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. 2023 Aug 21;99:109–130. doi: 10.3897/mycokeys.99.105317

Additions to Hohenbuehelia (Basidiomycota, Pleurotaceae): two new species and notes on H.tristis from northern Thailand

Monthien Phonemany 1, Santhiti Vadthanarat 1,2, Bhavesh Raghoonundon 1, Naritsada Thongklang 1, Olivier Raspé 1,✉
PMCID: PMC10463566  PMID: 37649965

Abstract

Two new species and a first geographical record of Hohenbuehelia are described from Thailand. Macroscopic and microscopic descriptions with photoplates, as well as a multigene phylogeny are provided. Hohenbueheliaflabelliformissp. nov. is recognised by large flabelliform basidiomata, densely villose yellowish-white pileus with white hairs near the point of attachment, basidiospores that mostly are ellipsoid in front view and phaseoliform in side view, the absence of cheilocystidia, and a trichoderm pileipellis. Hohenbuehelialageniformissp. nov. is characterised by fleshy basidiomata, velutinous pileus with whitish hairs near the point of attachment and the margin, elsewhere pale greyish-yellow and with only sparse white hairs, pale brown to light brown and mucilaginous context, subglobose basidiospores, lageniform cheilocystidia, an ixotrichoderm pileipellis, and the absence of pileoleptocystidia. Hohenbueheliatristis is characterised by small creamy-white, spathuliform basidiomata that are larger than the type subspecies, minutely pubescent pileus with tiny greyish hairs that disappear when mature, leaving the surface glutinous, faintly translucent and shiny, ellipsoid to sub-ellipsoid basidiospores, lecythiform to sublageniform cheilocystidia, and an ixotrichoderm pileipellis. Hohenbueheliatristis is recorded for Thailand for the first time. Based on the polymorphism observed in part of the nrLSU gene, the presence of two divergent lineages within H.tristis is discussed.

Key words: Agaricales, DNA sequence heteromorphisms, molecular phylogeny, pleurotoid mushrooms, Southeast Asia, taxonomy, two new species

Introduction

Hohenbuehelia Schulzer belongs to the family Pleurotaceae Kühner in the order Agaricales Underw. In former studies, the asexual stages of Hohenbuehelia species were separately placed in the genus Nematoctonus Drechsler (Drechsler 1941; Thorn and Barron 1986). Following the One Fungus = One Name nomenclatural rule, both the asexual and sexual stages were placed under Hohenbuehelia (Taylor 2011; McNeill et al. 2012; Thorn 2013), with H.petaloides (Bull.) Schulzer as the type species. Currently, 126 taxon names are listed under Hohenbuehelia in Index Fungorum (http://www.indexfungorum.org/), for 50 accepted species (He et al. 2019; Wijayawardene et al. 2022). The typical characteristics of this genus are pleurotoid, gelatinous basidiomata, white basidiospores with a germ pore, lecythiform cheilocystidia (if present) and thick-walled metuloid pleurocystidia (Stevenson 1964; Thorn and Barron 1986; Corner 1994; Silva-Filho and Cortez 2017; Holec and Zehnálek 2020). Hohenbuehelia and Pleurotus (Fr.) P. Kumm. have some similar morphological characters. However, Hohenbuehelia is distinguished by the synapomorphic gelatinous layer in the context under the pileipellis, which is absent in Pleurotus (Mentrida 2016). Most Hohenbuehelia species are decomposers and widely distributed in temperate and tropical areas (Læssøe and Petersen 2019). Hohenbuehelia species have been found growing on dead branches, decayed wood, logs, and sometimes on the bark of living trees or on herbaceous stems (Holec and Zehnálek 2020).

A few Hohenbuehelia species have been reported as edible. However, they have very low culinary value (Cruz and Gándara 2005). This genus is a good source of polyphenols and polysaccharides (Li et al. 2012; Li et al. 2017; Wang et al. 2018; Wang et al. 2019). Bioactive compounds extracted from some Hohenbuehelia species were found to have antioxidant properties as well as antitumor and antiviral activities (Ji et al. 2012; Sandargo et al. 2018a). Furthermore, the new derivatives thiopleurotinic acid A and thiopleurotinic acid B from extracts of H.grisea (Peck) Singer (strain MFLUCC 12-0451) were found to exhibit cytotoxicity towards a mouse fibroblast cell line, as well as antimicrobial activities (Sandargo et al. 2018a). Another compound, 4-hydroxypleurogrisein, was shown to inhibit hepatitis C virus infectivity in mammalian liver cells (Sandargo et al. 2018b). Hohenbuehelia sp. ZW-16 has been used for bioethanol production (Liang et al. 2013). Thorn et al. (2000) also found that the mycelia of the asexual stage of some Hohenbuehelia species are able to produce adhesive knobs that can capture nematodes. The diversity of bioactive compounds from Hohenbuehelia species and their potential applications underline the importance of detailed taxonomic study of this genus (Shipley et al. 2006; Bohni et al. 2013,Sandargo et al. 2018a, 2018b).

Thailand has a high mushroom diversity with many new species yet to be discovered (Thongbai et al. 2018; Vadthanarat et al. 2021). Only four Hohenbuehelia species have been recorded from Thailand, namely H.grisea, H.panelloides Høiland, H.petaloides and H.reniformis (G. Mever & Fr.) Sing. (Chandrasrikul et al. 2011; Sandargo et al. 2018a). However, most of those reports did not provide detailed morphological descriptions nor molecular data in order to confirm the identifications (H.grisea was identified, based on ITS sequences only, without morphological data). In this study, during the survey of pleurotoid mushrooms in northern Thailand, several collections of Hohenbuehelia were obtained and studied. Based on morphological and phylogenetic results, two new species, H.flabelliformis and H.lageniformis, and the first record of H.tristis are described herein.

