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Research Article
Two new rare species of Candolleomyces with pale spores from China
expand article infoTolgor Bau, Jun-Qing Yan§
‡ Jilin Agricultural University, Changchun, China
§ Jiangxi Agricultural University, Nanchang, China
Open Access

Abstract

Most species of Candolleomyces have brown or dark brown spores. Although pale-spored members are rare in the genus we frequently collected two such species from many Provinces during our investigations in subtropical China from 2016–2020. As revealed by morphological characterisation and multigene phylogenetic analyses (ITS LSU β-tub and tef-) these species which we have named C. subcacao and C. subminutisporus are unique and distinct from known taxa. In addition a new combination C. cladii-marisci is proposed on the basis of ITS sequence analysis of the type specimen. Detailed descriptions colour photos illustrations and a key to related species are presented.

Keywords

Basidiomycete, new taxon, Psathyrellaceae, phylogenetic analysis, taxonomy

Introduction

On the basis of extensive comparisons of gene sequences and phylogenetic analyses, the historical genus Psathyrella (Fr.) Quél. has been split into several genera. One of these genera is Candolleomyces D. Wächt. & A. Melzer, which differs from Psathyrella s.s. in lacking pleurocystidia (Örstadius et al. 2015; Wächter and Melzer 2020). Approximately 100 taxa (including synonyms and subspecies) without pleurocystidia have been previously described in Psathyrella s.l. (Fries 1838; Smith 1972; Kits van Waveren 1985; Örstadius and Kundsen 2012; Battistin et al. 2014); however, many of these taxa have been treated as synonyms, as unique features, based on conventional methods, are scarce (Galland et al. 1979; Kits van Waveren 1980; Knudsen and Vesterholt 2012). Currently, 26 species have been assigned to Candolleomyces (Wächter & Melzer, 2020).

According to the research of Wächter and Melzer (2020), Candolleomyces may be more speciose than previously thought and better delimitation of species boundaries is needed. Although controversies still exist regarding some species boundaries, the number of new taxa is steadily increasing (Melzer et al. 2018; Sicoli et al. 2019a; Büttner et al. 2020). This continuous discovery of new taxa with clear boundaries deepens understanding of the species in this genus.

Approximately eight taxa in the genus Candolleomyces have previously been reported from China (Yan 2018). During our investigations in subtropical China from 2016–2020, we frequently collected two unknown Candolleomyces species with pale spores from many Provinces. Spores that are pale or almost colourless in water and 5% potassium hydroxide (KOH) are very rare in this genus. On the basis of our morphological and phylogenetic analyses, the specimens are described as new species in this paper.

Materials and methods

Morphological studies

Specimens were deposited in the Herbarium of Mycology, Jilin Agricultural University (HMJAU) and the Herbarium of Fungi, Jiangxi Agricultural University (HFJAU). Macromorphological characters and habitat details were recorded from fresh basidiomata. Colour codes were based on the Methuen Handbook of Colour (Kornerup and Wanscher 1978). More than 30 spores, cystidia and basidia in water and 5% aqueous KOH were measured under a microscope. In subsequent descriptions, measurements are shown as (a)bc (d), where a is the lowest value, bc encompasses at least 90% of values and d is the highest value, while Q is the length–width ratio of a spore (Bas 1969; Yu et al. 2020).

DNA extraction and sequencing

DNA was extracted from dried specimens using a NuClean Plant Genomic DNA kit (CWBIO, China). Four DNA regions (ITS, LSU, Tef-1α and β-tub) were selected for analysis (Örstadius et al. 2015) and were respectively amplified using the primer pairs ITS1/ITS4 (White et al. 1990), LR0R/LR7 (Hopple and Vilgalys 1999), EF983F/EF2218R (Örstadius et al. 2015) and B36f/B12r (Nagy et al. 2011). PCR amplifications were performed using the following touchdown programme: 5 min at 95 °C, followed by 15 rounds of 1 min at 95 °C, 30 s at 65 °C (lowered by 1 °C per cycle) and 1 min at 72 °C, followed by 20 rounds of 1 min at 95 °C, 30 s at 50 °C and 1 min at 72 °C, with a final extension of 10 min at 72 °C (Yan and Bau 2018b). Sequencing was carried out by Qing Ke Biotechnology Co. (Wuhan, China).

