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Research Article
New species and new records of Laccaria (Agaricales, Basidiomycota) from Northern Thailand
expand article infoSong-Ming Tang‡§, Santhiti Vadthanarat|, Bhavesh Raghoonundon, Zong-Long Luo§, Xin-Yu Zhu#, Feng-Ming Yu¤, Jun He«, Shu-Hong Li‡
‡ Biotechnology and Germplasm Resources Institute, Yunnan Academy of Agricultural Sciences, Kunming, China
§ Dali University, Dali, China
| Ubon Ratchathani University, Ubon Ratchathani, Thailand
¶ Mae Fah Luang University, Chiang Rai, Thailand
# Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
¤ Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China
« West Yunnan University, Lincang, China

Corresponding author: Shu-Hong Li ( shuhongfungi@126.com )

Academic editor: Samantha C. Karunarathna
© 2024 Song-Ming Tang, Santhiti Vadthanarat, Bhavesh Raghoonundon, Zong-Long Luo, Xin-Yu Zhu, Feng-Ming Yu, Jun He, Shu-Hong Li.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Tang S-M, Vadthanarat S, Raghoonundon B, Luo Z-L, Zhu X-Y, Yu F-M, He J, Li S-H (2024) New species and new records of Laccaria (Agaricales, Basidiomycota) from Northern Thailand. MycoKeys 107: 189-217. https://doi.org/10.3897/mycokeys.107.127907
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Abstract

Two new species Laccaria pseudoalba and L. subroseoalbescens are described and illustrated, based on morphological characteristics and molecular phylogenetic analysis. Two new records, Laccaria umbilicata and L. yunnanensis from Thailand, are also reported. Laccaria subroseoalbescens is characterized by small basidiomata, stipe equal with an enlarged base, and nearly subclavate, pale pink to light orange. Laccaria pseudoalba is characterized by pale orange to orange white pileus, has umbo when young on the pileus, and fistulose stipe of the pale to pastel red color. Phylogenetic analysis based on sequence data from rDNA internal transcribed spacer ITS1-5.8S-ITS2 rDNA (ITS), nuc 28S rDNA (28S), RNA polymerase II subunit 2 (rpb2), and translation elongation factor 1-α (tef1-α) are provided as further evidence. Molecular analysis confirms the phylogenetic positions of the two new species and two new records. The differences in characteristics of these two new species and closely related species are discussed herein.

Key words

2 new taxa, Hydnangiaceae, phylogeny, taxonomy

Introduction

The genus Laccaria Berk. & Broome, 1883 is a group of ecologically important ectomycorrhizal fungi that inhabit the soil (He et al. 2019). Laccaria, along with Hydnangium Wallr., Maccagnia Mattir. and Podohydnangium G.W. Beaton, Pegler & T.W.K. Young, belongs to the family Hydnangiaceae within the order Agaricales, phylum Basidiomycota.

Species of Laccaria are characterized by collybioid to omphaloid basidiomata; echinulate, acyanophilous, and inamyloid basidiospores; and a convex, plane, or umbilicate, hygrophanous pileus. Clamps are present in all parts of the basidiomata (Singer 1986; Mueller 1992; Latha and Raj 2019). Approximately 100 species of Laccaria have been described worldwide (according to Index Fungorum 2024), known to form symbiotic associations with plants of more than 20 genera (including Abies, Castanea, Fagus, Pinus, Picea, Quercus, Larix, Lithocarpus, and others) (Wilson et al. 2017). These associations benefit plant growth and facilitate effective nutrient acquisition (Smith and Read 2008). Therefore, studying Laccaria diversity is crucial for understanding terrestrial ecosystems and forest management.

Laccaria species are globally distributed and have been reported on every continent except Antarctica (Kropp and Mueller 1999). They have been found in association with both angiosperms and gymnosperms worldwide (Wilson et al. 2017) and form ectomycorrhizas (ECM) with many economically important plant species (Kropp and Mueller 1999). However, due to the morphological similarity among Laccaria species, defining species boundaries within the genus is challenging (Sheedy et al. 2013).

Since the establishment of Laccaria by Berk. and Broome (1883), many mycologists have contributed to its taxonomy (Orton 1960; McNabb 1972; Mueller 1984; Wang et al. 2004; Wilson et al. 2013, 2017; Popa et al. 2014; Popa et al. 2016; Luo et al. 2016; Cho et al. 2018; Li 2020). Historically, Laccaria was divided into Russuliopsis by J. Schröt, who only included species with a white spore print in Laccaria (Mueller and Vellinga 1986). To date, seven sectional names have been introduced within Laccaria (http://www.indexfungorum.org/Names/Names.asp; accessed date: 20 June 2024), leading to much controversy in its taxonomy.

The number of Laccaria species described from Asia has been increasing, with more studies focusing on Basidiomycetes. Since 2013, twenty-three new species of Laccaria have been described in Asia (Wilson et al. 2013; Popa et al. 2014; Luo et al. 2016; Popa et al. 2016; Cho et al. 2018; Li 2020; Cui et al. 2021; Zhang et al. 2023). Nevertheless, no Laccaria species were reported or described in Thailand during the same period.

Thailand is renowned as one of the world’s most important biodiversity hotspots with high fungal diversity (Hyde et al. 2018; Thongbai et al. 2018). During our recent investigation of Laccaria in Thailand, nine Laccaria specimens were collected. Based on morphological characteristics and phylogenetic analysis, two undescribed species and two new records have been identified. This paper provides detailed descriptions, illustrations, and phylogenetic analyses for these species.