Materials and methods

Sample collection and morphological study

The mushroom specimens were collected during the rainy season in 2019 and 2020 from Chiang Mai and Chiang Rai Provinces, in northern Thailand. The fresh basidiomata were photographed in situ. Details including collecting date, locality, habitat and ecology of the surroundings, were noted. The specimens were wrapped in aluminium foil or kept in plastic boxes and brought back to the lab for morphological descriptions.

Macromorphological descriptions were done, based on the fresh specimens and colour codes were given following the colour charts of Kornerup and Wanscher (1978). The specimens were dried in a hot air dryer at 50 °C until the samples were completely dried and then kept separately in zip-lock plastic bags. The specimens were deposited in the Herbarium of Mae Fah Luang University (MFLU). Micromorphological characters were observed from the dried specimens. A razor blade was used to make thin sections of the specimens and these were mounted on slides in water, 5% potassium hydroxide (KOH) solution or 1% ammoniacal Congo red. The microcharacters were studied and photographed using a compound microscope Nikon Eclipse Ni. Freehand drawings were made for the microscopic features. Fifty basidiospores per basidioma were measured in side view. The notation [x/y/z] denotes the number of basidiospores (x) measured from the number of basidiomata (y) of the number of collections (z). At least 25 basidia, pleurocystidia, cheilocystidia, and pileipellis hyphae were observed and measured. The dimensions of microscopic structures are presented in the following format: (a–)b–c–d (−e), in which c represents the average, b the 5th percentile, d the 95th percentile, and minimum and maximum values a and e are shown in parentheses. Q, the length/width ratio, is presented in the same format. Facesoffungi numbers and MycoBank numbers are provided for each new species.

DNA extraction and sequencing

Genomic DNA was extracted from the dried herbarium specimens using the Biospin Fungus Genomic DNA Extraction Kit (Bioer Technology, Hangzhou, China), following the manufacturer’s instructions. The ITS region and parts of the nrLSU and tef1 genes were amplified by a polymerase chain reaction (PCR) and sequenced. The following primers were used: ITS1-F and ITS4 for ITS (White et al. 1990; Gardes and Bruns 1993), LR0R and LR5 for nrLSU (Vilgalys and Hester 1990; White et al. 1990) and EF1-983F and EF1-1567R for tef1 (Rehner and Buckley 2005). The PCR cycling for ITS and LSU was as follows: 3 min at 94 °C; 35 cycles of 30 s at 94 °C, 30 s at 52 °C, 1 min at 72 °C; 10 min at 72 °C. For tef1, the following programme was used: 5 min at 95 °C; 35 cycles of 1 min at 94 °C, 2 min at 52 °C, 1.5 min at 72 °C; 10 min at 72 °C. The PCR-amplified products were purified and sequenced in forward and reverse directions, using PCR primers by Sangon Biological Engineering Technology & Services (Shanghai).

Sequence alignment and phylogenetic analyses

Sequence reads were checked using Bioedit Sequence Alignment Editor version 7.0.9.0 and assembled using SeqMan (DNAstar, Madison, WI, USA). Each sequence was blasted using the Basic Local Alignment Search Tool (BLAST) against the National Center for Biotechnology Information (NCBI) database (http://www.ncbi.nlm.nih.gov/genbank/) to check that it was from the correct genus and not from contamination, as well as to find the closest matches. Newly-generated sequences were deposited in GenBank. All sequences (Table 1) including the outgroup were retrieved and aligned using MAFFT v.7 (Katoh et al. 2017) on the online server (http://mafft.cbrc.jp/alignment/server/). For tef1, introns were delimited by comparing with the amino acid sequence of a reference sequence and locating the GT/AG motifs of the splicing sites and removed for further analyses. The ITS and LSU alignments were trimmed separately using TrimAl to eliminate ambiguously aligned positions (Capella-Gutiérrez et al. 2009). The length of each character set was: ITS1+ITS2 = 445; LSU+5.8S = 995; TEF1 (exons) = 438. After checking for supported conflicts (BS ≥ 70%) between single-gene Maximum Likelihood (ML) phylogenies, a concatenated three-gene dataset was assembled.

Table 1.

GenBank accession numbers and geographical origins of taxa used in the phylogenetic analyses.

