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Article

Morphological and Phylogenetic Evidence Reveal Five New Telamonioid Species of Cortinarius (Agaricales) from East Asia

by
Meng-Le Xie
1,2,
Chayanard Phukhamsakda
1,
Tie-Zheng Wei
3,
Ji-Peng Li
1,
Ke Wang
3,
Yang Wang
1,4,
Rui-Qing Ji
1,* and
Yu Li
1,2,*
1
Engineering Research Center of Chinese Ministry of Education for Edible and Medicinal Fungi, Jilin Agricultural University, Changchun 130118, China
2
Life Science College, Northeast Normal University, Changchun 130024, China
3
State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China
4
College of Plant Protection, Shenyang Agricultural University, Shenyang 110866, China
*
Authors to whom correspondence should be addressed.
J. Fungi 2022, 8(3), 257; https://doi.org/10.3390/jof8030257
Submission received: 4 February 2022 / Revised: 1 March 2022 / Accepted: 1 March 2022 / Published: 2 March 2022
(This article belongs to the Special Issue Polyphasic Identification of Fungi)
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Abstract

:
Five new Cortinarius species, C. neobalaustinus, C. pseudocamphoratus, C. subnymphatus, C. wuliangshanensis and C. yanjiensis spp. nov., are proposed based on a combination of morphological and molecular evidence. Cortinarius neobalaustinus is characterized by a very weakly hygrophanous and yellowish-brown to brown pileus and small and weakly verrucose basidiospores. Cortinarius pseudocamphoratus can be characterized by a viscid pileus, a strongly unpleasant smell, amygdaloid to somewhat ellipsoid basidiospores and lageniform to subfusiform cheilocystidia. Cortinarius subnymphatus is identified by a strongly hygrophanous pileus that is reddish-brown with a black-brown umbo, a yellowish universal veil and ellipsoid to subamygdaloid basidiospores. Cortinarius wuliangshanensis is characterized by a moderately to strongly hygrophanous, translucently striated and yellowish to reddish-brown pileus and rather weakly and moderately verrucose basidiospores. Cortinarius yanjiensis is distinguished by a weakly to moderately hygrophanous and yellowish to brown pileus and moderately to rather strongly verrucose basidiospores. The phylogenetic analyses were performed with maximum likelihood and Bayesian inference methods based on the data set of nuc rDNA ITS1-5.8S-ITS2 (ITS), D1–D2 domains of nuc 28S rDNA (28S) and RNA polymerase II second largest subunit (rpb2), and the results show that C. neobalaustinus, C. wulianghsanensis and C. yanjiensis cluster in sect. Illumini, C. pseudocamporatus belongs to sect. Camphorati and C. subnymphatus belongs to sect. Laeti. In addition, a study of basidiospores under field emission scanning electron microscopy (FESEM) was conducted. An identification key for the five new species and related species from China is also provided.

1. Introduction

Cortinarius (Pers.) Gray is an important ectomycorrhizal agaric genus in Agaricales and few species have sequestrate basidiome morphologies [1,2,3]. Although Cortinarius is known to be the largest basidiomycete genus with more than 3000 species worldwide [4], there are many new species described every year [5,6,7]. This could be due to the application of a polyphasic approach that combines phylogenetic and morphological methods [8,9,10].
Telamonia (Fr.) Trog is a traditional Cortinarius subgenus characterized by a dry to more or less hygrophanous pileus and stipe, often without bright colours [3,11]. However, some species have a more or less bluish tinge and/or a brightly coloured universal veil [3,11]. Some phylogenetic studies have shown that this subgenus is polyphyletic, while many lower ranking taxa formed well-supported monophyletic clades [3,12,13,14]. The subgenus is divided into subg. Telamonia s.s. and other telamonioid sections, in which subg. Telamonia s.s. is a monophyletic entity containing the vast majority of species, and another group is a polyphyletic assembly of several sections of Camphorati (Liimat., Niskanen & Ammirati) Soop, B. Oertel & Dima, Illumini (Liimat., Niskanen & Kytöv.) Soop, B. Oertel & Dima, Laeti Melot, Obtusi Melot, etc. [14].
In this study, five undescribed telamonioid species of Cortinarius were collected from China. Morphological characteristics and molecular phylogenetic analyses supported the recognition of five new species within Cortinarius and confirmed their infrageneric taxonomic status.

2. Materials and Methods

2.1. Specimens and Morphological Description

The studied specimens were deposited in the Herbarium of Mycology, Jilin Agricultural University (HMJAU), and the Fungarium of the Institute of Microbiology, Chinese Academy of Sciences (HMAS). Macroscopic characteristics were based on field notes and photos captured in the field. Micromorphological data were obtained from the dried specimens, which were observed in 5% potassium hydroxide water solution and/or Melzer’s reagent under a light microscope, following Xie et al. [15]. The ornamentation of basidiospores was studied using a Hitachi, model SU8010, field emission scanning electron microscope (FESEM) in Jilin Agricultural University. Basidiospore measurements, averages based on 30–40 basidiospores per collection, and measurements in parentheses are exceptional. Factor Q is the value of the length divided by width.