Data analyses

Taking into consideration the results of BLAST searching against GenBank and the research of Büttner et al. (2020) and Wächter and Melzer (2020), we analysed ITS, LSU, tef-1α (Tef 1st, Tef 2nd and Tef 3rd) and β-tub (Tub 1st and Tub 2nd) sequences from 37 taxa. Details are presented in Table 1. Sequences were aligned using the online version of the multiple sequence alignment programme MAFFT v.7 (Katoh and Standley 2013), followed by manual adjustment in BIOEDIT v.7.1.3.0 (Hall 1999). Phylogenetic analyses were conducted using Bayesian Inference (BI) in MrBayes v.3.2.6 (Ronquist et al. 2012) and by Maximum Likelihood (ML) in IQTREE v.1.5.6 (Nguyen et al. 2014). For the BI analyses, four Monte Carlo Markov chains were run for 10 million generations, with sampling every 100th generation and with the first 25% of trees discarded as burn-in (Ronquist et al. 2012). ML analyses were undertaken by applying the ultrafast bootstrap approximation with 1000 replicates. The sequence alignment has been deposited in TreeBASE (S28074).

Table 1.

Sequences used in this study.

Taxa Voucher Locality ITS LSU β-Tub tef-1α
Candolleomyces albipes DED8340 Sao Tome KX017209
C. aberdarensis GLM-F116094 Kenya MH880928
C. badhyzensis 79478 (TAA) Type Turkmenistan KC992883 KC992883
C. badiophyllus SZMC-NL-2347 FN430699 FM876268 FN396261 FM897252
C. cacao SFSU DED 8339 Sao Tome NR148106
FP1R4 USA KU847452
MP2R2 USA KU847436
C. candolleanus LAS73030 Neotype Sweden KM030175 KM030175
C. efflorescens Pegler2133 (K) Sri Lanka KC992941
C. eurysporus GLM-F126263 Type Germany MT651560 MT651560
C. leucotephrus LÖ138-01 (UPS) Sweden KC992885 KC992885 KJ664865 KJ732775
C. luteopallidus Sharp20863 (MICH) Type USA KC992884 KC992884
HMJAU5148 China: Jilin MG734736 MW301084 MW314056 MW314073
C. secotioides UES2918 Type Mexico KR003281 KR003282 KR003283
C. singeri HMJUA37867 China: Jilin MG734718 MW301088 MW314059 MW314077
HMJAU37877 China: Chongqing MW301073 MW301091 MW314062 MW314080
Candolleomyces sp. BAB-4773 India KP686450
BAB-5172 India KR349656
BAB-4748 India KR154977
BAB-4747 India KR154976
BAB-5202 India KT188611
C. subcacao HMJAU37807 Type China: Henan MW301064 MW301092 MW314063 MW314081
HMJAU37808 China: Henan MW301065 MW301093 MW314064 MW314082
HFJAU1014 China: Jiangxi MW559218
HFJAU1274 China: Jiangxi MW559219
HFJAU1488 China:Anhui MW559220
C. subminutisporus HMJAU37801 Type China: Hubei MW301066 MW301094 MW314065 MW314083
HMJAU37916 China: Henan MW301067 MW301095 MW314066 MW314084
C. subsingeri HMJAU37811 Type China: Jilin MG734715 MW301097 MW314067 MW314085
HMJAU37913 China: Jilin MG734725 MW301098 MW314068 MW314086
C. sulcatotuberculosus GB:LO55-12 KJ138422 KJ138422
HFJAU1515 China: Fujian MW375696 MW382967 MW382965
Chiarello 07-10-2013 KJ138423
C. trinitatensis TL9035 (C) Ecuador KC992882 KC992882 KJ664863
ADK4162 (BR) Togo KC992886 KC992886
Psathyrella cladii-marisci CLUF302 Type Italy MK080112
Outgroup
Psathyrella multipedata LÖ237-04 Sweden KC992888 KC992888 KJ664867 KJ732777