Species Specimen/culture Country GenBank accession numbers
ITS nLSU tef1
Hohenbueheliaalgonquinensis RGT 870601/12 UWO (culture T-434) Canada KU355341 AF139950 KU355456
H.angustata CBS 856.85 Canada MH861919 MH873608 –
H.atrocoerulea AMB 18080 Hungary KU355304 KU355389 KU355439
H.auriscalpium PRMJH1372007 Czech Republic MT525862 MT534054 –
H.bonii K(M):165700 England KX064444 – –
H.boullardii JCM06005 Spain MG553637 MG553644 –
H.canadensis, as H.atrocoeruleavar.grisea DAOM 158848 Canada KU355356 – –
H.carlothornii AMB 18106 Costa Rica KY698012 KY698013 –
H.chevallieri WU:6528 Austria KT388040 – –
H.culmicola Roux 3488 Italy KU355323 – –
H.cyphelliformis Z+ZT 994 Switzerland KU355325 KU355393 KU355445
H.faerberioides Mertens France MG553638 MG553645 MW240984
H.flabelliformis MFLU22-0008 Thailand OP236779 OM521957 OM714821
H.flabelliformis MFLU22-0009 Thailand OP236780 – –
H.fluxilis WU 29608 Austria KU355326 – –
H.grisea MCVE 27293, as H.myxotricha Italy KU355329 KU355394 KU355447
H.grisea VPI-F-0001921 (culture VT 1324 = T-132), as H.nigra USA KY679143 KY679143 –
H.grisea MFLUCC 12-0451 Thailand MF150036 – –
H.grisea HFJAU0029 China MN258645 – –
H.ilerdensis Roux 3924 Spain MG553639 MG553646
H.josserandii P.K. EG10-812-T-F Germany KU355353 KU355403 KU355463
H.lageniformis MFLU22-0010 Thailand OP236781 OM521958 OM763737
H.lageniformis MFLU22-0012 Thailand OP236783 OM521959 –
H.leightonii WU 5846 Spain MG553640 MG553647 –
H.ligulata PDD:80775 New Zealand KM975439 – –
H.longipes LIP 0400317 Italy KU355333 KU355396 KU355449
H.mastrucata TRTC 152314 Italy KU355336 KU355397 KU355451
H.mustialensis DAOM 46374 Canada KY124252 – –
H.nimueae RGT 871128/01 UWO (culture T-489 = CBS 212.91), as H.nigra Canada KY679144 KY679144 –
H.odorata TBGT17443 India MN059651 – –
H.petaloides AMB 18088 Italy KU355346 KU355402 KU355460
H.pinacearum DAOM 84313 Canada MH137814 MH137837 –
H.portegna J.E. Wright 1136 BAFC Argentina AF139959 AF139959 –
H.tristis MFLU22-0015 Thailand OP355451 OM521961 –
H.tristis MFLU22-0016 Thailand OP355450 OM521962 ON394004
H.reniformis HMJAU7091 China GQ142024 GQ142041 –
H.robusta CBS 130.68 – MH859087 MH870800 –
H.thornii WU 21790 Portugal KU355343 KU355401 KU355457
H.tremula M 0223665 Italy KU355358 KU355406 KU355466
H.tristis RV95/214 DUKE Australia – AF042601 –
H.tristis RV95/295 DUKE Australia – AF135171 –
H.unguicularis Z+ZT 1112 France KU355361 KU355408 KU355467
H.valesiaca Roux 2975 France KU355340 KU355399 KU355455
H.wilhelmii Z+ZT n. 1154 France MF494947 MF494948 MF494949
Pleurotuscitrinopileatus YAASM1585 China KX836372 – KX840311
P.eryngii CCMSSC00480 China KX836350 – KX840226
P.ostreatus TENN 53662 (= AFTOL-ID 564) Austria AY854077 AY645052 AY883432
P.djamor, as P.placentodes HKAS51745 China KR827693 KR827695 KR827699
P.pulmonarius BCRC36906 Taiwan MH453616 MH447275 MH500353
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Notes: The newly-generated sequences in this study are presented in bold, “–” refers to the unavailability of sequence.

All phylogenetic analyses were done on the CIPRES Science Gateway version 3.3 web server (Miller et al. 2010), accessed at https://www.phylo.org/. For both Maximum Likelihood and Bayesian analyses, a mixed-model (partitioned) scheme was used, with the alignment divided in the following three character sets: ITS1+ITS2, LSU+5.8S, tef1. Maximum Likelihood phylogenetic inference was performed using RAxML-HPC2 version 8.2.12 (Stamatakis 2006) on XSEDE. Five Pleurotus species were used as outgroup. For Bayesian analysis, the best-fit substitution models were selected from jModelTest2 version 2.1.6 (Darriba et al. 2012) on XSEDE. The best-fit models were HKY+G for ITS1+ITS2, GTR+I+G for nrLSU+5.8S and SYM+G for tef1. Bayesian analysis was performed in MrBayes version 3.2.7a (Ronquist et al. 2012). Two runs of five chains each were run for 500,000 generations and sampled every 200 generations. The average standard deviation of split frequencies was 0.008720 at the end of the runs. The burn-in phase (25%) was estimated by checking the stationarity in the generation-likelihood plot in Tracer ver. 1.7.1 (Rambaut et al. 2018). The phylogenetic tree was visualised and edited in FigTree version 1.4.4 (Rambaut 2018).

Results

Phylogenetic analyses

The combined dataset consisted of 39 Hohenbuehelia and five Pleurotus accessions (Table 1). The final alignment, including the gaps, was 1,878 characters long and was deposited in TreeBASE (submission ID 29653). The Bayesian and ML analyses resulted in similar tree topologies; thus, only the ML tree is shown with both Maximum Likelihood bootstrap (BS) values and Bayesian posterior probabilities (PP) (Fig. 1). In the phylogram, H.flabelliformis (MFLU22-0008 and MFLU22-0009) was closely related to H.algonquinensis (RGT 870601/12 UWO) from Canada with high support (90% BS, 1.00 PP). Hohenbuehelialageniformis (MFLU22-0010 and MFLU22-0012) was closely related to H.odorata (TBGT17443) from India with high statistical support (96% BS, 1.00 PP). The sequences of H.tristis (MFLU22-0015 and MFLU22-0016) are identical to two sequences from GenBank identified as H.grisea from Thailand (culture MFLUCC 12-0451) and China (HFJAU0029) with three substitution heteromorphisms and were closely related to H.tristis (RV95/214 DUKE and RV95/295 DUKE) from Australia with 92% BS, but low support in the BI analysis.

Figure 1.

Figure 1.