2.2. Molecular Phylogeny

Total DNA was extracted from dried specimens, using a NuClean PlantGen DNA Kit (CWBIO, Taizhou, China). Primers ITS1F and ITS4 were used to amplify the nrDNA ITS1-5.8S-ITS2 (ITS) region [16,17]. The D1–D2 domains of nuc 28S rDNA (28S) were amplified with primers LR0R and LR7 [18]. The RNA polymerase II second largest subunit (rpb2) were amplified with primers bRPB2-6F and bRPB2-7.1R [19,20]. The PCR procedures are as follows: for the ITS region, initial denaturation at 95 °C for 5 min, followed by 35 cycles at 95 °C for 30 s, 48 °C for 30 s and 72 °C for 1 min, and a final extension of 72 °C for 10 min; for 28S, initial denaturation at 94 °C for 2 min, followed by 35 cycles at 94 °C for 30 s, 51 °C for 30 s and 72 °C for 1 min, and a final extension of 72 °C for 10 min; for rpb2, initial denaturation at 95 °C for 5 min, followed by 35 cycles at 95 °C for 30 s, 58 °C for 40 s and 72 °C for 1 min, and a final extension of 72 °C for 8 min. Sequencing was performed by Sangon Biotech (Shanghai, China) Co., Ltd. All newly generated sequences were deposited in GenBank (Table 1).
The taxon sampling strategy for the selection of sequences for phylogenetic trees was to choose related taxa based on a BLASTn search in GenBank within Cortinarius and based on Soop et al. [14]. Three partition datasets (ITS, 28S, rpb2) were separately aligned and manually adjusted with BioEdit 7.1.3.0 [21]. Phyutility 2.2 was used to concatenate the aligned datasets [22]. Cortinarius cyanites Fr. and C. boreicyanites Kytöv., Liimat., Niskanen & A.F.S. Taylor were selected as an outgroup for phylogenetic analyses of the combined dataset, following Xie et al. [7].
For phylogenetic analyses, Bayesian inference (BI) and maximum likelihood (ML) methods were used. For BI analysis, the best-fit model for each partition was estimated using the Akaike information criterion (AIC), implemented in MrModeltest 2.3 [23]. The BI analysis was performed with MrBayes 3.2.6 [24]. Four Markov chains were run for 2 runs from random starting trees for 500,000 generations, sampling every 100th generation. The first 25% of trees were discarded to build the 50% majority rule consensus tree. RAxML 8.2.12, implemented in raxmlGUI, was used for ML analysis, with a rapid bootstrapping algorithm of 1000 replicates [25,26]. All default parameters with the GTRGAMMA model were used in the ML analysis. For BI analysis, GTR + I + G, GTR + I + G and GTR + I were the best-fit model for ITS, 28S and rpb2 partitions, respectively.

3. Results

3.1. Molecular Phylogeny

The ITS + 28S + rpb2 dataset for phylogenetic analyses included 68 samples, representing 50 species. The resulting alignments were deposited at TreeBASE (http://www.treebase.org; submission ID S29164; accessed on 28 December 2021). The BI and ML trees showed similar topologies, and the ML tree was selected as the representative phylogeny (Figure 1).
The phylogenetic tree recovered four sections and one subgenus, which clustered into three clades, subg. Telamonia s.s., telamonioid and outgroup, respectively. The telamonioid clade consisted of sect. Camphorati, sect. Illumini and sect. Leati. Cortinarius neobalaustinus, C. wuliangshanensis and C. yanjiensis clustered in sect. Illumini (BPP/ML = 1.00/99%), in which C. neobalaustinus is sister to C. balaustinus Fr. (BPP/ML = 1.00/100%). Cortinarius pseudocamphoratus belonged to sect. Camphorati (BPP/ML = 1.00/100%) and formed a sister relationship (BPP/ML = 1.00/80%) with the clade of C. camphoratus (Fr.) Fr. and C. putorius Niskanen, Liimat. & Ammirati (BPP/ML = 0.98/85%). Cortinarius subnymphatus was retrieved as a sister species of C. nymphatus Kytöv., Niskanen, Liimat. & Bojantchev (BPP/ML = 1.00/99%) in sect. Leati (BPP/ML = 1.00/100%).

