC, Raspé O, Kakishima M, Sánchez-Ramírez S, Vellinga EC, Halling R, Papp V, Zmitrovich IV, Buyck B, Ertz D, Wijayawardene NN, Cui BK, Schoutteten N, Liu XZ, Li TH, Yao YJ, Zhu XY, Liu AQ, Li GJ, Zhang MZ, Ling ZL, Cao B, Antonín V, Boekhout T, da Silva BDB, De Crop E, Decock C, Dima B, Dutta AK, Fell JW, Geml J, Ghobad-Nejhad M, Giachini AJ, Gibertoni TB, Gorjón SP, Haelewaters D, He SH, Hodkinson BP, Horak E, Hoshino T, Justo A, Lim YW, Menolli Jr. N, Mešić A, Moncalvo J, Mueller GM, Nagy LG, Nilsson RH, Noordeloos M, Nuytinck J, Orihara T, Ratchadawan C, Rajchenberg M, Silva-Filho AGS, Sulzbacher MA, Tkalčec Z, Valenzuela R, Verbeken A, Vizzini A, Wartchow F, Wei TZ, Weiß M, Zhao CL, Kirk PM (2019) Notes, outline and divergence times of Basidiomycota. Fungal Diversity 99: 105–367. https://doi.org/10.1007/s13225-019-00435-4
  • Horak E (1983) Mycogeography in the South Pacific region: Agaricales, Boletales. Australian Journal of Botany supplement 10: 1–41.
  • Kornerup A, Wanscher JHK (1978) The Methuen Handbook of Colour (3rd edn). Eyre Methuen Ltd. Reprint, London, UK.
  • Kytövuori I, Niskanen T, Liimatainen K, Lindström H (2005) Cortinarius sordidemaculatus and two new related species, C. anisatus and C. neofurvolaesus in Fennoscandia (Basidiomycota, Agaricales). Karstenia 45: 33–49. https://doi.org/10.29203/ka.2005.402
  • Li GJ, Zhao D, Li SF, Wen HA (2015) Russula chiui and R. pseudopectinatoides, two new species from southwestern China supported by morphological and molecular evidence. Mycological Progress 14: 33. https://doi.org/10.1007/s11557-015-1054-y
  • Liimatainen K, Niskanen T, Dima B, Kytövuor I, Ammirati JF, Frøslev TG (2014) The largest type study of Agaricales species to date: bringing identification and nomenclature of Phlegmacium (Cortinarius) into the DNA era. Persoonia 33: 98–140. https://doi.org/10.3767/003158514X684681
  • Niskanen T (2008) Cortinarius subgenus Telamonia pp in North Europe. PhD Thesis, University of Helsinki, Finland.
  • Niskanen T, Kytövuori I, Bendiksen E, Bendiksen K, Brandrud TE, Frøslev TG, Høiland K, Jeppesen TS, Liimatainen K, Lindström H (2012) Cortinarius (Pers.) Gray. In: Knudsen H, Vesterholt J (Eds) Funga Nordica, 2nd revised edition. Agaricoid, boletoid, clavarioid, cyphelloid and gastroid genera, Nordsvamp, Copenhagen, Denmark, 762–763.
  • Niskanen T, Kytövuori I, Liimatainen K (2011) Cortinarius section Armillati in northern Europe. Mycologia 103(5): 1080–1101. https://doi.org/10.3852/10-350
  • Niskanen T, Kytövuori I, Liimatainen K, Lindström H (2013b) The species of Cortinarius, section Bovini, associated with conifers in northern Europe. Mycologia 105(4): 977–993. https://doi.org/10.3852/12-320
  • Niskanen T, Liimatainen K, Ammirati JF (2013a) Five new Telamonia species (Cortinarius, Agaricales) from western North America. Botany 91(7): 478–485. https://doi.org/10.1139/cjb-2012-0292
  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala.
  • Peintner U, Moser MM, Thomas KA, Manimohan P (2003) First records of ectomycorrhizal Cortinarius species (Agaricales, Basidiomycetes) from tropical India and their phylogenetic position based on rDNA ITS sequences. Mycological Research 107(4): 506–508. https://doi.org/10.1017/S0953756203007585
  • San-Fabian B, Niskanen T, Liimatainen K, Kooij PW, Mujic AB, Truong C, Peintner U, Dresch P, Nouhra E, Matheny PM, Smith ME (2018) New species of Cortinarius sect. Austroamericani, sect. nov. , from South American Nothofagaceae forests, Mycologia 110(6): 1127–1144. https://doi.org/10.1080/00275514.2018.1515449
  • Schmidt-Stohn G, Brandrud TE, Dima B (2017) Interessante Cortinarius–Funde der Journées européennes du Cortinaire 2016 in Borgsjö, Schweden. Journal des JEC 19: 28–52.
  • Shao LP, Xiang CT (1997) Forest Mushrooms of China. Northeast Forestry University Press, Haerbin.
  • Soop K (2014) Cortinarius in Sweden (14 edition). Éditions Scientrixk, Sweden.
  • Soop K, Dima B, Cooper JA, Park D, Oertel B (2019) A phylogenetic approach to a global supraspecific taxonomy of Cortinarius (Agaricales) with an emphasis on the southern mycota. Persoonia 42: 261–290. https://doi.org/10.3767/persoonia.2019.42.10
  • Tai FL (1979) Sylloge fungorum sinicorum. Science Press, Beijing.
  • Teng SC (1963) Fungi of China. Science Press, Beijing.
  • Wei TZ, Liu TZ (2019) Resource survey of macro-basidiomycetes in southern Greater Khingan Mountains, Chifeng City. Journal of Liaocheng University 32(6): 76–89.
  • Wei TZ, Yao YJ (2013) Cortinarius korfii, a new species from China. Mycosystema 32(3): 557–562.
  • White TJ, Bruns TD, Lee SB, Taylor JW, Innis MA, Gelfand DH, Sninsky JJ (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, et al. (Eds) PCR protocols: a guide to methods and applications: 315–322. Academic Press, New York. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
  • Wu CY (1979) The regionalization of Chinese flora. Acta Botanica Yunnanica 1: 1–22.
  • Xie ML (2018) Resources and Taxonomy of Cortinarius in Northeast of China. MA thesis, Jilin Agricultural University, China.
  • Xie ML, Li D, Wei SL, Ji RQ, Li Y (2019) Cortinarius subcaesiobrunneus sp. nov., (Cortinariaceae, Agaricales) a new species from northwest China. Phytotaxa 392(3): 217–224. https://doi.org/10.11646/phytotaxa.392.3.4