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Phylogeny of selected sequences of Hohenbuehelia based on a Maximum Likelihood analysis of three nuclear gene regions (nrITS, nrLSU, tef1). The Maximum Likelihood bootstrap values (BS ≥ 70%) and Bayesian posterior probabilities values (PP ≥ 0.90) are shown on the branches. Newly-sequenced collections are in bold. Five Pleurotus species were used as outgroup. (T) designates holotypes. The sequence H.flabelliformis voucher number MFLU22-0008 was identical to MFLU22-0009 (ITS only). Sequences of H.lageniformis voucher number MFLU22-0010 were identical to MFLU22-0012 (ITS and LSU). Sequences of H.tristis voucher number MFLU22-0016 were identical to MFLU22-0015 (ITS and LSU) and to the two specimens MFLUCC 12-0451 and HFJAU0029, identified as H.grisea (both only ITS) from GenBank, except for three substitution heteromorphisms in the ITS sequence of MFLU22-0016 (see Table 2).

Taxonomy

. Hohenbuehelia flabelliformis

Phonemany & Raspé sp. nov.

98C53127-8E77-5CC6-8B74-F912A9EEA19D

MycoBank No: 843984

Facesoffungi Number: FoF10708

Figs 2 , 3

Figure 2.

Figure 2.

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Basidiomata of Hohenbueheliaflabelliformis in the field a, c–e MFLU22-0008 b MFLU22-0009. Scale bars: 1 cm (a–e).

Figure 3.

Figure 3.

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Micromorphology of Hohenbueheliaflabelliformis (MFLU22-0008, MFLU22-0009) a basidiospores b pleurocystidia c basidia and basidioles d pileipellis. Scale bars: 10 µm (a, c); 20 µm (b, d).

Diagnosis.

This species is distinguished from other Hohenbuehelia species by large flabelliform basidiomata, yellowish-white pileus that is densely villose with white hairs longer near the point of attachment, and shorter towards the margin, ellipsoid basidiospores, absence of cheilocystidia, and a trichoderm pileipellis.

Holotype.

Thailand, Chiang Mai Province, Mae Taeng District, Pha Daeng Village, 27 May 2019, Monthien Phonemany (MFLU22-0008).

Etymology.

"flabelliformis" refers to the flabelliform shape of basidiomata.

Description.

Pileus 35–45 × 20–40 mm, spathulate when young, expanding to spathuliform, flabelliform, rounded flabelliform or orbicular, white when young, becoming yellowish-white to pale yellow (4A2–4A3) at the centre and cream (2A3–2B3) to slightly darker elsewhere in age; surface densely villose with white hairs that are longer near the attachment and shorter towards the margin, as observed with a lens; margin white, incurved when young, becoming straight when old. Lamellae 1–3 mm wide, decurrent, pale yellow to yellowish-white (4A3–4A2), moderately crowded when mature, with lamellulae in 1–3 tiers; edge concolorous to sides, fimbriate. Stipe absent or as pseudostipe 5–12 mm × 3–8 mm. Context consisting of two layers: 1) non-gelatinous layer, 1 mm thick, soft when young and rather leathery when old, white to dirty white (4A1–4A2); 2) gelatinous layer 0.5 mm thick, soft, sticky, colourless. Odour mild, pleasant. Taste none. Spore print white.

Basidiospores [150/3/2] (5.8–)6–7–8(–8.6) × (3.5–)4–4.2–5(–5.1) µm, Q = (1.3–)1.36–1.67–2.01(–2.03), ellipsoid to elongate (oblong) in side view, smooth, thin-walled, inamyloid. Basidia (21–)21–25.8–35(–37) × (5–)5.3–7.3–10.5(–11) µm, subclavate to clavate, with 4 sterigmata 4–8 µm long, hyaline, smooth, thin-walled. Cheilocystidia absent. Pleurocystidia metuloidal, present on both sides of lamellae and visible with a lens, (34–)34–42–54(–55) × (8.5–)8.5–11–14(–14.5) µm, scattered, narrowly fusiform to fusiform, mucronate at apex, brownish in KOH. Hymenophoral trama irregular, hyphae 2–5 µm wide. Pileipellis a trichoderm, hyaline in KOH, brownish in water, with cylindrical terminal elements 34–86 × 4–7 µm. Pileoleptocystidia absent. Pileus trama consists of two different layers: 1) upper layer gelatinous, composed of horizontally arranged, smooth, colourless encrusted hyphae, 2–5 µm wide; 2) lower layer, non-gelatinous, composed of interwoven, smooth, hyaline hyphae, 2–4 µm wide. Clamp connections present in pileipellis, pileus trama, and hymenophoral trama.

Habitat and distribution.

On dead wood, scattered or fasciculate by 2–4 basidiomata. So far only found in tropical forests of northern Thailand.

Additional specimens examined.

Thailand. Chiang Rai Province, Pa Daed District, Pa Ngae Village, 9 August 2019, Monthien Phonemany (MFLU22-0009).

Notes.