3.2. Taxonomy

Cortinarius neobalaustinus M.L. Xie, T.Z. Wei & Y. Li, sp. nov. Figure 2A1,A2 and Figure 3A1–A3.
Mycobank: MB 842322.
Diagnosis: Basidiomata small to medium-sized. Pileus weakly hygrophanous, innately fibrillose, whitish, yellowish to brown. Lamellae moderately crowded, greyish-yellow to yellowish-brown. Stipe subcylindrical to clavate or bulbous, white at first, then yellowish at upper part, basal mycelium white. Universal veil white, rather copious. Basidiospores small, on average 5.9–6.3 μm × 4.9–5.4 μm, subglobose to ovoid or broadly ellipsoid, finely verrucose.
Holotype: China. Jilin Province, Yanji County, Sandaowan Town, in Quercus mongolica forests, alt. 580 m, 43°16′ N, 129°7′ E, 8 September 2018, Mengle Xie, HMJAU58951.
Etymology: The name refers to the affinity to Cortinarius balaustinus.
Description: Pileus 20–50 mm, convex at first, then becoming plano-convex with a broad umbo; weakly hygrophanous, innately fibrillose; whitish to lightly yellowish-white at first, then yellowish-brown to brown. Lamellae emarginated, moderately crowded, light yellow to greyish-yellow at first, then yellowish-brown to brown, edge paler, uneven. Stipe 43–57 mm long, 9–12 mm thick on top, 11–18 mm thick at the base, subcylindrical to clavate or bulbous, white fibrils, white at first, somewhat yellowish-brown at the upper part, basal mycelium white. Universal veil white, rather copious. Context thick, white at first, later brownish. Odour: radish.
Basidiospores 5.6–6.8(–7.6) μm × 4.6–5.8(–6.8) μm, av. 5.9–6.3 μm × 4.9–5.4 μm, Q = 1.04–1.37, av. Q = 1.18–1.24, subglobose to broadly ellipsoid, finely verrucose, indextrinoid. Basidia clavate, four-spored. Lamellar edges fertile, with clavate cells. Lamellar trama hyphae lightly olivaceous-brown to olivaceous-brown, up to 33 μm wide, finely encrusted. Pileipellis duplex: epicuit hyphae colourless to lightly olivaceous-brown, 2–6.5 μm wide, smooth. Hypodermium developed, hyphae lightly olivaceous-brown, 7–25 μm wide, smooth. Clamp connections present.
Ecology and distribution: Gregarious in Quercus mongolica forests in northeast of China and mixed forests of Picea sp. and Quercus semicarpifolia in southwest of China. Known from Jilin Province, Tibet Autonomous Region and Yunnan Province of China.
Additional specimens examined: China. Jilin Province, Yanji County, Sandaowan Town, in Quercus mongolica forest, alt. 580 m, 43°16′ N, 129°7′ E, 3 September 2017, Mengle Xie, HMJAU58948, HMJAU58949, HMJAU58950; ibid., 4 September 2019, Mengle Xie, HMJAU58952. Tibet Autonomous Region, Nyingchi City, Lulang Town, mixed forest with Picea sp. and Quercus semicarpifolia, 7 September 2014, Tiezheng Wei, Jianyun Zhuang, Xiaoyong Liu & Hao Huang, HMAS271994; ibid., 13 September 2014, Tiezheng Wei, Jianyun Zhuang, Xiaoyong Liu & Hao Huang, HMAS272377; ibid., 22 September 2015, Tiezheng Wei & Binbin Li, HMAS275263, HMAS254451, HMAS254466. Yunnan Province, Shangri-La County, Bitahai Nature Reserve, mixed forest with Picea sp. and Quercus semicarpifolia, 12 August 2008, Tiezheng Wei, HMAS250504.
Notes: Cortinarius neobalaustinus is characterized by the weakly hygrophanous yellowish-brown to brown pileus, small-sized basidiospores with finely verrucose and finely encrusted hyphae of the lamellar trama. It is a typical member of sect. Illumini. Cortinarius balaustinus shows similarity to the new taxon for its brown pileus and small basidiospores, but the basidiospores of C. balaustinus are moderately verrucose [27,28]. In addition, C. balaustinus is a widely distributed species in the Northern Hemisphere, usually under Betula, but less often with Carpinus, Corylus and Quercus trees [27,28]. Molecularly, (in ITS) based on the BLASTn, the most closely related species is C. balaustinus, which differs by 20 substitutions and indel positions, with a similarity of 96.5%. Table 2 provides the critical characteristics distinguishing new species and their similar species in sect. Illumini.
Cortinarius pseudocamphoratus M.L. Xie, T.Z. Wei & Y. Li, sp. nov. Figure 2B1,B2 and Figure 3B1–B3.
Mycobank: MB 842324.
Diagnosis: Pileus hemispherical to plano-convex, viscid, not hygrophanous, greyish-white when young with slightly violet tinge. Lamellae pale violet then bluish-brown, edge paler. Stipe cylindrical to clavate, violet. Universal veil whitish. Basidiospores on average 9.8–9.9 μm × 6.3–6.4 μm, amygdaloid to somewhat ellipsoid, finely and densely verrucose. Cheilocystidia present, somewhat lageniform to subfusiform.
Holotype: China. Tibet Autonomous Region, Linzhi City, Sejila Mountain, in Abies forest with Rhododendron spp., alt. 4200 m, 29°36′56″ N, 94°41′54″ E, 30 August 2019, Mengle Xie, HMJAU48694.
Etymology: The name refers to the affinitive species Cortinarius camphoratus.
Description: Pileus 26–55 mm diam., hemispherical, later plano-convex, viscid, not hygrophanous; greyish-white when young, with slightly violet tinge, later yellow; surface with veil remnants, especially on the margin. Lamellae emarginated, moderately crowded, violet when young, later bluish-brown to brown, edge paler, uneven. Stipe 50–75 mm long, 6–15 mm at above, 9–28 mm at the base, cylindrical to clavate, violet, especially at the apex, coated by abundant veil layer, more violet tinge visible when scraped. Universal veil whitish, then yellowish, very copious, forming incomplete girdles on the stipe. Context of the pileus whitish-yellowish, violet at the apex of the stipe, gradually transitioning to yellowish-grey at the base. Odour strong and unpleasant, typical of C. camphoratus.
Basidiospores 8.7–11.6 μm × 5.8–7 μm, av. 9.8–9.9 μm × 6.3–6.4 μm, Q = 1.35–1.90, av. Q = 1.50–1.60, amygdaloid to somewhat ellipsoid, finely and densely verrucose. Basidia clavate, four spores, colourless or lightly olivaceous-brown to olivaceous-brown. Lamellar trama hyphae lightly olivaceous-brown, up to 25 μm wide, smooth. Lamellar edge fertile, with small clavate sterile cells. Cheilocystidia present, somewhat lageniform to subfusiform, 28–53 μm × 9–13 μm, colourless. Pileipellis duplex: epicuits in weakly gelatinous substance, hyphae lightly olivaceous-brown to olivaceous-brown, 3–7 μm wide, smooth. Hypodermium developed, hyphae colourless to lightly olivaceous-brown, 5–25 μm wide, smooth. Trama hyphae colourless to lightly olivaceous-brown, smooth. Clamp connections present.
Ecology and distribution: Solitary or gregarious on moist soil of Abies forest with Rhododendron spp. Known from Qinghai–Tibetan Plateau of China.
Additional specimens examined: China. Tibet Autonomous Region, Linzhi City, Sejila Mountain, in Abies forests with Rhododendron spp., alt. 4200 m, 29°36′56″ N, 94°41′54″ E, 30 August 2019, Mengle Xie, HMJAU48698; 5 September 2020, Mengle Xie, HMJAU48794, HMJAU48795, HMJAU48796, HMJAU48797, HMJAU48798.