Results

According to a BLAST analysis, the ITS sequence of C. subcacao is 98% similar (eight different loci) to that of C. cacao (Desjardin & B.A. Perry) D. Wächt. & A. Melzer and approximately 97% similar (19 different loci) to five ITS sequences from two unnamed species (KP686450 for BAB-4773, KR349656 for BAB-5172, KR154977 for BAB-4748, KR154976 for BAB-4747 and KT188611 for BAB-5202) isolated from Oeceoclades maculata (Lindley) Lindley (Bayman et al. 2016). The ITS sequence of C. subminutisporus shares 97% similarity (22 different loci) with that of C. sulcatotuberculosus (J. Favre) D. Wächt. & A. Melzer. The generated BI and ML trees are shown in Fig. 1 and Suppl. material 1, respectively. In both trees, sequences of the two new species comprise strongly supported clades that are distinct from closely-related taxa. The C. subcacao clade groups together with C. cacao and two unnamed species with high statistical support, while the C. subminutisporus clade clusters with C. singeri (A.H. Sm.) D. Wächt. & A. Melzer and C. sulcatotuberculosus. The type sequence of Psathyrella cladii-marisci Sicoli, N.G. Passal., De Giuseppe, Palermo & Pellegrino is clearly nested within Candolleomyces, where it groups most closely, although with only weak to moderate support, with C. badhyzensis (Kalamees) D. Wächt. & A. Melzer, C. badiophyllus (Romagn.) D. Wächt. & A. Melzer and C. candolleanus (Fr.) D. Wächt. & A. Melzer.

Figure 1. 

Phylogenetic tree of Candolleomyces. The tree was generated by Bayesian analysis of a concatenated dataset of sequences from four nuclear regions (ITS, LSU, tef-1α and β-tub). Psathyrella multipedata (Peck) A.H. Sm. was used as an outgroup. Bayesian posterior probabilities (BI-PP) ³ 0.95 and Maximum Likelihood bootstrap support values (ML) ≥ 75% are shown above nodes as BI-PP/ML. ● indicates newly-described species.

Taxonomy

Candolleomyces subcacao T. Bau & J.Q. Yan, sp. nov.

MycoBank No: 839231
Fig. 2

Holotype

China. Henan Province: Bird Island, Nanwan Lake, Xinyang City, 32°06'43.32"N, 113°06'03.06"E, 124 m elevation, 17 July 2016, Tolgor Bau, Jun-Qing Yan, HMJAU37807 (holotype!)

Etymology

Referring to its morphological similarity to C. cacao.

Diagnosis

Differs from C. cacao in having a distinct spore germ pore.

Description

Pileus 11–35 mm, spreading hemispherically to planar, hygrophanous, brown (7E7–7E8), striate up to halfway from the margin or indistinct, becoming slightly dirty white (7B1–7B2) upon drying. Veil pale brown (7A5–7B6), thin, fibrillose, falling off easily. Context thin and very fragile, dirty white (7B1–7B2), approximately 1.0 mm thick at the centre. Lamellae 3.0–4.0 mm wide, moderately close, adnate to slightly adnexed, pale brown (C3–C4) to dark brown (7D6–7E6), saw-toothed under 20× magnification. Stipe 40–50 mm long, approximately 2.0 mm thick, white (7A1–7B1), hollow, equal, smooth, with white fibrils (7A1–7B1) at the base. Odour and taste indistinct.

Spores 6.8–8.0(8.8) × 3.9–4.9 μm, Q = 1.4–1.8, ellipsoid to oblong-ellipsoid, profile slightly flattened on one side, rarely phaseoliform, inamyloid, smooth, pale yellow-brown, darkening in 5% KOH, pale brown, germ pores distinct, but small, approximately 1.0 μm wide. Basidia 17–22 × 6.1–7.3 μm, clavate, hyaline, 4-spored. Pleurocystidia absent. Cheilocystidia 22–36 × 9.8–14 μm, scattered to moderately numerous, various, utriform to fusiform, with an obtuse to broadly obtuse apex, rarely subcapitate or clavate, ovoid, thin-walled. Trama of gills irregular. Pileipellis consisting of 2–3 cells in the deep layer of the subglobose cell, 20–37 μm wide.