The basidiomata colour of Hohenbueheliaflabelliformis is similar to H.angustata (Berk.) Singer, H.bonii A.M. Ainsw., H.concentrica Corner, H.carlothornii Consiglio, Setti & Thorn, H.horrida (Boedijn) Corner, H.luteola G. Stev, H.malesiana Corner, H.odorata C.K. Pradeep & Bijeesh, H.olivacea Yu Liu & T. Bau, and H.testudo (Berk.) Pegler. The basidiomata range from white, yellowish-white, yellow-brown, to pinkish-orange, and are spathulate to flabelliform. Hohenbueheliaangustata, originally described from Brazil, differs from H.flabelliformis by its smaller, smooth, greyish-yellow basidiomata, with stipe 4.5 mm long, smaller basidiospores (3.5–5 × 2.5–3.5 µm), smaller cheilocystidia, and the presence of pileocystidia (Silva-Filho and Cortez 2017). H.horrida and H.odorata differ from H.flabelliformis by smaller basidiospores (5.2–7.6 × 4.8–6.4 µm), lack of cheilocystidia, and presence of pileoleptocystidia (Bijeesh et al. 2019). Hohenbueheliatestudo differs by smaller basidia (20–25 × 5–6 µm), larger pleurocystidia (44–78 × 12–18 µm) with thick yellowish walls, and the presence of cheilocystidia (Corner 1994). Hohenbueheliamalesiana, described from Brazil, is different from H.flabelliformis by having longer, subcylindrical basidiospores (7–9 × 3.5–4 µm), pileipellis as an interrupted cutis, and presence of cheilocystidia (Corner 1994). Hohenbueheliabonii, from England, has larger yellow-brown basidiomata (20–75 mm diam.), smooth pileus surface, larger basidiospores (7.2–10.4 × 4.5–6.1 µm), larger pleurocystidia (56–103 × 11–19 µm), and an ixotrichoderm or ixocutis pileipellis (Ainsworth et al. 2016). Hohenbueheliacarlothornii described from Costa Rica, is different by having off-white basidiomata with a large pseudostipe (20–32 × 14–25 mm), presence of cheilocystidia (Consiglio et al. 2018b). Hohenbueheliaconcentrica from Singapore, has larger basidiomata (80 mm wide), larger basidiospores (8–8.5 × 6–6.7 µm), and absence of cheilocystidia (Corner 1994). Hohenbueheliaincarnata, from the Solomon Islands, differs from H.flabelliformis by subglobose basidiospores and the presence of subcylindrical to submoniliform cheilocystidia (Corner 1994). Hohenbueheliaolivacea, originally described from China, has reniform basidiomata with dense and long tomentum, light brown to pallid brown in gelatinous zone, and the presence of cheilocystidia (Liu and Bau 2009).

Phylogenetically, H.flabelliformis was closely related to H.algonquinensis Consiglio, Setti & Thorn. (voucher RGT 870601/12 UWO) with 3.5% (21/599) differences in the ITS sequence, 1.4% (12/839) in the LSU sequence, and 6.66% (35/540) in the tef1 sequence. Moreover, the morphologies of both species are completely different, with H.algonquinensis having glossy black pileus, ungulate to dimidiate basidiomata and contrasting white or off-white lamellae (Consiglio et al. 2018b).

. Hohenbuehelia lageniformis

Phonemany & Raspé sp. nov.

B27429FD-2A21-5A2C-A8CE-62C1441E7BA5

MycoBank No: 843985

Facesoffungi Number: FoF10709

Figs 4 , 5

Figure 4.

Figure 4.

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Basidiomata of Hohenbuehelialageniformis on the substrate and detailed photographs in the lab a–c MFLU22-0010 d MFLU22-0012 e, f MFLU22-0014. Scale bars: 1 cm (a–e); 2 cm (f).

Figure 5.

Figure 5.

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Micromorphology of Hohenbuehelialageniformis (MFLU22-0010, MFLU22-0012, MFLU22-00104) a basidiospores b basidia c pleurocystidia d cheilocystidia e pileipellis. Scale bars: 5 µm (a); 20 µm (b, c); 10 µm (d); 50 µm (e).

Diagnosis.

This species is distinguished from other Hohenbuehelia species by having velutinous pileus with whitish hairs near the point of attachment, and at the margin, elsewhere pale greyish-yellow, and with only sparse white hairs, pale brown to light brown and mucilaginous context, subglobose to ellipsoid basidiospores, lageniform cheilocystidia, an ixotrichoderm pileipellis, and the absence of pileoleptocystidia.

Holotype.

Thailand, Chiang Mai Province, Mae On District, Huai Kaew Subdistrict, Pok Village, 29 June 2019, Monthien Phonemany (MFLU22-0010).

Etymology.

"lageniformis" refers to the lageniform shape of cheilocystidia.

Description.

Pileus 25–30 × 15–25 mm, spathuliform when young, rounded flabelliform to sub-rounded flabelliform when mature, light yellow (4A4), pale orange to orange white (5A2–5A3), greyish-orange (5B4) becoming darker with age, sometimes sessile or with laterally attached stipe; surface moist, shiny, velutinous with whitish (1A1) hairs near the point of attachment, elsewhere light yellow to pale greyish-yellow (4A4–4B4); margin discolorous from pileus, velutinous with whitish hairs as observed under the lens, incurved even when mature, entire or sometimes undulate when old. Lamellae 1–2 mm wide, decurrent, white to pale orange (5A1–5A2) becoming slightly dark in age, close to moderately crowded, in 2–3 tiers. Stipe absent or sometimes with pseudostipe 0.5–1 mm long when young and disappearing when mature. Context consisting of two layers: 1) non-gelatinous layer, 1 mm thick, fleshy, white (1A1); 2) gelatinous layer, 1–2 mm thick, soft, sticky, brownish-orange to light brown (5C5–5D5). Odour mild. Taste none. Spore print white.

Basidiospores [150/3/3] (6.9–)7–8.8–10(–10.5) × (5.5–)6–7.0–8(–8.3) µm, Q = (0.99–)1.11–1.26–1.49(–1.53) subglobose to ellipsoid in front view, ellipsoid to phaseoliform in side view, smooth, thin-walled, inamyloid. Basidia (24.3–)24–31.9–53(–58.2) × (5.4–)5.5–9.4–14(–14.6) µm, clavate, with (2)–4 sterigmata, 4–8 µm long, hyaline, smooth, thin-walled. Cheilocystidia (17.6–)18–21.9–26.5(–26.9) × (3.2–)3–5.0–9(–8.9) µm, lageniform with an inflated base with a thin, rostrate apex, hyaline, thin-walled. Pleurocystidia (31–)31–50.3–70(–71) × (9.7–)10–15.3–20(–20.3) µm, metuloidal, setiform, narrowly fusiform to fusiform, encrusted with crystals, brownish or yellowish in water, colourless, but still encrusted with crystals in KOH. Hymenophoral trama subregular, hyphae 2–4 µm wide. Pileipellis an intricate trichoderm with cylindrical terminal elements 41–122 × 2–5 µm. Pileoleptocystidia absent. Pileus trama consisting of two layers: 1) upper layer gelatinous, composed horizontally arranged, smooth, colourless, encrusted hyphae, 1–4 µm wide; 2) non-gelatinous layer, composed interwoven, smooth with hyaline hyphae, 2–5 µm wide. Clamp connections present in pileipellis, pileus trama and hymenophoral trama.