Notes: Cortinarius pseudocamphoratus is characterized by whitish with slightly violet-tinged basidiomata, viscid pileus, strong and unpleasant odour, amygdaloid to somewhat ellipsoid basidiospores, finely and densely verrucose and somewhat lageniform to subfusiform cheilocystidia, which correspond well to the circumscription of the sect. Camphorati. There are only five described species that belong to sect. Camphorati [14,30]. Three species are only distributed in Australasia, whereby C. dysodes and C. tasmacamphoratus are associated with Nothofagus and C. austrotorvus is a Eucalyptus-associated species. Another two species, C. camphoratus and C. putorius, are conifer-associated species and distributed in the Northern Hemisphere. However, C. camphoratus has a more violet and non-viscid pileus and the universal veil is lilac when young [28,31,32]. Cortinarius putorius, meanwhile, usually has a thin universal veil and the basidiospores are smaller, 8.8–9.5(–10) μm × 5–5.7 μm [30]. Phylogenetically, C. pseudocamphoratus cluster in sect. Camphorati and form a sister relationship with the clade of C. camphoratus and C. putorius. Molecularly, (in ITS) based on the BLASTn, the most closely related species is C. camphoratus, which differs by 35 substitutions and indel positions, with a similarity of 94.1%. Table 3 provides the critical characteristics distinguishing C. pseudocamphoratus and its similar species in sect. Camphorati.
Cortinarius subnymphatus M.L. Xie, T.Z. Wei & Y. Li, sp. nov. Figure 2C and Figure 3C1–C3.
Mycobank: MB 842325.
Diagnosis. Pileus conical to plano-convex with an umbo reddish-brown, black-brown at the centre, yellowish at the margin, strongly hygrophanous. Lamellae rusty brown. Stipe cylindrical. Universal veil yellowish. Basidiospores on average 7.6–7.7 μm × 5.0–5.1 μm, ellipsoid to subamygdaloid, finely to moderately verrucose, lamellar trama hyphae encrusted.
Holotype. China. Inner Mongolia Autonomous Region, Genhe County, Mangui Town, in mixed forests of Larix gmelinii, Betula platyphylla and Vaccinium, alt. 630 m, 52°03′52″ N, 122°04′40″ E, 24 August 2017, Mengle Xie, HMJAU48633.
Etymology. The name refers to the affinity to Cortinarius nymphatus.
Description: Pileus 24–52 mm diameter, somewhat conical at first, later convex to somewhat planar and umbonate; strongly hygrophanous; reddish-brown to dark reddish-brown, black-brown at the center, yellowish at the margin; very slightly translucently striated at the margin. Lamellae adnexed to emarginated, moderately crowded, rusty brown, sometimes with dark spots, edge uneven. Stipe 44–67 mm long, 5–8 mm thick, cylindrical; with white fibrillose. Basal mycelium white. Universal veil fairly distinct, yellowish, forming many thin patches and incomplete girdles on the stipe. Context fairly thin, strongly hygrophanous and brownish when moist. Odour indistinct.
Basidiospores 7.2–8.0(–8.7) μm × 4.6–5.4 μm, av. 7.6–7.7 μm × 5.0–5.1 μm, Q = 1.32–1.76, av. Q = 1.50–1.55, ellipsoid to subamygdaloid, finely to moderately verrucose. Basidia clavate, four spores, colourless to olivaceous-brown. Lamellar trama hyphae lightly olivaceous-brown to olivaceous-brown, up to 25 μm wide, moderately encrusted. Lamellar edge fertile, with clavate sterile cells. Pileipellis duplex: epicuit hyphae 5–17 μm wide, olivaceous-brown, zebra-striped, encrusted to finely encrusted. Hypodermium hyphae lightly olivaceous-brown, 3–30 μm wide, zebra-striped, encrusted to almost smooth. Trama hyphae lightly olivaceous to olivaceous, encrusted. Clamp connections present.
Ecology and distribution. Gregarious in a mixed forest of Larix gmelinii, Betula platyphylla and Vaccinium. Known from northeast China.
Additional specimens examined. China. Inner Mongolia Autonomous Region, Genhe County, Mangui Town, in mixed forest of Larix gmelinii, Betula platyphylla and Vaccinium, alt. 630m, 52°03′52″ N, 122°04′40″ E, 24 August 2017, Mengle Xie, HMJAU48632.
Notes: Cortinarius subnymphatus is characterized by a reddish-brown, mat and strongly hygrophanous pileus with a black-brown umbo, yellowish universal veil, ellipsoid to subamygdaloid basidiospores and encrusted hyphae of the lamellar trama. Morphologically, C. subnymphatus is similar to C. fulvescens and C. fulvescentoideus. Cortinarius fulvescens and C. fulvescentoideus, however, usually have bigger basidiospores, over 8 μm long [33]. Phylogenetically, C. subnymphatus clustered in sect. Laeti, sister to C. nymphatus. However, the pileus of C. nymphatus is redder, without the black-brown umbo, the basidiospores are usually less than 5 μm wide and associated with Pinus and Picea [33]. Molecularly, (in ITS) based on the BLASTn, the most closely related species is C. nymphatus, which differs by 10 substitutions and indel positions, with a similarity of 98.4%. Table 4 provides the critical characteristics distinguishing C. subnymphatus and its similar species in sect. Laeti.
Cortinarius wuliangshanensis M.L. Xie, T.Z. Wei & Y. Li, sp. nov. Figure 2D1,D2 and Figure 3D1–D3.
Mycobank: MB 842326.
Diagnosis: Basidiomata small to medium-sized. Pileus hygrophanous, translucently striate, innately fibrillose, yellowish, then reddish-brown at the centre. Lamellae subdistant, greyish-yellow to yellowish-brown. Stipe bulbous at the base when young, then clavate, yellowish-white to yellow, yellowish-brown, basal mycelium white. Universal veil white. Basidiospores small, on average 5.1–5.7 μm × 4.1–4.6 μm, subglobose to broadly ellipsoid, rather finely verrucose.
Holotype: China. Yunnan Province, Jingdong Yi Autonomous County, Wuliangshan National Nature Reserve, in broadleaf forest of Castanopsis, Myrica, Quercus, Schima and Ericaceae, alt. 1870 m, 24°28′33″ N, 100°43′26″ E, 12 September 2020, Mengle Xie, HMJAU58940.
Etymology: The name refers to the type location, Wuliangshan Mountains.
Description: Pileus 24–77 mm, hemispherical to convex at first, then becoming planar, slightly depressed at the centre, wavy and eroded at the margin in mature condition; surface medium hygrophanous, with a clear hygrophanous zone, slightly translucently striated and crenated at the margin, innately fibrillose, silvery-whitish when young, then strongly hygrophanous, with distinct translucent striations; yellowish-white to greyish-yellow at first, reddish-orange to reddish-brown at the centre with age. Lamellae emarginated, subdistant, greyish-yellow at first, then yellowish-brown to brown, edge even. Stipe 28–80 mm long, 4–12 mm thick at above, 6–25 mm thick at the base, bulbous at the base when young, then clavate, with white fibrils, whitish to lightly yellowish-white, yellow to yellowish-brown with age, basal mycelium white. Universal veil white, rather sparse. Context thin, yellowish-white when young, later yellowish-brown to brown at the stipe, hollow at the stipe when mature. Odour: radish.
Basidiospores 4.8–6.1 (–6.8) μm × 3.9–4.8 (–5.1) μm, av. 5.1–5.7 μm × 4.1–4.6 μm, Q = 1.09–1.41, av. Q = 1.23–1.26, subglobose to broadly ellipsoid, rare ellipsoid, rather finely verrucose, moderately dextrinoid. Basidia clavate, four-spored. Lamellar edges fertile, with narrow clavate cells. Lamellar trama hyphae lightly olivaceous-brown to olivaceous-brown, up to 18 μm wide, smooth. Pileipellis with a very thin epicuits, hyphae 3–7.5 μm wide, equal, colourless to lightly olivaceous-brown, smooth. Hypodermium developed, hyphae colourless to lightly olivaceous-brown, 6–20 μm wide, cylindrical to subcellular, smooth. Clamp connections present.
Ecology and distribution: Gregarious in broadleaf forests of Castanopsis, Myrica, Quercus, Schima and Ericaceae or mixed with Pinus. Known from Yunnan Province of China.
Additional specimens examined: Yunnan Province, Jingdong Yi Autonomous County, Wuliangshan National Nature Reserve, in broadleaf forest of Castanopsis, Myrica, Quercus, Schima and Ericaceae, alt. 1870 m, 24°28′33″ N, 100°43′26″ E, 12 September 2020, Mengle Xie, HMJAU58941; ibid., in broadleaf forests of Castanopsis, Myrica, Quercus, Schima and Ericaceae alt. 1850 m, 24°28′32″ N, 100°43′28″ E, 12 September 2020, Mengle Xie, HMJAU58942; ibid., in mixed forest of Castanopsis, Myrica, Pinus, Quercus, Schima and Ericaceae, alt. 1850 m, 24°28’31″ N, 100°43’28″ E, 12 September 2020, Mengle Xie, HMJAU58943.