Materials and methods

Morphological study

Specimens were collected from Chiang Mai Province, Thailand. They were photographed in the field, then separately wrapped in aluminium foil or kept in a plastic collection box. The fresh basidiomata were macro-morphologically described on the same day of collection. Colour codes were determined following Kornerup and Wanscher (1978). After being thoroughly dried at 50 °C (Hu et al. 2022) in a food drier, the specimens were stored in sealed plastic bags and deposited in Mae Fah Luang University Herbarium (MFLU) and Herbarium of Cryptogams Kunming Institute of Botany, Academia Sinica (KUN-HKAS). Dried materials were sectioned under a stereo microscope, transferred onto slides, and mounted in a 5% KOH solution. For microscopic characteristics, anatomical and cytological characteristics including basidia, basidiospores, and cystidia, were observed and photographed using a Nikon Eclipse 80i microscope at magnifications up to × 1000. For SEM studies, fragments of the lamellae of the dried material were taken, sputter coated with gold, and analysis with a Hitachi S520 (Hitachi Japan). The notation [x/y/z] specifies that measurements were made on x basidiospores measured from y basidiomata of z collections. At least 50 basidiospores and 20 basidia were measured from one basidioma. Basidiospores dimensions are given as (a–) b–c (–d). Where “a” and “d” refer to the minimum and maximum values of all measurements, respectively, b–c presents the range of 95% of the measured values, and Q is the length/width ratio of basidiospores, Qm is the average Q of all basidiospores and is given as Qm ± standard deviation.

DNA extraction, PCR amplification, and sequencing

Genomic DNA was extracted from dried specimens using Ezup Column Fungi Genomic DNA extraction kit (Sangon China) following the manufacturer’s protocol. Primer pairs for PCR were respectively ITS1/ITS4 (White et al. 1990), LR5/LR0R (Vilgalys and Hester 1990), rpb2-5F/rpb2-7cR (Liu et al. 1999), and tef1-983F/tef1-2218R (Rehner and Buckley 2005). ITS, LSU, rpb2, and tef1 were amplified in 25 μL reactions containing 12.5 μL 2× Taq Plus Master Mix II (Vazyme Biotech Co., Ltd China), 9.5 μL ddH2O, 1 μL 10 μM of forward and reverse primers, 1 μL DNA. PCR conditions were carried out as follows in Table 1 using a C1000 thermal cycler (Bio-Rad China). The PCR amplicons were sent to Sangon Biotech (China) for Sanger sequencing. Sequence reads were assembled in SeqMan II (DNA STAR Inc.).

Table 1.
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PCR primers and cycling conditions used in the study.

Locus Primers (Reference) PCR conditions a
ITS ITS1, ITS4 (White et al. 1990) 94 °C: 30 s, 48 °C: 30 s, 72 °C: 1.00 min. (35 cycles)
LSU LR0R, LR5 (Vilgalys and Hester 1990) 94 °C: 30 s, 48 °C: 30 s, 72 °C: 1.30 min. (35 cycles)
rpb2 f RPB2-5F, b RPB2-7cR (Liu et al. 1999) 95 °C: 30 s, 55 °C: 1 min, 72 °C: 1.30 min. (35 cycles)
tef1 983F, 2218R (Rehner and Buckley 2005) 95 °C: 30 s, 55 °C: 1 min, 72 °C: 1.30 min. (35 cycles)

a The three steps given for each primer pair were repeated for 35 cycles, preceded by an initial denaturation step of 5 min at 94 °C, and followed by a final elongation step of 10 min at 72 °C and a final hold at 4 °C.

Sequence alignment and phylogenetic analysis

The newly generated sequences were checked using BioEdit Sequence Alignment Editor version 7.0.4 and assembled using SeqMan (DNAstar, Madison, WI, USA). The sequences were then blasted using the Basic Local Alignment Search Tool (BLAST) against the GenBank database (Nilsson et al. 2006) to check the most closely related sequences. Reference sequences for a total of 103 specimens representing 55 species were retrieved (Table 2) and minimally adjusted by hand in BioEdit v.7.0.4 (Hall 2007) first, and then aligned using TrimAl (Salvador et al. 2009).

Table 2.
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Laccaria taxa and sample IDs with geographic location and GenBank ID numbers for ITS, LSU, rpb2, and tef1 sequences used in phylogenetic analysis. Sequences produced in this study are marked in bold. “*” following a species name indicates that the specimen is the holotype of that species.