Habitat and distribution.

Solitary, gregarious to imbricate, on decaying branches in a tropical forests in northern Thailand.

Additional specimens examined.

Thailand. Chiang Rai Province, Muang Chiang Rai District, Mae Yao Subdistrict, Huai Mae Sai Village, 10 July 2019, Monthien Phonemany (MFLU22-0011); ibid., 10 July 2019, Monthien Phonemany (MFLU22-0012); ibid., 10 July 2019, Monthien Phonemany (MFLU22-0013); Pa Daed District, Pa Ngae Village, 7 September 2019, Monthien Phonemany (MFLU22-0014).

Notes.

Hohenbuehelialageniformis is characterised by velutinous pileus with whitish hairs near the point of attachment and at the margin, elsewhere pale greyish-yellow and with only sparse white hairs, subglobose to ellipsoid basidiospores, and the absence of pileoleptocystidia. Hohenbueheliaangustata, H.bonii, H.carlothornii, H.concentrica, H.flabelliformis, H.horrida, H.luteola, H.mellea Corner, and H.odorata have similar pileus colour, for example, pale orange to orange white, light yellow, yellowish-white, yellow-brown, honey-yellow or ochraceous brownish. However, those species have significant morphological differences. Hohenbueheliaangustata differs from H.lageniformis by having a smooth pileus surface, serrate margin, smaller basidiospores (3.5–5 × 2.5–3.5 µm), cutis pileipellis (Silva-Filho and Cortez 2017). Hohenbueheliabonii differs by having a smooth pileus surface and larger pleurocystidia (56–103 × 11–19 µm) (Ainsworth et al. 2016). Hohenbueheliacarlothornii differs by having finely white-tomentose pileus, smaller basidiospores (7–8.2 × 3.1–3.7 µm), smaller basidia (19–24 × 5.2–6.8 µm), smaller cheilocystidia (13–17 × 4.9–9.4 µm), and larger pleurocystidia (55–63 × 14–18 µm) (Consiglio et al. 2018b). Hohenbueheliaconcentrica has larger basidiomata (80 mm wide), ovoid basidiospores (8–8.5 × 6–6.7 µm), and no cheilocystidia (Corner 1994). Hohenbueheliahorrida has pale grey to greyish-brown lamellae, larger basidiomata (70 mm wide), smaller basidiospores (5–6 × 3–4 µm), smaller basidia (18–25 × 3–4 µm), and larger pleurocystidia (140 × 12.5 µm) (Corner 1994). Hohenbuehelialuteola differs by smaller basidiospores (8–9 × 4.5–5 μm), and smaller pleurocystidia (45–50 ×15–20 µm) (Stevenson 1964). Hohenbueheliamellea has smaller basidiospores (5–6.5 × 2–3.5 µm), larger cheilocystidia (30–50 × 8–18 µm), and larger pleurocystidia (50–160 × 12–20 µm) (Corner 1994). Hohenbueheliaflabelliformis has thinner gelatinous layer (0.5 mm), smaller basidiospores (6–8 × 4–5 µm), smaller pleurocystidia (34–54 × 8.5–14 µm), and no cheilocystidia. Hohenbueheliaodorata differs by having smaller basidiospores (5.2–7.6 × 4.8–6.4 µm), smaller cheilocystidia (15–23.5 × 3–7 µm), smaller pleurocystidia (28.5–49 × 10–14.5 µm), and presence of cylindrical to flexuous pileoleptocystidia (Bijeesh et al. 2019).

In the phylogenic tree, the most closely-related species to H.lageniformis was H.odorata (voucher TBGT17443). However, the genetic distance between the ITS sequence of H.lageniformis and H.odorata was 4.62% (27/584), which supports the distinction of the two species. Moreover, these two species also show morphological differences (see above).

. Hohenbuehelia tristis

G. Stev.

73D7AFED-3038-5FD2-AE0E-17EF3A25B5CB

MycoBank No: 332010

Figs 6 , 7

Figure 6.

Figure 6.

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Basidiomata of Hohenbueheliatristis in the field a–c MFLU22-0015 d MFLU22-0016. Scale bars: 1 cm (a–d).

Figure 7.

Figure 7.

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Micromorphology of Hohenbueheliatristisa basidiospores b basidia c pleurocystidia d cheilocystidia e pileipellis (MFLU22-0015, MFLU22-0016). Scale bars: 5 µm (a), 10 µm (b, d), 20 µm (c), 50 µm (e).

Remarks.

The following description is based solely on the Thai materials we collected and examined.

Description.

Pileus 15–20 × 20–30 mm, spathuliform to reniform, dimidiate to orbicular, greyish-white (1B1) to yellowish-white (1B2) when young, becoming white (1A1) in age, glutinous, very faintly translucent, shiny when mature; upper surface minutely pubescent with greyish hairs (5A1–5B1) near the point of attachment and more sparsely so towards the margin as observed with a lens, with hairs disappearing in age; margin incurved becoming upturned in age. Lamellae radiating from point of attachment, 1 mm broad, very crowded, white (1A1) to pale yellow (1A3); lamellulae in 1–4 tiers. Stipe absent or pseudostipe sometimes present, laterally or dorsally attached, 1 mm long when young, then disappearing when old. Context consisting of two layers: 1) leathery layer, 1 mm thick; 2) gelatinous layer, 1–2 mm thick, soft, sticky, colourless. Odour and taste not observed. Spore print white.