Notes: Cortinarius wuliangshanensis is characterized by moderately to strongly hygrophanous, yellowish to reddish-brown and distinctly translucently striated pileus, bulbous at the stripe base when young, small-sized and rather finely verrucose basidiospores and smooth hyphae of lamellar trama. It is a typical member of sect. Illumini. Morphologically, it is similar to C. microglobisporus, sharing the yellowish pileus and white fibrillate stipe when young. However, the pileus of C. microglobisporus is without the distinct translucent striations and never reddish-brown and it is only distributed in the Mediterranean under Quercus cerris trees [29]. Molecularly, (in ITS) based on the BLASTn, the most closely related species is C. microglobisporus, which differs by 33 substitutions and indel positions, with a similarity of 94.8%. Table 2 provides the critical characteristics distinguishing C. wuliangshanensis and its similar species in sect. Illumini.
Cortinarius yanjiensis M.L. Xie, T.Z. Wei & Y. Li, sp. nov. Figure 2E and Figure 3E1–E3.
Mycobank: MB 842327.
Diagnosis: Basidiomata small to medium-sized. Pileus weakly to moderately hygrophanous, innately fibrillose, yellowish to brown. Lamellae subdistant to moderately crowded, greyish-yellow to yellowish-brown. Stipe cylindrical to slightly clavate, usually tapered at the base, white at first, then yellowish or yellowish spots at the upper part, basal mycelium white. Universal veil white, spares. Basidiospores small, on average 5.9–6.2 μm × 5–5.2 μm, subglobose to broadly ellipsoid, rather strongly verrucose.
Holotype: CHINA. Jilin Province, Yanji County, Sandaowan Town, in Quercus mongolica forests, alt. 580 m, 43°16′ N, 129°7′ E, 4 September 2019, Mengle Xie, HMJAU58947.
Etymology: The name refers to the type location, Yanji county.
Description: Pileus 20–70 mm, convex at first, then becoming plano-convex with a broad umbo; weakly to moderately hygrophanous, innately fibrillose; lightly yellow, yellowish-brown to brown, paler at the margin. Lamellae adnexed to subadnate, subdistant to moderately crowded, greyish-yellow at first, then yellowish-brown to brown, edge even at first, then uneven. Stipe 25–83 mm long, 4–14 mm thick at above, 7–23 mm thick at the base, cylindrical to slightly clavate, usually with slightly tapered base, white fibrils, white at first, somewhat yellow or yellowish spots at the upper part, basal mycelium white. Universal veil white, spares. Context rather thick, white at first, then yellowish to yellowish-brown at the stipe. Odour: radish.
Basidiospores 5.5–6.8 μm × 4.6–5.8 μm, av. 5.9–6.2 μm × 5–5.2 μm, Q = 1.04–1.34, av. Q = 1.17–1.2, subglobose to broadly ellipsoid, rather strongly verrucose, moderately dextrinoid. Basidia clavate, four-spored. Lamellar edges fertile, with clavate cells. Lamellar trama hyphae colourless to lightly olivaceous-brown, cylindrical to subcellular, up to 28 μm wide, smooth. Pileipellis duplex: epicuit hyphae olivaceous-brown, 2.5–10 μm wide, smooth. Hypodermium developed, hyphae lightly olivaceous-brown, 5–20 μm wide, smooth. Clamp connections present.
Ecology and distribution: Gregarious in Quercus mongolica forests. Known from Jilin Province of China.
Additional specimens examined: Jilin Province, Yanji County, Sandaowan Town, in Quercus mongolica forests, alt. 580 m, 43°16′ N, 129°7′ E, 7 September 2018, Mengle Xie, HMJAU58944; ibid., 4 September 2019, Mengle Xie, HMJAU58945, HMJAU58946.
Notes: Cortinarius yanjiensis is characterized by a weakly to moderately hygrophanous and yellowish to brown pileus, tapered base of the stipe, small-sized and rather strongly verrucose basidiospores, and smooth hyphae of the lamellar trama. It is a typical member of sect. Illumini. Morphologically, it is similar to C. balaustinus and C. neobalaustinus, sharing the weakly hygrophanous pileus. However, the lamellar trama hyphae of C. balaustinus and C. neobalaustinus are finely encrusted. The basidiospores of C. balaustinus are moderately verrucose [27,28] while those of C. neobalaustinus are finely verrucose. Molecularly, (in ITS) based on the BLASTn, the most closely related species is C. illuminus, which differs by 43 substitutions and indel positions, with a similarity of 93.1%. Table 2 provides the critical characteristics distinguishing C. yanjiensis and its similar species in sect. Illumini.
A key to the species in sections Camphorati, Illumini and Laeti from China
1. Universal veil white………………………………………………………………………2
1. Universal veil bright colour…………………………………………………(sect. Laeti) 8
2. Basidiomata strongly unpleasant odour, pileus viscid, universal veil white, basidiospores amygdaloid to somewhat ellipsoid, finely and densely verrucose, cheilocystidia somewhat lageniform………………………………(sect. Camphorati) C. pseudocamphoratus
2. Basidiomata usually indistinct to more or less like radish without unpleasant odour, basidiospores globose, subglobose, to broadly ellipsoid…………………(sect. Illumini) 3
3. Pileus with distinctly translucent stripe…………………………………………………4
3. Pileus without distinctly translucent stripe………………………………………………5
4. Pileus vivid reddish-brown, basidiospores moderately verrucose, hyphae of the lamellar trama finely encrusted, usually occur in mixed forests of Larix gmelinii, Betula platyphylla and Vaccinium, distributed in northeast China…………………C. khinganensis
4. Pileus yellowish at first, then reddish-brown, stipe usually bulbous when young, basidiospores rather finely verrucose, hyphae of the lamellar trama smooth, occur in broadleaf forests of Castanopsis, Myrica, Quercus, Schima and Ericaceae, distributed in southwest China……………………………………………………………C. wuliangshanensis
5. Pileus usually reddish-brown, basidiospores moderately verrucose……………………6
5. Pileus usually yellowish to brown, almost without reddish-brown……………………7
6. Pileus often concentrically hygrophanous, with slightly translucent stripe at the margin, usually occur in coniferous forests, distributed in southwest China………C. illuminus
6. Pileus weakly hygrophanous, never translucently striated, usually occur in deciduous forests, distributed in northeast China……………………………………C. balaustinus
7. Pileus usually yellowish at first, stipe cylindrical to slightly clavate, usually with slightly tapered base, universal veil spares, basidiospores rather strongly verrucose, hyphae of the lamellar trama smooth……………………………………………C. yanjiensis
7. Pileus whitish to slightly yellowish-white at first, stipe subcylindrical to clavate or bulbous, universal veil rather copious, basidiospores finely verrucose, hyphae of the lamellar trama finely encrusted………………………………………………C. neobalaustinus
8. Basidiospores subglobose to broadly ellipsoid……………………………………………9
8. Basidiospores ellipsoid to subamygdaloid………………………………………………10
9. Pileus distinctly hygrophanous, universal veil reddish-brown to vinaceous-brown……………………………………………………………………………C. badiovinaceus
9. Pileus weakly hygrophanous, universal veil yellowish-brown……………C. ochrophyllus
10. Universal veil pink……………………………………………………C. roseobulliardioides
10. Universal veil yellowish to ochraceous…………………………………………………11
11. Pileus reddish-brown, black at the centre…………………………….C. subnymphatus
11. Pileus yellowish-brown to black-brown…………………………………C. cadi-aguirrei