Habit and habitat

Solitary to scattered on rotten wood in oak forest.

Other specimens examined

China. Henan Province: Bird Island, Nanwan Lake, Xinyang City, 17 July 2016, Tolgor Bau and Jun-Qing Yan, HMJAU37808, HMJAU37809; Borden Forest Park, Xinyang City, 17 July 2017, Jun-Qing Yan, HMJAU37898, HMJAU37899, HMJAU37900, HMJAU37948, HMJAU44554; Jiangxi Province: Jiangxi Agricultural University, Nanchang City, 3 June 2019, Jun-Qing Yan, HFJAU0716, 9 June 2019, Jun-Qing Yan, HFJAU1274; Yun Bi Feng National Forest Park, Shangrao City, 5 July 2019, HFJAU1014.

Figure 2. 

Basidiomata and microscopic features of Candolleomyces subcacao a–c Basidiomata d spores e basidia f pileipellis g cheilocystidia. Scale bars: 10 mm (a–c); 10 μm (d–g).

Candolleomyces subminutisporus T. Bau & J.Q. Yan, sp. nov.

MycoBank No: 839232
Fig. 3

Etymology

Referring to the small spores.

Holotype

China. Henan Province: Boerdeng National Forest Park, Xinyang City, 16 July 2017, Tolgor Bau and Jun-Qing Yan, HMJAU37801 (holotype!).

Diagnosis

Differs from C. sulcatotuberculosus in having smaller spores (5.8–6.8 μm long).

Description

Pileus 8.0–22 mm, spreading hemispherically to broadly conical convex, hygrophanous, pale yellow-brown (6C7–6C8) at the centre, pale at the margin (6A2–6A4), striate from margin to centre, becoming pale brown (6B6–6B7) when dry. Veil present in early stages, thin, white (6A1), fibrillose, evanescent. Context thin and very fragile, 1.0–1.5 mm thick at the centre, same colour as the pileus. Lamellae 2.5–3.0 mm wide, adnate, moderately close, white (6B1) to pale coffee (6B2–6B3), edges saw-toothed under 20× magnification. Stipes 15–40 mm long, 1.0–2.0 mm thick, cylindrical, hollow, white (6B1), sometimes subhyaline or slightly yellow-brown (6A2–6B2) at the base, apex pruinose, evanescent, slightly expanded at the base. Odour and taste indistinct.

Spores 5.8–6.8(7.8) × 3.8–4.9 μm, Q = 1.4–1.8, ovoid, ellipsoid to oblong-ellipsoid, in profile flattened on one side, rarely phaseoliform, inamyloid, smooth, very pale, nearly hyaline in water and 5% KOH, germ pore absent. Basidia 14–20 × 7.3–7.8 μm, 4-spored, clavate, hyaline. Pleurocystidia absent. Cheilocystidia 20–32 × 11–17 μm, utriform, with obtuse apex, bottom side tapering to the long or short stipe. Caulocystidia 27–42 × 6.1–9.8 μm, present at the apex, mostly solitary, various, similar to cheilocystidia or clavate and subcapitate or not. Trama of gills irregular. Pileipellis consists of 1–2 cells in a deep layer of the subglobose cell, up to 36 μm broad.

Figure 3. 

Basidiomata and microscopic features of Candolleomyces subminutisporus a–c Basidiomata d spores e basidia f pileipellis g cheilocystidia h caulocystidia. Scale bars: 10 mm (a–c); 10 μm (d–h).

Habit and habitat

Scattered on rotten wood or humus in Pinus massoniana and oak forests.