Species name Sample no. Location GenBank accession
ITS LSU rpb2 tef1
Laccaria acanthospora HKAS45998 China KU685719 KU685870 KU686069 –
L. alba F1121461 China JX504129 – – –
ASIS18039 South Korea MG519546 – MG551620 MG551652
TPML20120807-69 South Korea MG519542 MG519583 MG551616 MG551649
L. ambigua PDD89696* New Zealand KU685725 KU685876 KU686018 KU686132
L. amethysteo-occidentalis AWW556 America JX504107 JX504191 KU685919 –
KGP40* America DQ822817 – – –
DAVFP 28205 Canada HQ650762 – – –
L. amethystina GMM7041 Russia KU685654 KU685797 KU685940 –
GMM7621 France JX504150 JX504224 KU686046 KU686152
L. araneosa SFC2013091721* South Korea MG519549 MG519589 MG551622 MG551655
TPML20120912-40 South Korea MG519548 MG519588 MG551621 MG551654
L. aurantia KUNF78557* China NR154113 – – –
MBFB001109 Japan JQ681209 – – –
L. bicolor GMM7620 France JX504149 JX504223 – –
HKAS44062 China JX504159 JX504235 KU686068 –
KA130253 South Korea MG519524 MG519570 MG551599 MG551636
GM7712 USA KM067866 – KU686012 –
L. bullipellis AWW465* China JX504100 JX504184 KU685914 –
L. canaliculata GMM7267 Australia JX504137 JX504213 KU685960 KU686093
L. fagacicola HKAS90435* China MW540806 – – –
HKAS107731 China MW540807 – – –
L. fengkaiensis HKAS106739* China MN585657 MN621238 – –
HKAS106741 China MN585658 – – –
L. fulvogrisea KUN-F78556* China NR154114 – – –
KUN-FB-101105 China JQ681210 – – –
L. guizhouensis HMAS352265* China OP244890 – – –
HMAS352266 China OP244891 – – –
L. glabripes GMM7521 New Zealand KU685708 KU685849 KU685991 KU686117
L. himalayensis AWW463 China JX504098 JX504182 KU685913 –
AWW484* China JX504101 JX504185 KU685915 –
L. japonica F64167* Japan KU962988 – – –
SFC2012072212 South Korea MG519518 MG519566 MG551595 MG551633
L. longipes F1092175 America KU685637 KU685780 – –
L. laccata GMM7615 France JX504148 – – –
L. macrocystidia GMM7616 France KM067850 KU685863 KU686004 –
GMM7612 France KM067847 KU685861 KU686002 –
miniata GDGM76043* China OR689440 OR785476
L. montana TWO591 America DQ149865 – – –
TWO319 America DQ149862 – – –
L. moshuijun HKAS 93732* China KU962989 – – –
HKAS 123302 China ON557378 ON556493 – ON598893
HKAS 110653 China ON557379 ON556494 – –
L. murina ASIS216 South Korea MG519553 – – –
ASIS24249 South Korea MG519552 MG519592 MG551625 MG551658
L. nanlingensis GDGM 84954* China OR689442 OR785478 OR835199 OR826273
GDGM 84949 China OR689441 OR785477 OR835198 OR826274
L. negrimarginata GMM7631 France JX504152 JX504226 – –
BAP360* China JX504120 – – –
L. neovinaceoavellanea GDGM52852* China OR689447 OR785479 – –
GDGM53063 China OR689448 OR785480 – –
GDGM89621 China OR689449 OR785481 – –
L. nobilis F1091206 America KU685636 KU685779 – –
L. oblongospora ObiFr France GQ406466 – – –
L. ochropurpurea PRL4777 America KU685733 KU685883 KU686025 –
L. ohiensis GMM7539 New Zealand KU685712 KU685853 KU685994 KU686119
L. prava A3394 Japan JN942788 JN939770 JN993522 –
ASIS19814 South Korea MG519531 MG519575 MG551606 MG551642
SFC2012091940* South Korea MG519525 – MG551600 –
L. prava HKAS106742* China MN585660 – – –
HKAS106745 China MN585661 – – –
L. proxima F1081079 Argentina KU685633 KU685777 KU685928 –
GMM7584 Russia KU685717 KU685858 KU685999 KU686120
L. pseudoalba MFLU 22-0106* Thailand ON557377 ON556492 ON598886 –
HKAS 110664 Thailand ON557376 ON556491 ON598887 ON598894
L. pseudomontana pse1625* America DQ149871 – – –
L. pumila pum1252 America DQ149864 – – –
L. roseoalbescens LM5099* Mexico KJ874328 KJ874331 – –
L. rubroalba MS15 China KX449358 – – –
MS20 China KX449357 – – –
L. rufobrunnea GDGM82878* China OR689443 OR785482 OR835197 OR826272
GDGM89627 China OR689444 OR785483
L. salmonicolor GMM7596* China JX504143 JX504218 KU686045 KU686151
GMM7602 China JX504145 – – –
L. squarrosa DM63* Mexico MF669958 MF669965 – –
SYC109 Panama KP877340 – – –
L. subroseoalbescens MFLU23-0339* Thailand PP785397 PP789598 – –
MFLU23-0340 Thailand PP785398 PP789599 – –
L. tetraspora F1080957 Germany KU685631 KU685775 – –
L. torosa SFC2015090217* South Korea MG519561 MG519598 MG551631 MG551664
KA12-1306 South Korea MG519562 – – –
L. tortilis ASIS22273* South Korea MG519533 MG519576 MG551608 MG551644
GMM7635 France JX504155 KU685906 KU686053 KU686156
L. trichodermophora F1111951 Costa Rica KU685640 KU685784 KU686063 –
GMM7733 America JX504157 – KU686013 –
L. trullisata PRL7587 China JX504170 JX504247 KU686047 KU686153
L. umbilicata GDGM82883 China OR689445 OR785485 OR835194 OR826270
GDGM82911* China OR689446 OR785486 OR835192 OR826268
MFLU 22-0105 Thailand ON557372 ON556490 ON598888 ON598896
HKAS 110652 Thailand ON557371 ON556489 – ON598895
L. versiforma KNU2012100803 South Korea MG519560 MG519597 MG551630 MG551663
SFC20120926-01* South Korea MG519556 MG519594 MG551627 MG551660
L. vinaceoavellanea A2986 Japan JN942810 JN939738 JN993520 –
A0559 Japan JN942803 JN939756 JN993512 –
SFC20150810-10 South Korea MG519539 MG519580 MG551614 MG551646
L. violaceonigra GMM7520 New Zealand KU685707 KU685848 KU685990 –
L. violaceotincta CAL1389* India MK141034 – – –
L. yunnanensis KUNF78558* China NR154115 – – –
MFLU 22-0107 Thailand ON557374 ON556488 – ON598892
HKAS 110636 Thailand ON557373 ON556487 ON598889 ON598891
HKAS 110638 Thailand ON557375 ON556486 ON598890 –
Mythicomyces corneipes ES11.10.2.A Germany KC964108 – – –
AFTOLID972 Germany DQ404393 AY745707 DQ408110 DQ029197

Maximum likelihood (ML) analysis was performed separately for each locus and the concatenated dataset using RAxML-HPC2 v. 8.2.12 (Stamatakis 2014) as implemented on the CIPRES portal (Miller et al. 2010), with the GTR+G model for both genes and 1,000 rapid bootstrap (BS) replicates. For Bayesian Inference (BI), the best substitution model for each character set was determined with MrModeltest 2.2 (Nylander 2004) on CIPRES, using the Akaike information criterion. Bayesian analysis was performed using MrBayes ver. 3.2.7a (Ronquist et al. 2011) as implemented on CIPRES (Miller et al. 2010).