4. Discussion

In this study, five species, Cortinarius neobalaustinus, C. pseudocamphoratus, C. subnymphatus, C. wuliangshanensis and C. yanjiensis, are described from China as new species based on macro-, micro- and ultra-characteristics and multi-gene phylogeny. Phylogenetic analyses showed that the five new species clustered in the telamonioid clade, outside Telamonia s.s., which is consistent with other studies [3,12,13,14].
Section Camphorati was described as a subgenus in a previous study [34] but was reduced to a section based on multi-gene phylogenetic analyses [14]. Section Camphorati has the typical characteristics of medium to large-sized basidiomata, with a blue to purple tinge when young, a strongly unpleasant odour, basidiospores that are amygdaloid to somewhat ellipsoid and cheilocystidia that are somewhat lageniform. There are five species in this section worldwide [14,29], and in the present study, C. pseudocamphoratus is considered to be the sixth species worldwide and the only confirmed species from China in this section.
Section Illumini was described as a subgenus based on a previous study [34] but was reclassified at section level based on multi-gene phylogenetic analyses [14]. Section Illumini has the typical characteristics of medium to large-sized basidiomata, a yellowish to brown or reddish-brown pileus, being more or less hygrophanous and innately fibrillose, its basidiospores globose, subglobose, ovoid to broadly ellipsoid and weakly to rather strongly verrucose. There are six species in this section worldwide, with one species described from China [14,35]. The present study confirms the placement of six species in sect. Illumini, including three new species from China.
Section Laetii species were previously included in subg. Telamonia or subg. Hydrocybe [36,37] and as a section within sect. Fulvescentes Melot, distinguished by the colour of the universal veil [3,33]. However, previous phylogenetic analyses showed that sect. Fulvescentes is a synonym of sect. Laetii [12,13,14,33]. Section Laeti has the typical characteristics of small to medium-sized basidiomata, a pileus that is more or less hygrophanous, its universal veil a bright colour, its basidiospores subglobose, ellipsoid to amygdaloid and weakly to moderately verrucose. In this study, we confirmed five species in sect. Laeti distributed in China, with the new species C. subnymphatus, sister to C. nymphatus, a European species [33].
Most of the Cortinarius species were originally described in Europe and North America, while little work has been done in Asia [38]. In recent years, we have been devoted to researching Cortinarius in China. The present study reports 12 telamonioid species, including five new species, confirming and clarifying the species component of sections Camphorati, Illumini and Laeti in China, enriching the diversity of Cortinarius.

Author Contributions

M.-L.X., R.-Q.J. and Y.L. conceived and designed the study. M.-L.X., T.-Z.W., J.-P.L. and Y.W. collected specimens from China. M.-L.X., T.-Z.W. and K.W. generated the DNA sequence data and checked the specimens. M.-L.X., T.-Z.W., J.-P.L., K.W. and Y.W. analysed the data. M.-L.X., C.P., T.-Z.W., R.-Q.J. and Y.L. checked issues related to nomenclatural articles. M.-L.X. wrote the manuscript draft. M.-L.X., C.P., T.-Z.W., R.-Q.J. and Y.L. revised the draft, and all authors approved the final manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Key Project on R&D of the Ministry of Science and Technology, grant numbers 2018YFE0107800, 2021YFD1600401, the China Agriculture Research System, grant number CARS20, the Overseas Expertise Introduction Project for Discipline Innovation (111 Project), grant number D17014, the National Natural Science Foundation of China, grant number 31270072, the Special Funds for the Young Scholars of Taxonomy of the Chinese Academy of Sciences, grant number ZSBR-001, and the National Key Research and Development program of China, grant number 2019YFC1604703.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All resulting alignments were deposited in TreeBASE (http://www.treebase.org; accession number S29164; accessed on 28 December 2021). All newly generated sequences were deposited in GenBank (https://www.ncbi.nlm.nih.gov/genbank/; accessed on 23 December 2021). All new taxa were linked with MycoBank (https://www.mycobank.org/; accessed on 23 December 2021).

Acknowledgments

We thank Rong Xie and Hui-Juan Sun (Tibet Academy of Agricultural and Animal Husbandry Sciences), Ju-Zuo Li (Life Science College, Northeast Normal University) and Zhen-Yuan Cao for their kind help in the fieldwork. We also thank Xiao-Ya An (Engineering Research Center of Edible and Medicinal Fungi, Ministry of Education, Jilin Agricultural University) for her help with molecular experiments and FESEM.