Other specimens examined

China. Anhui Province: Huangshan City, 3 July 2018, Jun-Qing Yan, HFJAU1253, HFJAU1361; Guangxi Zhuang Autonomous Region: Qingxiushan National Forest Park, Nanning City, 12 Aug 2016, HMJAU37930; Phoenix Valley Forest Park, Nanning City, 17 Aug 2016, Jun-Qing Yan, HMJAU37950; Henan Province: Boerdeng National Forest Park, Xinyang City, 16 July 2017, Jun-Qing Yan, HMJAU37916, HMJAU37958; 17 July 2017, Jun-Qing Yan, HMJAU37959, HMJAU37960, HMJAU37961: Hubei Province: Dagui Temple National Forest Park, Suizhou City, 16 July 2016, Tolgor Bau and Jun-Qing Yan, HMJAU37800; Jiangxi Province: Lushan Mountain, Jiujiang City, 30 June 2020, Jun-Qing Yan, HFJAU0921; Yunnan Province: Kunming Botanical Garden, Kunming City, 6 Aug 2016, Jun-Qing Yan, HMJAU37929.

New combination

Candolleomyces cladii-marisci (G. Sicoli, N.G. Passalacqua, A.B. De Giuseppe, A.M. Palermo & G. Pellegrino) J.Q. Yan, comb. nov.

MycoBank No: 839233

Psathyrella cladii-marisci Sicoli, N.G. Passal., De Giuseppe, Palermo & Pellegrino, MycoKeys 52: 99, 2019. Basionym.

Note

According to the ITS phylogenetic analysis including the type specimen, P. cladii-marisci belongs to Candolleomyces and has a close phylogenetic relationship with C. candolleanus, C. badiophyllus and C. trinitatensis. In addition, the morphological characteristics of this species correspond to Candolleomyces, which lack pleurocystidia.

For detailed descriptions and line drawings of this species, see Sicoli et al. (2019a; b).

Discussion

Most species of Candolleomyces have dark brown or brown spores, whereas species with pale spores are rare. Candolleomyces subcacao is very easily confused with C. cacao in the field because of their similar macroscopic characteristics. In addition, these two species have highly similar ITS regions (98%). Nevertheless, some members of Candolleomyces with high ITS similarity are still treated as separate species on the basis of morphological characters (Sicoli et al. 2019a; Büttner et al. 2020; Wächter and Melzer 2020). Candolleomyces subcacao and C. cacao group together, but comprise independent lineages, in the phylogenetic tree (Fig. 1). Moreover, C. cacao has ventricose to broad lageniform cheilocystidia, an indistinct germ pore in 5% KOH and a tropical distribution (Desjardin 2016).

On the basis of morphology, C. subcacao has been classified into Psathyrella sect. Spintrigerae using the classification system of Kits van Waveren (1985; 1987) and Psathyrella sect. Subatratae, based on the system of Smith (1972). Some species in these sections lack pleurocystidia and may thus actually belong to Candolleomyces, but molecular analyses of type materials are needed prior to their possible reassignment. In this paper, we have, therefore, only compared these species and the new ones with respect to morphology (see the key below). In particular, two species in these sections possess the combined characteristics of small basidiomata, a pale brown and evanescent veil and pale yellow-brown spores with a distinct germ pore: P. lacuum Huijsman, which can be distinguished from C. subcacao by the presence of a veil with dispersed white arachnoid fibrils or flocci, abundant pyriform cells at the marginal of the lamellae and very rare utriform cheilocystidia (Kits van Waveren 1985; Battistin et al. 2014) and P. cordobaensis A.H. Sm., which differs mainly in having a 10 mm wide pileus, an indistinct germ pore and saccate to ellipsoid cheilocystidia (Smith 1972; Desjardin 2016).

Candolleomyces subminutisporus is characterised by the presence of small basidiomata, a pileus that is striate from the margin up to the centre and very pale to nearly hyaline spores that are mainly less than 7.0 μm long. Candolleomyces sulcatotuberculosus and C. subminutisporus are morphologically very similar and are phylogenetically closely related (Fig. 1); however, the former has a sulcate-tuberculose pileus surface and much larger spores, which measure (7.6)7.9–8.5(9) × (4.5)4.6–5.0(5.2) μm (Einhellinger 1976). Although Kits van Waveren (1985) and Battistini (2014) detected some smaller spores in these species, which measured (6.2)6.9–7.8(8.9) × (3.6)4.1–4.7(5.0) μm, most spores of C. sulcatotuberculosus are clearly longer than 7.0 μm.