Results

Phylogenetic analyses

Thirty-three new sequences (11 of ITS, 11 of LSU, 5 of rpb2, and 6 of tef1) were generated for Laccaria species and deposited in GenBank (Table 2). The ITS dataset included 103 specimens representing 55 species, while the ITS-LSU-rpb2-tef1 dataset included 71 specimens representing 42 species. Two phylogenetic analyses were conducted: one for the 5.8S, ITS1+ITS2 dataset, and the other with concatenated matrix of 5.8S+LSU, ITS1+ITS2, rpb2 codon, rpb2 introns+tef1 introns and tef1 codons (Vaidya et al. 2011). The ITS final aligned matrix contained 687 positions (170 for 5.8S, 517 for ITS1+ITS2), while the concatenated matrix contained 3,509 positions (1,054 for 5.8S+LSU, 430 for ITS1+ITS2, 1,026 for rpb2 exons, 163 for tef1 introns+rpb2 introns, 836 for tef1 exons). Based on previous phylogenies (Wilson et al. 2013, 2017; Popa et al. 2014, 2016; Luo et al. 2016; Cho et al. 2018; Li 2020; Cui et al. 2021; Zhang et al. 2023), species of the Mythicomyces corneipes (Fr.) Redhead & A.H. Sm. were selected as the outgroup. In the 5.8S-ITS1-ITS2 dataset, the following models were selected by mrModelTest: SYM for 5.8S and GTR+I+G for ITS1+ITS2. In the ITS, LSU, rpb2, and tef1 datasets, the models selected by mrModelTest were: GTR+I+G for 5.8S+LSU and tef1 codon, GTR+G for ITS1+ITS2 and rpb2 codon, GTR+G for rpb2 introns+tef1 introns.

In MrBayes analysis, two runs of five chains each were run for 2,000,000 generations and sampled every 200 generations. Convergence was further evaluated by checking that the potential scale reduction factor (PSRF) statistic was close to 1 for all parameters. Moreover, the effective sample size (ESS) was much higher than 200 for all parameters. A clade was considered to be supported if showing a bootstrap support value (BS) ≥75% and/or a posterior probability (PP) ≥0.90. Trees were edited in FigTree version 1.4.0 and PowerPoint.

Fig. 2 presents the phylogeny from the combined datasets. Nine specimens collected in northern Thailand formed three monophyletic clades, here described as L. pseudoalba, L. subroseoalbescens, L. umbilicata, and L. yunnanensis, respectively. Each clade was well supported by both ML and BI in the concatenated trees (Fig. 2). In our phylogenetic analysis, the four species clustered as separate clades with high support. Thus, these species are formally described in this paper.

Taxonomy

Laccaria pseudoalba S.M Tang & S.H. Li, sp. nov.

MycoBank No: 844144
Figs 3, 4, 5, 12

Etymology

The epithet “pseudoalba” refers to its similarity to L. alba in their small basidiomata and orange-white to pale orange pileus.

Holotype

Thailand. Chiang Mai Province: Mae On district, Huay Keaw subdistrict, Pox village, 18°43'55.6"N, 99°17'50.1"E, elevation 789 m., 6 September 2020, S. M. Tang, 2020090608 (MFLU 22-0106).

Description

Basidiomata small. Pileus 9–15 mm in diam., convex to applanate, hemispherical, applanate to plano-concave, pale orange (5A2–3, 6A2–3), orange-white (5A2–3, 6A2–3), when dry moisture loss of moisture or with age becoming whitish, clearly striate on the surface; umbo when young, becoming papilla to abrupt papilla with age; margin inflexed, sometime reflexed; context thin, 1–2 mm, pale orange (5A2–3), unchanging. Lamellae distant, arcuate, adnate with decurrent tooth, orange white (5A2–3, 6A2–3) when young, become pale orange with age, 3–4 mm in height; lamella edge even or entire, sometime undate; lamellulae in 3–4 tiers. Stipe 28.0–41.1 × 1.8–2.7 mm, cylindrical, central, equal with an enlarged base and nearly subclavate, pale (7–8A6) to pastel red (7A4–5, 8A4–5), smooth, basal mycelium white (1A1); stipe context stuffed, pastel red. Odor and taste not observed.

Basidia 29–38 × 9–13 μm, (mean length = 32 ± 2.5, mean width = 11 ± 1.2), clavate, mostly 4-spored, rarely 2-spored, sterigmata 5–8 μm × 2–3 μm, (mean length = 6.0 ± 1.22, mean width = 2.4 ± 0.45). Basidiospores (excluding ornamentation) [150/3/2] (6.0–) 7.1–11.0 (–12.0) × (6.5–) 7.0–10.4 (–10.9) μm, (mean length = 8.9 ± 0.83, mean width = 8.4 ± 0.71), Q = 1.00–1.36, Qm = 1.08 ± 0.07, globose to subglobose, hyaline, echinulate, spines 2–3 μm long, ca. 1–2 μm wide at the base, crowded. Cheilocystidia 20–31 × 6–9 μm, (mean length = 25 ± 3.5, mean width = 7 ± 1.0), narrowly clavate, thin-walled, colorless and hyaline, abundant. Pleurocystidia 15–31 × 6–8 μm, (mean length = 21 ± 4.2, mean width = 7 ± 0.8), narrowly clavate to subclavate, flexuose or mucronate, thin-walled, hyaline, abundant. Lamellar trama 50–70 μm thick, regular, composed of slightly thick-walled, filamentous hyphae 2–8 μm wide. Lamellar edge more in number of sterile basidia. Subhymenium 7–10 μm thick, tightly interwoven, fusiform or irregular cells, 5–8 × 3–4 μm, (mean length = 7 ± 0.8, mean width = 3.6 ± 0.5). Pileipellis 70–100 μm thick, orange hyaline in KOH, composed of appressed, parallel, simply septate, thin-walled, cylindrical, filamentous hyphae 4–6 μm wide, colorless and hyaline. Stipitipellis composed of appressed, parallel, simply septate, thick-walled, hyphae 3–7 μm wide; stipe trama composed of longitudinally arranged, pastel red in KOH, clavate terminal cells, infrequently branching, septate, thick-walled, hyphae hyaline 3–10 μm wide. Caulocystidia not seen. Clamp present at some septa in pileipellis, lamellae and stipitipellis.