Conflicts of Interest

The authors declare no conflict of interest.

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Jof 08 00257 g001 550
Figure 1. ML phylogram inferred from the ITS + 28S + rpb2 dataset. The tree is rooted with sect. Cyanites. The Bayesian posterior probabilities (BPP) ≥ 0.95 and ML bootstrap values (ML) ≥ 75% are shown on the branches (BPP/ML). New species are marked in black bold font.
Figure 1. ML phylogram inferred from the ITS + 28S + rpb2 dataset. The tree is rooted with sect. Cyanites. The Bayesian posterior probabilities (BPP) ≥ 0.95 and ML bootstrap values (ML) ≥ 75% are shown on the branches (BPP/ML). New species are marked in black bold font.
Jof 08 00257 g001
Jof 08 00257 g002 550
Figure 2. Basidiomata of Cortinarius neobalaustinus: (A1) HMJAU58951, holotype, (A2) HMJAU58948; C. pseudocamphoratus: (B1) HMJAU48698, holotype, (B2) HMJAU48795; C. subnymphatus: (C) HMJAU48633, holotype; C. wuliangshanensis: (D1) HMJAU58940, holotype, (D2) HMJAU58943; C. yanjiensis: (E) HMJAU58947, holotype. Bars = 10 mm.
Figure 2. Basidiomata of Cortinarius neobalaustinus: (A1) HMJAU58951, holotype, (A2) HMJAU58948; C. pseudocamphoratus: (B1) HMJAU48698, holotype, (B2) HMJAU48795; C. subnymphatus: (C) HMJAU48633, holotype; C. wuliangshanensis: (D1) HMJAU58940, holotype, (D2) HMJAU58943; C. yanjiensis: (E) HMJAU58947, holotype. Bars = 10 mm.
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Figure 3. The basidiospores and pileipellis of the new species. (A1–A3) C. neobalaustinus, HMJAU58951, holotype; (B1–B3) C. pseudocamphoratus, HMJAU48698, holotype; (C1–C3) C. subnymphatus, HMJAU48633, holotype; (D1–D3) C. wuliangshanensis, HMJAU58940, holotype; (E1–E3) C. yanjiensis, HMJAU58947, holotype. (A1–E1) Basidiospores under FESEM; (A2–E2) Basidiospores under microscope, bars = 10 μm; (A3–E3) Pileipellis under microscope, bars = 20 μm.
Figure 3. The basidiospores and pileipellis of the new species. (A1–A3) C. neobalaustinus, HMJAU58951, holotype; (B1–B3) C. pseudocamphoratus, HMJAU48698, holotype; (C1–C3) C. subnymphatus, HMJAU48633, holotype; (D1–D3) C. wuliangshanensis, HMJAU58940, holotype; (E1–E3) C. yanjiensis, HMJAU58947, holotype. (A1–E1) Basidiospores under FESEM; (A2–E2) Basidiospores under microscope, bars = 10 μm; (A3–E3) Pileipellis under microscope, bars = 20 μm.
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Table
Table 1. Sequences used in the phylogenetic analyses.
Table 1. Sequences used in the phylogenetic analyses.
SpeciesVoucher NumberGenBank Accession Number
ITS28Srpb2
C. armillatusKH11KC842408—KC842479
C. badiovinaceusIB19500061 (holotype)HQ845169——
C. badiovinaceusHMJAU48923OM001515——
C. badiovinaceusHMJAU49069OM001516OM001532OM001816
C. balaustinusF44840 (neotype)MW599265——
C. balaustinusHMJAU48838OM001501——
C. balaustinusHMJAU48920OM001502——
C. balaustinusHMJAU48930OM001503——
C. balaustinusHMJAU48936OM001504——
C. balaustinusHMJAU48977OM001505——
C. balaustinusHMJAU48983OM001500OM001529OM001817
C. balaustinusHMJAU49095OM001506——
C. balaustinusHMJAU49097OM001507——
C. boreicyanitesCFP931 (holotype)KF732296——
C. boreicyanitesHMJAU44340OM001482OM001522OM001811
C. boulderensisAHS17461 (holotype)DQ499466—KC608614
C. brunneusTN04-932EU266638—JX407372
C. brunneusDB2548—MK358063—
C. cadi-aguirreiJB-3089/98 (holotype)KJ866953——
C. cadi-aguirreiHMJAU48993OM001521OM001533OM001818
C. camphoratusEH23FJ717505FJ717505—
C. camphoratusCGG1070609MT775573——
C. camphoratusSMI193FJ039626FJ039626—
C. cinnabarinusCFP379 (epitype)JX114944—KC608616
C. cyanitesAT2005069 (neotype)KF732355——
C. cyanitesHMJAU48681MT299957OM001523OM001812
C. cypripediPDD107723 (holotype)KT875199KT875199—
C. dysodesPDD70499 (holotype)GU233340GU233394
C. illuminusF44877 (neotype)KP866156——
C. illuminusHMJAU58853OM001490——
C. illuminusHMJAU58854OM001491OM001526—
C. khinganensisHMJAU44507 (holotype)MT299952OM001525OM001814
C. laetusF15817FJ157034FJ157034—
C. microglobisporusIB20110123 (holotype)NR153027——
C. neobalaustinusHMJAU58948OM001509——
C. neobalaustinusHMJAU58949OM001510——
C. neobalaustinusHMJAU58950OM001512——
C. neobalaustinusHMJAU58951 (holotype)OM001508OM001530OM001819
C. neobalaustinusHMJAU58952OM001511——
C. nymphatusIK95-1549 (holotype)KX388639——
C. ochrophyllusHMAS274769OM001518——
C. ochrophyllusHMAS274847OM001517——
C. ochrophyllusSMI07FJ039604FJ039604—
C. pseudocamphoratusHMJAU48694OM001484——
C. pseudocamphoratusHMJAU48698 (holotype)OM001483OM001524OM001813
C. pseudocamphoratusHMJAU48794OM001485——
C. pseudocamphoratusHMJAU48795OM001486——
C. pseudocamphoratusHMJAU48796OM001487——
C. pseudocamphoratusHMJAU48797OM001488——
C. pseudocamphoratusHMJAU48798OM001489——
C. putoriusTN07-411 (holotype)KR011124——
C. raphanoidesIK00-003JX407333—JX407378
C. roseobulliardioidesTN11-452 (holotype)KX388641——
C. roseobulliardioidesHMAS254397OM001519——
C. roseobulliardioidesHMAS275019OM001520——
C. suberiTN04-155JX407336—JX407382
C. subnymphatusHMJAU48632OM001514——
C. subnymphatusHMJAU48633 (holotype)OM001513OM001531OM001820
C. tasmacamphoratusHO-A20606A0AY669633AY669633—