Basidiospores [150/3/2] (5.1–)6–6.8–8(–9) × (3.5–)3.5–4.0–5(–5.2), Q = (1.21–)1.38–1.70–2.08(–2.26), ellipsoid, sub-ellipsoid to elongate, smooth, thin-walled, inamyloid. Basidia (13–)14–21.2–24(–24.2) × (5–)5.5–6.6–7(–7) µm, clavate to subcylindrical, mostly with four sometimes with two sterigmata, 2–4 µm long, hyaline, smooth, thin-walled. Cheilocystidia (10.9–)11–13.1–19(–19.8) × (4.2–)4.4–5.5–6.5(–6.5) µm, lecythiform to sublageniform, with subcapitate to capitate apex, hyaline, thin-walled. Pleurocystidia (38–)38–61.5–82(–82) × (10.7–)11–15.0–18.5(–18.6) µm, subfusiform, narrowly fusiform to fusiform, brownish, encrusted with crystals when observed in water, but crystals disappearing in KOH. Hymenophoral trama subregular, hyphae 2–4 µm wide. Pileipellis as tufts of ixotrichoderm with cylindrical terminal elements 40–105 × 3–5.5 µm, with light brown intracellular pigments. Pileoleptocystidia absent. Pileus trama consisting of two layers: 1) upper layer gelatinous, composed of horizontally arranged, smooth, colourless, encrusted hyphae, 1.5–2.5 µm wide; 2) lower layer non-gelatinous, composed of interwoven, smooth and hyaline hyphae, width 2–4 µm. Clamp connections present in pileipellis, pileus trama and hymenophoral trama.

Habitat.

Solitary, gregarious to imbricate, on dead small branches.

Specimens examined.

Thailand. Chiang Rai Province, Muang Chiang Rai District, Nang Lae Nai Village, 31 July 2019, Monthien Phonemany (MFLU22-0015). Chiang Rai Province, Muang Chiang Rai District, Mae Yao subdistrict, Huai Mae Sai Village, 31 July 2019, Monthien Phonemany (MFLU22-0016).

Notes.

Two accessions identified as H.grisea, the culture MFLUCC 12-0451 from Thailand and HFJAU0029 from China (unpublished), had the same ITS sequence than H.tristis (MFLU22-0015 and MFLU22-0016) except for three substitution heteromorphisms in the ITS sequence of MFLU22-0016 (see Table 2). The two former sequences retrieved from GenBank have no corresponding morphological descriptions available as evidence. Therefore, these might have been wrongly identified, since ITS sequences are identical to sequences obtained from our collections of H.tristis (except for the heteromorphisms detailed in Table 2). Additional confirmation of the taxonomic identity of our specimens was obtained by comparing the morphology of our specimens with H.grisea which was originally described as Pleurotusatrocoeruleusvar.griseus Peck from New York. The latter is distinguished by a greyish to greyish-brown, sparsely tomentose pileus, the lamellae becoming cream-coloured in age (Peck 1891). Hohenbueheliatristis is characterised by reniform basidiomata, minutely pubescent pileus with greyish hairs that disappear when mature, leaving the surface gelatinous, faintly translucent and shiny, ellipsoid to sub-ellipsoid basidiospores, lecythiform to sublageniform cheilocystidia, and an ixotrichoderm pileipellis. Hohenbueheliatristis described from New Zealand differs from our collections (MFLU2022-0015 and MFLU2022-0016) by having smaller basidiomata (10–20 × 10–15 mm), smaller (mostly narrower) basidiospores (7 × 3 µm), larger and pseudo-amyloid metuloids (80–90 × 15–20 µm), pileipellis as tufts of parallel larger hyphae (3–8 µm in diam.) (Stevenson 1964). In our phylogenetic analysis (Fig. 1), the Thai accessions of H.tristis formed a monophyletic group with the accessions of H.tristis from New Zealand. The morphological differences we observed between the Thai and New Zealand accessions suggested that they might not be conspecific. Additionally, the single synapomorphic position we observed in the LSU sequence (position 685 in the alignment; see Table 3) is not incompatible with two distinct species, since a genetic distance of only one substitution can be observed between other closely-related species (e.g. H.tremula and H.longipes; Table 4). However, the LSU sequence of the Thai specimen MFLU22-0016 showed two to three heteromorphisms corresponding to the differences between the other Thai specimens and the New Zealand specimens (Table 3). This suggests either incomplete lineage sorting or that the two lineages can still interbreed. Heteromorphisms were also observed in the ITS sequence of MFLU22-0016, but we could not compare with ITS sequences of materials from New Zealand, which were unavailable. In view of all the heteromorphisms, we decided not to treat the Thai materials as a new species distinct from H.tristis.

Table 2.

Positions of substitution heteromorphisms in the ITS sequence of H.tristis MFLU22-0016 and corresponding character states in other H.tristis ITS sequences.

Specimen name/vouchers Accession number Position in alignment
147 552 588
H.tristis MFLU22-0015 OP355451 T C T
H.tristis MFLU22-0016 OP355450 K Y Y
H.tristis MFLUCC 12-0451(as H.grisea in GenBank) MF150036 T C T
H.tristis HFJAU0029(as H.grisea in GenBank) MN258645 T C T
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Table 3.

Position of substitutions and substitution heteromorphisms in the LSU sequence of H.tristis MFLU22-0015, MFLU22-0016, and corresponding character states in H.tristis RV95/214 DUKE, RV95/295 DUKE.