Habitat and phenology

Scattered, gregarious, or caespitose on the ground in the Fagus and Dipterocarpus.

Additional specimens examined

Thailand. Chiang Mai Province: Mae On District, Huay Keaw Sub-district, elevation 799 m. 6 September 2020, S. M. Tang, HKAS110664; ibid., 6 September 2020, S. M. Tang, HKAS110663.

Notes

In our single gene (Fig. 1) phylogenetic analysis, the phylogenetic position of L. fengkaiensis, L. prava, L. vinaceoavellanea, L. violaceotincta, L. umbilicata and L. yunnanensis, within L. pseudoalba is well supported (100/1.00) as monophyletic clades. However, L. yunnanensis has bigger basidiomata (pileus 60–100 mm wide), brownish to flesh-colored pileus, and relatively bigger basidia (45–50 × 9–10 μm) (Popa et al. 2014). Laccaria vinaceoavellanea has vinaceous-buff pileus, and rare pileocystidia (Li 2020). Laccaria violaceotincta has dark brown to reddish brown pileus and pleurocystidia absent (Latha and Raj 2019). Laccaria fengkaiensis has relatively larger basidiomata (pileus 50–90 mm), more obvious striate, stipitipellis hyphal ends are either ascending or aggregating into scattered clusters, smaller basidiospores (5.2–6.3 × 5.1–6.3 μm) and narrower basidia (30–45 × 6–8.5 μm) (Li 2020). Laccaria prava has larger basidiomata (pileus 30–75 mm), presence of caulocystidia, and absence of pleurocystidia (Li 2020).

Figure 1. 

Maximum likelihood tree based on ITS1-5.8S-ITS2. Bootstrap support values ≥ 70%. The new sequences are highlighted in red, and the holotype of each species is in bold.

Figure 2. 

Maximum likelihood phylogeny using ITS1-5.8S-ITS2, LSU, rpb2, and tef1 sequence data to identify species of Laccaria growing on roots of Mythicomyces corneipes. ML bootstrap (≥70%) and posterior probabilities (≥0.90) are indicated above branches or in front of the branch leading to each node. The new species and a new record are highlighted in red; the holotype of each species is in bold.

Figure 3. 

Fresh basidiomata of Laccaria pseudoalba (a holotype, MFLU 22-0106 b, e HKAS 110664 c, d HKAS 110663). Scale bars: 5 mm. Photographs by Song-Ming Tang.

Figure 4. 

Laccaria pseudoalba a basidiospores b basidium and basidioles c basidia d cheilocystidia e pleurocystidia. Scale bars: 10 μm. Photographs by Song-Ming Tang.

Figure 5. 

Laccaria pseudoalba A stipitipellis B pileipellis. Scale bars: 10 μm. Photographs by Song-Ming Tang.

Laccaria pseudoalba can be confused with Laccaria alba Zhu L. Yang & Lan Wang due to their similar orange-white to whitish basidiomata. However, L. alba has white to whitish stipe while L. pseudoalba has pale to pastel red stipe, relatively thicker pileipellis (30–75 μm), absent pleurocystidia, narrower cheilocystidia (4–6 μm), and present clavate, hyaline caulocystidia (Wang et al. 2004).

Laccaria subroseoalbescens S.M. Tang & S.H. Li, sp. nov.

MycoBank No: 853964
Figs 6, 7, 8, 15

Etymology

The epithet “subroseoalbescens” refers to its similarity to L. roseoalbescens in their pale orange to greyish orange and clearly striate on the pileus surface.

Holotype

Thailand. Chiang Rai Province: Thasud, Muang District, Mae Fah Luang University Park, elevation 488 m, dominated by Dipterocarpus sp., 10 August 2020, OR1663 (MFLU23-0339).

Basidiomata small. Pileus 2–8 mm in diam., plano-concave to concave, glabrous, pale yellow (4A3), light yellow (4A4), pale orange (5A3) to greyish orange (5A4), light orange at center, becoming paler towards the margin, without umbo, when loss of moisture or with age becoming whitish, clearly striate on the surface; context thin, below 1 mm, pale orange (5A2–3), unchanging. Lamellae distant, arcuate, adnate with decurrent tooth, pale pink (6–7A2), 1–2 mm in height; lamella edge even or entire, sometime undate; lamellulae in 2–3 tiers. Lamellae pale pink (6–7A2) to bright flesh-pink, 1.2 mm diam., subdecurrent or decurrent, thick, regular, close. Stipe 5.0–13.0 × 0.8–1.7 mm, cylindrical, central or eccentric, equal with an enlarged base and nearly subclavate, pale pink (7A2) to light orange (6A5), concolorous with pileus, becoming whitish after loss of moisture or with age, smooth; stipe context stuffed, pale orange. Odor and taste not observed.

Figure 6. 

Fresh basidiomata of Laccaria subroseoalbescens (holotype a, c OR 1663, MFLU23-0339 b, d OR 1664, MFLU23-0340). Scale bars: 1 cm.