Candolleomyces singeri (A.H. Sm.) D. Wächt. & A. Melzer, C. eurysporus A. Karich, E. Büttner & R. Ullrich and C. aberdarensis (A. Melzer, Kimani & R. Ullrich) D. Wächt. & A. Melzer group together with C. subminutisporus in the phylogenetic tree (Fig. 1). These species can be separated as follows: C. singeri has larger spores, mostly 6.8–7.8 μm long (Smith 1972, pers. obs. of HMJUA37867 by JQ Yan), whereas C. eurysporus can be separated on the basis of its broader spores, a Q-value of 1.2–1.6(–1.7) and brown lamellae at maturity (Büttner et al. 2020) and C. aberdarensis is distinguished by having larger spores [7.5–8(–8.8) μm long] (Melzer et al. 2018). In addition, two species are morphologically similar to C. subminutisporus in having more-or-less pale spores, germ pores that are indistinct or lacking and no pleurocystidia. These species can be separated from C. subminutisporus as follows: C. halophilus (Esteve-Rav. & Enderle) D. Wächt. & A. Melzer has larger spores, which are 8.6–11 × 4.8–6.2 μm (Esteve-Raventós and Enderle 1992; Battistin et al. 2014) and C. subsingeri (T. Bau & J.Q. Yan) D. Wächt. & A. Melzer is easily distinguished on the basis of its stout basidiomata (Yan and Bau 2018a).

Finally, P. cladii-marisci was described by Sicoli et. al. (2019) and is characterised by the absence of pleurocystidia and the presence of large spores up to 11 μm long (Sicoli et al. 2019a; b). According to our phylogenetic analysis, this species is relatively closely related to C. candolleanus, C. badiophyllus and C. trinitatensis and should be moved to Candolleomyces. A new combination is thus proposed.

1 Spores very pale, nearly hyaline in 5% KOH 2
Spores pale yellow-brown, greyish-brown or darker 7
2 Spores mostly less than 7.0 μm 3
Spores up to 8.0 μm 4
3 Spores broader, Q = 1.2–1.6, lamellae brown at maturity C. eurysporus
Spores slenderer, Q = 1.4–1.8, lamellae pale coffee at maturity C. subminutisporus
4 Surface of pileus is sulcate-tuberculose, up to two-thirds of the radius C. sulcatotuberculosus
Not as above 5
5 Pileus less than 10 mm wide, lamellae brown C. aberdarensis
Not as above 6
6 Basidiomata stout, spores up to 5.5 μm broad C. singeri
Basidiomata slender, spores up to 4.5 μm broad C. subsingeri
7 Spores up to 11 μm, growing on plant debris in brackish water C. halophilus
Not as above 8
8 Germ pore distinct 9
Germ pore indistinct 10
9 Margin of lamellae with abundant pyriform cells, utriform cheilocystidia very rare P. lacuum
Not as above C. subcacao
10 Cheilocystidia ventricose to broadly lageniform C. cacao
Cheilocystidia saccate to ellipsoid P. cordobaensis

Acknowledgements

This work is supported by the National Natural Science Foundation of China (No. 31960008 and 32070010); and Jiangxi Provincial Natural Science Foundation (20202BABL213041). We thank Dr. Barbara Goodson for editing the English text of this manuscript.

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Supplementary material

Supplementary material 1 

Phylogram generated by Maximum Likelihood (ML) analysis

Tolgor Bau, Jun-Qing Yan

Data type: phylogenetic tree

Explanation note: Phylogram generated by Maximum Likelihood (ML) analysis of Candolleomyces based on sequences of a concatenated data set from four nuclear regions (ITS, LSU, Tef-1α and β-tub), rooted with Psathyrella multipedata (Peck) A.H. Sm. (/multipedata clade). ML bootstrap proportion (ML-BP)≥ 75% are shown. ● indicates newly described species.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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