C. torvusTUB011515AY669668AY669668—
C. waiporianusPDD95907MH101548MH108387MH141009
C. wuliangshanensisHMJAU58940 (holotype)OM001496OM001528OM001821
C. wuliangshanensisHMJAU58941OM001497——
C. wuliangshanensisHMJAU58942OM001498——
C. wuliangshanensisHMJAU58943OM001499——
C. yanjiensisHMJAU58944OM001492——
C. yanjiensisHMJAU58945OM001493——
C. yanjiensisHMJAU58946OM001494——
C. yanjiensisHMJAU58947 (holotype)OM001495OM001527OM001815
New sequences are shown in black bold font.
Table
Table 2. Morphological comparisons of the new species and their similar species in sect. Illumini.
Table 2. Morphological comparisons of the new species and their similar species in sect. Illumini.
SpeciesPileusStipeSporesHyphae of the
Lamellar Trama
Cortianrius balaustinusWeakly hygrophanous, yellowish-brown to reddish-brown, without translucently striateCylindrical to weakly clavateAv. 6–6.1 μm × 4.9–5.1 μm, moderately verrucoseFinely encrusted
C. illuminusConcentrically hygrophanous,
reddish-brown, slightly translucently striate at the margin		Cylindrical to slightly clavate, sometimes with slightly tapered baseAv. 5.9 μm × 5.1 μm, moderately verrucoseFinely encrusted
C. khinganensisStrongly hygrophanous,
reddish-brown, distinctly translucently striate at the margin		Cylindrical to slightly clavateAv. 6.8–6.9 μm × 5.9–6.0 μm, moderately verrucoseFinely encrusted
C. microglobisporus [29]Hygrophanous zone, yellowish, slightly translucently striate at the marginCylindrical to slightly clavate or bulbous, sometimes with slightly tapered baseAv. 5.6 μm × 4.4 μm—
C. neobalaustinusWeakly hygrophanous, yellowish-brown to brown, without translucently striateSubcylindrical to clavate or bulbousAv. 5.9–6.3 μm × 4.9–5.4 μm, finely verrucoseFinely encrusted
C. wuliangshanensisStrongly hygrophanous, yellowish to reddish-brown, distinct translucently striateClavate, somewhat bulbous when youngAv. 5.1–5.7 μm × 4.1–4.6 μm, rather finely to moderately verrucoseSmooth
C. yanjiensisWeakly hygrophanous, yellowish-brown to brown, without translucently striateCylindrical to slightly clavate, usually with slightly tapered baseAv. 5.9–6.2 μm × 5–5.2 μm, rather strongly verrucoseSmooth
Table
Table 3. Morphological comparisons of the new species and their similar species in sect. Camphorati.
Table 3. Morphological comparisons of the new species and their similar species in sect. Camphorati.
SpeciesPileusStipeUniversal VeilSpores
Cortianrius camphoratus [28,30,31,32]Not hygrophanous, not viscid, blue to almost white, then yellowish-brownCylindrical to clavateLilac, then yellowish, very copious(9–)9.5–10.5 μm × (5.5–)6–6.5 μm, finely and densely verrucose
C. pseudocamphoratusNot hygrophanous,
viscid, grayish-white, then yellowish		ClavateWhitish, then yellowish, very copiousAv. 9.8–9.9 μm × 6.3–6.4 μm, finely and densely verrucose
C. putorius [30]Not hygrophanous,
viscid, purple, then pale purple to almost whitish		Cylindrical to somewhat clavateWhite, sparseAv. 9.2 μm × 5.4 μm, finely and densely verrucose
Table
Table 4. Morphological comparisons of the new species and their similar species in sect. Laeti.
Table 4. Morphological comparisons of the new species and their similar species in sect. Laeti.
SpeciesPileusStipeUniversal VeilSpores
Cortinarius fulvescens [33]Strongly hygrophanous, reddish-brown to vinaceous reddish-brownCylindricalPink, very sparse7.9–9.5 μm × 4.5–5.2 μm, often somewhat sharply verrucose
C. fulvescentoideus [33]Strongly hygrophanous,
warm reddish-brown		CylindricalPale pink, very sparse8.2–9.5 μm × (4.5–)5–5.4 μm, finely to moderately verrucose
C. nymphatus [33]Strongly hygrophanous,
brown to dark reddish-brown		CylindricalYellow to ochraceous, forming incomplete girdles on the stipe6.8–8.2 μm × 4.3–4.8 μm, finely to moderately, sharply verrucose
C. subnymphatusStrongly hygrophanous; reddish-brown to dark reddish-brown, black-brown at the centerCylindricalYellowish, forming many thin patches and incomplete girdles on the stipe7.2–8.0(–8.7) μm × 4.6–5.4 μm, finely to moderately verrucose
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Xie, M.-L.; Phukhamsakda, C.; Wei, T.-Z.; Li, J.-P.; Wang, K.; Wang, Y.; Ji, R.-Q.; Li, Y. Morphological and Phylogenetic Evidence Reveal Five New Telamonioid Species of Cortinarius (Agaricales) from East Asia. J. Fungi 2022, 8, 257. https://doi.org/10.3390/jof8030257

AMA Style

Xie M-L, Phukhamsakda C, Wei T-Z, Li J-P, Wang K, Wang Y, Ji R-Q, Li Y. Morphological and Phylogenetic Evidence Reveal Five New Telamonioid Species of Cortinarius (Agaricales) from East Asia. Journal of Fungi. 2022; 8(3):257. https://doi.org/10.3390/jof8030257

Chicago/Turabian Style

Xie, Meng-Le, Chayanard Phukhamsakda, Tie-Zheng Wei, Ji-Peng Li, Ke Wang, Yang Wang, Rui-Qing Ji, and Yu Li. 2022. "Morphological and Phylogenetic Evidence Reveal Five New Telamonioid Species of Cortinarius (Agaricales) from East Asia" Journal of Fungi 8, no. 3: 257. https://doi.org/10.3390/jof8030257

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