Basidia 30–46 × 8–14 μm, av. 38 ± 4.1 × 13.8 ± 1.3 μm, clavate, mostly 4–spored, rarely 2–spored; sterigmata 6–14 μm × 2–4 μm, av. 8.5 ± 2.9 × 3.3 ± 0.8 μm. Basidiospores [78/2/2] 7.0–8.9 × 6.8–9.0 μm, av. 8.3 ± 0.6 × 7.8 ± 0.6 μm, Qm = 1–1.3, Qav. = 1.1 ± 0.08, globose, hyaline; echinulate spines 2–3 × 1–2 μm, crowded. Cheilocystidia 23–37 × 4–8 μm, av. 34 ± 8.5 × 6.5 ± 1.5 μm, narrowly clavate, thin-walled, colorless and hyaline, abundant. Pleurocystidia 36–59 × 5–8 μm, av. 48 ± 7.6 × 6.5 ± 1.3 μm, subclavate, narrowly clavate, flexuose or mucronate, thin-walled, hyaline hyphae. Lamellar edge more in number of sterile basidia, composed of clavate, cylindrical inflated cells 11–23 × 8–15 μm, thin-walled, colorless, similar to basidioles in shape. Subhymenium 10–24 μm thick, tightly interwoven, fusiform or irregular cells, 4–7 × 5–6 μm. Lamellar trama 74–90 μm thick, regular, composed of slightly thick-walled, filamentous hyphae 2–5 μm wide. Pileipellis 60–90 μm thick, colorless hyaline in KOH, composed of appressed, parallel, simply septate, thin-walled, cylindrical, filamentous hyphae 7–11 μm wide, colorless and hyaline. Stipitipellis composed of appressed, parallel, simply septate, thick-walled, hyphae 3–5 μm wide; stipe trama composed of longitudinally arranged, pastel red in KOH, clavate terminal cells, infrequently branching, septate. Caulocystidia abundant, flexuose, thin-walled, hyaline hyphae, 4–5 μm wide. Clamp present at some septa in pileipellis, lamellae and stipitipellis.

Figure 7. 

Laccaria subroseoalbescens (OR1663, MFLU23-0339) a basidia b cheilocystidia c pleurocystidia d basidiospores. Scale bars: 10 μm.

Habitat and phenology

Scattered on the ground in subtropical forests of Dipterocarpus.

Figure 8. 

Laccaria subroseoalbescens (OR1663, MFLU23-0339) A pileipellis B stipitipellis. Scale bars: 10 μm. Photographs by Song-Ming Tang.

Additional specimens examined

Thailand. Chiang Rai Province: Thasud, Muang District, Mae Fah Luang University, 10 August 2020, elev. 489 m, OR1664 (MFLU23-0340).

Notes

In single gene (Fig. 1) phylogenetic analysis, L. subroseoalbescens is closely related to L. pseudoalba. However, L. pseudoalba has a pale orange to orange white pileus, and larger basidiospores 7.1–11.0 × 7.0–10.4 μm, shorter basidia sterigmata (5–8 μm × 2–3 μm).

Laccaria acanthospora A.W. Wilson & G.M. Muell., L. ambigua K. Hosaka, A.W. Wilson & G.M. Mueller, and L. negrimarginata A.W. Wilson & G.M. Mueller have similar small basidiomata (pileus ≤ 15 mm) as L. subroseoalbescens. However, L. acanthospora has orange pileus, relatively longer spines (2–6 μm) on the basidiospores, and longer basidia (40–56 × 10–14 μm) (Wilson et al. 2013). Laccaria ambigua has orange-brown basidiomata, without the striates on the pileus margin, and stipe orange-brown to ochraceous buff (Wilson et al. 2017). Laccaria negrimarginata has dark blackish brown to dark brown pileus and stipe, fibrillose to appressed squamulose on the pileus surface (Wilson et al. 2013).

Laccaria indohimalayana K. Das, I. Bera & Vizzini and L. roseoalbescens T.J. Baroni, Montoya & Bandala are similar to L. subroseoalbescens in their sharing a light yellow basidiomata. However, L. indohimalayana doesn’t have cheilocystidia and pleurocystidia, and is clearly separated in the phylogeny (Wang et al. 2019). Laccaria roseoalbescens has larger pileus (7–29 mm), and shorter echinae (1–2.5 μm) (Montoya et al. 2015).

Laccaria umbilicata Ming Zhang, in Zhang, Gao, Mu & Deng, Journal of Fungi 9(12, no. 1179): 16 (2023)

Figs 9, 10, 11, 15

Description

Basidiomata small. Pileus 7–11 mm in diam., applanate to plano-concave, depressed to subumbilicate shape of center, light yellow (1B4), when loss of moisture or with age becoming whitish, clearly striate towards the margin on the surface, without umbo; margin straight, eroded of margin; context thin, 0.5–1 mm, light yellow (1B4). Lamellae reddish brown (8E5–8), 3–5 mm wide; lamellulae subdecurrent to decurrent, thick, regular, distant, 3–4 mm in height; lamella edge even or entire, sometime undate, lamellulae in 3–4 tiers. Stipe 11.0–18.0 × 1.4–2.0 mm, cylindrical, fistulose, central or eccentric, equal with an enlarged base and nearly subclavate, white (1A1), sometime pale orange, basal mycelium white (1A1); stipe context fistulose, white, sometime pale orange. Odor and taste not observed.

Figure 9. 

Fresh basidiomata of Laccaria umbilicata (a–d MFLU 22-0105, e, f HKAS 110652, g HKAS 110651). Scale bars: 5 mm. Photographs by Song-Ming Tang.