Specimen name/vouchers Accession number Position in the alignment
658 663 664 666
H.tristis MFLU22-0015 OP355451 C G T G
H.tristis MFLU22-0016 OP355450 Y G Y R
H.tristis RV95/214 DUKE AF042601 T A T A
H.tristis RV95/295 DUKE AF135171 T G C A
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Table 4.

Genetic distance (number of substitutions, excluding heteromorphisms) between LSU sequences of closely-related Hohenbuehelia species.

Species name/ specimen number 1 2 3 4 5 6 7 8 9
1. H.tristis MFLU22-0015
2. H.tristis MFLU22-0016 0
3. H.atrocoerulea AMB 18080 13 13
4. H.carlothornii AMB 18106 3 3 14
5. H.reniformis HMJAU7091 11 11 2 12
6. H.robusta CBS 130.68 3 3 14 0 12
7. H.tristis RV95/214 DUKE 3 2 15 5 13 5
8. H.tristis RV95/295 DUKE 3 1 14 4 12 4 2
9. H.longipes LIP 0400317 24 24 15 23 13 23 24 23
10. H.tremula M 0223665 25 25 16 24 14 24 25 24 1
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Discussion

The Pleurotaceae belong to the Agaricales and comprise the monophyletic pleurotoid genera Pleurotus and Hohenbuehelia (Thorn et al. 2000; Koziak et al. 2007). Hohenbuehelia species have often been misidentified, in part because holotypes are missing or because types of species put in synonymy were not adequately studied (Consiglio et al. 2018b). In the past, most Hohenbuehelia species were introduced, based only on short morphological descriptions (e.g., Peck 1891; Coker 1944; Stevenson 1964). Consiglio (2016, 2017a, b) and Consiglio and Setti (2017) designated lectotypes, neotypes, and epitypes to clarify older species names or names that lack modern and molecularly-characterised holotypes. For example, the holotype of H.tristis was identified by Stevenson (1964) without any molecular evidence. Later, an nrLSU sequence of H.tristis was obtained for the first time by Moncalvo et al. (2000). The heteromorphisms we observed in the nrLSU and ITS sequences of one of the Thai specimens related to H.tristis suggested that interbreeding may occur between two divergent lineages within H.tristis. Although more data would be needed to confirm it, we hypothesise that those two lineages diverged in geographical isolation (between Southeast Asia and Oceania) and then came in contact in Southeast Asia. This kind of biogeographical history, revealed by DNA sequence variation, have been observed in other Agaricales, for example, Agaricussubrufescens Peck (Chen et al. 2016).

Some of the recently-described species were still introduced, based on only single-gene molecular evidence. In this study, we provide multiple-gene sequence data and detailed descriptions supporting the introduction of two new Hohenbuehelia species and a note on H.tristis from Thailand. At present, a total of six Hohenbuehelia species have been reported from Thailand including the ones in this study and three that were previously reported, namely H.panelloides, H.petaloides, and H.reniformis (Chandrasrikul et al. 2011). The report of H.grisea by Sandargo et al. (2018a) has to be excluded since we showed that the correct identification of their material is H.tristis. More studies on Hohenbuehelia are needed to clarify their taxonomy and more new species might be discovered.

Supplementary Material

XML Treatment for Hohenbuehelia flabelliformis
XML Treatment for Hohenbuehelia lageniformis
XML Treatment for Hohenbuehelia tristis

Acknowledgements

Monthien phonemany appreciates the kind support from a Thesis Writing Grant of Mae Fah Luang University, Thailand. The support from the Thailand Research Fund (TRF) grant "Study of saprobic Agaricales in Thailand to find new industrial mushroom products" (Grant No. DBG6180015) and the Thailand Science Research and Innovation (TSRI) grant "Macrofungi diversity research from the Lancang-Mekong Watershed and surrounding areas" (grant No. DBG6280009) is also acknowledged.

Citation

Phonemany M, Vadthanarat S, Raghoonundon B, Thongklang N, Raspé O (2023) Additions to Hohenbuehelia (Basidiomycota, Pleurotaceae): two new species and notes on H. tristis from northern Thailand. MycoKeys 99: 109–130. https://doi.org/10.3897/mycokeys.99.105317

Funding Statement

Thailand Science Research and Innovation

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

Thailand Research Fund and Thailand Science Research and Innovation.

Author contributions

Conceptualization: OR, MP. Formal analysis: MP. Funding acquisition: NT. Investigation: MP. Methodology: OR. Project administration: NT. Supervision: OR. Validation: SV. Writing – original draft: MP, OR. Writing – review and editing: BR, SV, NT, OR.

Author ORCIDs

Monthien Phonemany https://orcid.org/0000-0002-7865-4659

Santhiti Vadthanarat https://orcid.org/0000-0002-9035-0375

Bhavesh Raghoonundon https://orcid.org/0000-0001-6671-2404

Naritsada Thongklang https://orcid.org/0000-0001-9337-5001

Olivier Raspé https://orcid.org/0000-0002-8426-2133

Data availability

All of the data that support the findings of this study are available in the main text, or in publicly accessible data repositories, as indicated in the text.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

XML Treatment for Hohenbuehelia flabelliformis
mycokeys.99.105317-treatment1.xml (25.1KB, xml)
XML Treatment for Hohenbuehelia lageniformis
mycokeys.99.105317-treatment2.xml (24.4KB, xml)
XML Treatment for Hohenbuehelia tristis
mycokeys.99.105317-treatment3.xml (32.6KB, xml)

Data Availability Statement

All of the data that support the findings of this study are available in the main text, or in publicly accessible data repositories, as indicated in the text.

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