Basidia 30–49 × 9–15 μm, (mean length = 39 ± 6.3, mean width = 12 ± 1.9), clavate, hyaline, 4-spored; sterigmata 5–8 × 2–3 μm (mean length = 6 ± 0.7, mean width = 2.5 ± 0.23). Basidiospores (excluding ornamentation) [150/3/2] (6.4–) 7.9–11.0 (–12.0) × (5.7–) 7.4–9.6 (–10.8) μm, (mean length = 9.4 ± 0.76, mean width = 8.9 ± 0.73), Q = 1.00–1.34, Qm = 1.07 ± 0.06, globose to subglobose, hyaline, echinulate; spines 0.2–0.5 μm long, ca. 0.5–0.8 μm wide at the base, crowded. Cheilocystidia 15–20 × 3–5 μm, (mean length = 17 ± 1.7, mean width = 4 ± 0.8), subclavate, narrowly clavate, hyphae-like, flexuose or mucronate, thin-walled, hyaline, abundant. Pleurocystidia 17–25 × 4–6 μm, (mean length = 20 ± 2.6, mean width = 5 ± 0.7), subclavate, narrowly clavate, hyphae-like, flexuose or mucronate, thin-walled, hyaline, abundant. Lamellar trama regular, 50–70 μm wide, composed of slightly thick-walled, filamentous hyphae 2–8 μm wide. Subhymenium 7–11 μm thick, tightly interwoven, fusiform or irregular cells, 5–10 × 2–3 μm, (mean length = 8 ± 1.2, mean width = 2.3 ± 0.3). Lamellar edge heteromorphous, more in number of cheilocystidia. Pileipellis 60–100 μm thick, composed of interwoven radiating, thin-walled, cylindrical, filamentous hyphae 3–8 μm wide. Stipitipellis composed of appressed, parallel, simply septate, thick-walled, hyphae 2–8 μm wide; stipe trama composed of longitudinally arranged, pale orange in KOH, clavate terminal cells, infrequently branching, septate, thick-walled, hyphae 8–20 μm wide. Caulocystidia not seen. Clamp present at some septa in pileipellis, lamellae and stipitipellis.

Figure 10. 

Laccaria umbilicata (MFLU 22-0105) a basidiospores b–c basidia d cheilocystidia e pleurocystidia. Scale bars: 10 μm. Photographs by Song-Ming Tang.

Habitat and phenology

Gregarious or caespitose on the ground associated with the Fagus and Dipterocarpus.

Figure 11. 

Laccaria umbilicata A pileipellis B stipitipellis. Scale bars: 10 μm. Photographs by Song-Ming Tang.

Additional specimens examined

Thailand, Chiang Mai Province: Mae On District, Huay Keaw, Pox Village, elevation 795 m., 6 September 2020, S. M. Tang, HKAS110652; ibid., 6 September 2020, S. M. Tang, HKAS110651. Chiang Mai Province, Mae On District, Huay Keaw, elevation 812 m, 6 September 2020, S. M. Tang, 2020090626 (MFLU 22-0105)

Notes

Following BLASTn searches of NCBI GenBank, the closest matches of the ITS and LSU sequences of our new collection (HKAS110652) is L. umbilicata (specimen GDGM82911 (holotype) ITS 99.67% shared identity; specimen GDGM82883 LUS 99.54% shared identity). The morphology of Thai collections was fit to the original description of L. umbilicata from Southwest China (Yunnan) by Zhang et al. (2023), including small basidiomata (10–28 mm), pale yellow, pale orange to light orange pileus, and clavate to ellipsoid pleurocystidia. Phylogenetically, our specimens grouped with L. umbilicata GDGM82911 (holotype) have high support values (Fig. 1, 100). Thus, we identified this specimen as a new record from Thailand.

Laccaria yunnanensis F. Popa, Rexer, G. Kost, Mycol. Progress 13(4): 1113 (2014)

Figs 12, 13, 14, 15

Description

Basidiomata large. Pileus 50–110 mm in diam., plano-concave, concave to hemisphaericus, glabrous, without umbo, yellowish-brown (5D4–5D8), brown (6E5–6E8), dark brown (7–8F5–8), yellowish brown when young, becoming dark brown with age, clearly striate on the surface; margin inflexed, sometimes reflexed; context thin, 2–3 mm, yellowish brown (5D4). Lamellae adnate, distant, yellowish-brown (5D4–5D8), brown (6E5–6E8), dark brown (7–8F5–8), 5–8 mm in height; lamella edge even or entire, sometime undate; lamellulae subdecurrent or decurrent, thick, regular, close; lamellulae in 2–3 tiers. Stipe 24.2–77.8 × 2.1–5.6 mm, cylindrical, central or eccentric, equal, smooth, same color as the pileus, yellowish-brown (5D4–8), brown (6E5–8), dark brown (7F5–8, 8F5–8), to whitish at the base, basal mycelium white (1A1); stipe context stuffed, yellowish brown. Odor and taste not observed.

Figure 12. 

Laccaria yunnanensis a–d basidiomata (a, b HKAS 110638 c HKAS 110631 d HKAS 110630). Scale bars: 1 cm. Photographs by Song-Ming Tang.

Basidia 41–53 × 7–15 μm, (mean length = 45 ± 8.3, mean width = 10 ± 2.3), clavate, mostly 4–spored, rarely 2–spored, sterigmata 6–9 μm, 2–3 μm wide at base. Basidiospores (excluding ornamentation) [250/5/2] 7.9–10.9 × 8.0–10.9 μm, (mean length = 9.5 ± 0.81, mean width = 9.4 ± 0.73), Q = 1.00–1.21, Qm = 1.12, globose, hyaline, echinulate, spines 1–2 μm long, ca. 0.5–1.0 μm wide at the base, crowded. Pleurocystidia 50–70 × 10–25 μm, (mean length = 59 ± 5.4, mean width = 18 ± 2.4), clavate to ellipsoid, thin-walled, hyaline hyphae. Cheilocystidia abundant, 25–50 × 4–8 μm, (mean length = 38 ± 3.5, mean width = 6 ± 0.8), subclavate, narrowly clavate to cylindrical, flexuose or mucronate, thin-walled, hyaline hyphae. Lamellar trama 60–100 mm thick regular, composed of slightly thick-walled, filamentous hyphae 2–12 μm wide. Lamellar edge more in number of cheilocystidia. Subhymenium 7–10 μm thick, tightly interwoven, fusiform or irregular cells, 2–4 × 4–5 μm, (mean length = 3 ± 0.2, mean width = 4.3 ± 0.3). Pileipellis 40–80 μm thick, yellowish brown in KOH, composed of radiating interwoven, thin-walled, cylindrical, filamentous hyphae 3–5 μm wide. Stipitipellis composed of appressed, parallel, simply septate, thick-walled, hyphae 5–20 μm wide; stipe trama composed of longitudinally arranged, pale yellowish in KOH, clavate terminal cells, infrequently branching, septate, thick-walled, hyphae 6–18 μm wide. Caulocystidia not seen. Clamp present at some septa in pileipellis, lamellae and stipitipellis.

Figure 13. 

Laccaria yunnanensis A pileipellis B stipitipellis. Scale bars: 20 μm. Photographs by Song-Ming Tang.

Habitat and phenology

Scattered, gregarious, or caespitose on the ground in Dipterocarpus and Fagus.

Material examined

Thailand. Chiang Mai Province: Mare Taeng District, Pha Deng Village, 14 July 2020, S. M. Tang, HKAS 110638; ibid., 14 July 2020 S. M. Tang, HKAS 110636; ibid., 11 August 2020 S. M. Tang, MFLU 22-0107; ibid., 10 September 2020 F. M. Yu, HKAS 110630.

Figure 14. 

Laccaria yunnanensis a basidiospores b basidia c cheilocystidia d pleurocystidia. Scale bars: 10 μm. Photographs by Song-Ming Tang.

Notes

The morphology of Thai collections fit the original description of L. yunnanensis from Southwest China (Yunnan) by Popa et al. (2014) including large basidiomata (pileus 50–110 mm in diam.), yellowish brown, brown, dark brown, yellowish brown or dark brown pileus, basidia clavate, and clavate to ellipsoid pleurocystidia. Our molecular analysis also indicated that four Thai collections belong to the same species.

Figure 15. 

Characteristics of basidiospores ornamentations a, b Laccaria pseudoalba c, d Laccaria subroseoalbescens e–g Laccaria umbilicata h–i Laccaria yunnanensis. Scale bars: 2 μm. Photographs by Song-Ming Tang.

Discussion

With the development of molecular phylogenetic analysis, many new Laccaria species have been rapidly described (Wilson et al. 2013, 2017; Popa et al. 2014, 2016; Luo et al. 2016; Cho et al. 2018; Li 2020; Cui et al. 2021; Zhang et al. 2023). Morphological characteristics and systematically informative traits are few in Laccaria; hence, molecular analyses are important for classification and species identification. In this study, we used the molecular phylogenetic analysis (single gene ITS1+ITS2 and 5.8 S Fig. 1), and multi-locus phylogenetic analysis (ITS, LSU, RPB2 and TEF1 sequences Fig. 2) to evaluate the taxonomy of Laccaria in Thailand. We identified 2 new species, namely L. pseudoalba, L. subroseoalbescens, and two new records, L. umbilicata and L. yunnanensis.

Before this study, five Laccaria species, namely L. amethystina Cooke, L. laccata, L. ohiensis (Mont.) Singer, L. proxima (Boud.) Pat., and L. vinaceoavellanea Hongo were reported to occur in Thailand based on morphological characteristics, but the specimens lacked detailed descriptions (Chandrasrikul et al. 2011). In the future, more extensive specimen collection is needed in Thailand to determine whether these species are indeed distributed there.

So far, only Fagus and Dipterocarpus have been found to host L. pseudoalba, L. umbilicata and L. subroseoalbescens. Species in Laccaria are similar in morphology characters, so habitat and host trees can provide important information for species identification. It is clear that several Laccaria species have a wide range of host trees while other species of Laccaria associate with a limited group or single host (Mueller 1992). For example, L. laccata (Scop.) Cooke (hosts: Castanea, Quercus, Pinus) and L. himalayensis A.W. Wilson & G.M. Muell. (hosts: Abies, Pinus, Picea) have been reported with a variety of hosts in forests; whereas L. trichodermophora G.M. Muell. (host: Quercus) and L. masoniae G. Stev. (host: Nothofagus) have only been found with a single host tree species (Mueller 1984) .

To date, 42 species of Laccaria have been reported in Asia (Wilson et al. 2013, 2017; Popa et al. 2014, 2016; Luo et al. 2016; Cho et al. 2018; Li 2020; Zhang et al. 2023). These species are described in China (26 species), South Korea (12 species), Japan (seven species), India (seven species), and Thailand (four species, this study). The taxonomy of Laccaria species in Thailand is still poorly understood and unclear. As a result of their very similar morphological characteristics, many Laccaria species are misidentified as the same species. Thus, for a better understanding of the species diversity of Laccaria in Thailand and their relationships within the genus, additional studies and data are required.

Acknowledgement

We thank Dr. Olivier Raspé for his comments on the phylogenetic analysis and for providing specimens.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This study was financially supported by the earmarked fund for CARS (Project ID: CARS-20) and the National Natural Science Foundation of China (Project ID: 32060006).

Author contributions

Investigation: XYZ, JH. Software: FMY. Supervision: SHL. Writing - original draft: SMT. Writing - review and editing: ZLL, SV, BR.

Author ORCIDs

Song-Ming Tang https://orcid.org/0000-0002-6174-7314

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

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

Zong-Long Luo https://orcid.org/0000-0001-7307-4885

Feng-Ming Yu https://orcid.org/0000-0001-9133-8645

Jun He https://orcid.org/0000-0001-7027-7206

Data availability

All of the data that support the findings of this study are available in the main text.

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