A new species of the genus Truncocolumella (Basidiomycota, Boletales) found in the Hengduan Mountains of China

Lin Li; Shanping Wan; Yun Wang; Naritsada Thongklang; Zonglong Luo; Shuhong Li

doi:10.3897/BDJ.12.e128970

Biodiversity Data Journal : Taxonomy & Inventories

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Taxonomy & Inventories

A new species of the genus Truncocolumella (Basidiomycota, Boletales) found in the Hengduan Mountains of China

Lin Li^‡,§,|, Shanping Wan^¶, Yun Wang^#, Naritsada Thongklang^§,|, Zonglong Luo^‡, Shuhong Li^¤

‡ College of Agriculture and Biological Science, Dali University, Dali, China

§ School of Science, Mae Fah Luang University, Chiang Rai, Thailand

| Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai, Thailand

¶ College of Resources and Environment, Yunnan Agricultural University, Kunming, China

# New Zealand Institute for Crop and Food Research Limited, Mosgiel, New Zealand

¤ Biotechnology and Germplasm Resources Institute, Yunnan Academy of Agricultural Sciences, Kunming, China

Corresponding author: Shuhong Li (shuhongfungi@126.com)

Academic editor: Alfredo Vizzini

Received: 04 Jun 2024 | Accepted: 06 Nov 2024 | Published: 21 Nov 2024

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: Li L, Wan S, Wang Y, Thongklang N, Luo Z, Li S (2024) A new species of the genus Truncocolumella (Basidiomycota, Boletales) found in the Hengduan Mountains of China. Biodiversity Data Journal 12: e128970. https://doi.org/10.3897/BDJ.12.e128970

Abstract

Background

During surveys of hypogeous fungi in the Hengduan Mountains, south-western China, three specimens of the genus Truncocolumella were discovered in Sichuan Province.

New information

Morphological and molecular analyses revealed that the collections represent a new species, Truncocolumella pseudocolumella. This article describes the new species and discusses its relationship with the other two members of the genus.

Keywords

false truffles, Hengduan Mountainous, ITS, morphological, taxonomy

Introduction

Truncocolumella Zeller (Agaricomycetes, Basidiomycota) is a small genus of false truffles, established by Zeller in 1939 with the type species T. citrina Zeller (Zeller 1939). The main characteristics of this genus are: basidiomata depressed-spheroid to reniform, from a rhizomorphic base and with a central point of attachment; columella stump-like to dendroid, prominent; peridium persistent, not separating from the gleba; gleba pale white when immature, brown when mature; spores smooth, ellipsoid, as seen individually, almost hyaline. Another species, Truncocolumella rubra, was named in the same article and later recombined as Gastroboletus ruber (Zeller) Cázares & Trappe (Cázares and Trappe 1991). The third species in this genus, T. occidentalis (Malençon) Malençon & Zeller, was reclassified from Dodgea occidentalis Malençon (Malençon and Zeller 1940). Subsequently, T. citrina var. citrina Zeller and T. citrina var. separabilis A.H. Sm. were synonymised with T. citrina (Smith and Singer 1959). To date, only T. citrina and T. occidentalis are recognised within the genus Truncocolumella.

Truncocolumella citrina is a common ectomycorrhizal species, frequently found in coniferous forests in North America (Zeller 1939, Smith and Singer 1959, Goodman et al. 1998, Wood et al. 1998, Massicotte et al. 2000, Binder and Hibbett 2007, Twieg et al. 2007, Sato and Toju 2019). Truncocolumella occidentalis, however, is rare and has only been found in Canada (Malençon and Zeller 1940). Until 2012, Truncocolumella species had not been reported outside of North America. That year, a specimen was discovered at Mt. Yala in western Sichuan Province, China. Two additional collections were later found in the same region. Western Sichuan Province, part of the Hengduan Mountains, is one of the world's most biodiverse areas. Morphological and molecular analyses revealed that these three samples represent a new species, T. pseudocolumella, described in this paper.

Materials and methods

Morphological description

The specimens were collected from the Hengduan Mountainous in China. The type and other studied specimens were deposited in the herbarium of Cryptogams of the Kunming Institute of Botany, Academia Sinica (KUN-HKAS).

Descriptions of microscopic and macroscopic characters were based on specimens (HKAS131259 [YAAS L2327], HKAS95533, and HKAS95534) following the methods of Kumar et al. (2017) and Truong et al. (2017). Sections were made with a razor-blade by hand, mounted in a 5% potassium hydroxide (KOH) solution or water and then stained with a cotton blue or lactophenol solution. Mounts were observed under an Olympus BH-2 microscope. Key colours were selected from Kornerup and Wanscher (1978).

DNA extraction, PCR amplification and sequencing

Total genomic DNA was extracted from the specimens using the OMEGA Plant Genomic DNA Kit. The internal transcribed spacer (ITS) rDNA region was amplified with PCR primers ITS1F and ITS4 (White et al. 1990, Gardes and Bruns 1993, Truong et al. 2017). The large subunit nuclear ribosomal DNA (LSU) region was amplified with the PCR primers LROR and LR5 (Vilgalys and Hester 1990). PCR reactions were performed on a BIO-RAD C1000TM instrument. Thermal cycles with the following settings: initial denaturation for 5 min at 94°C, followed by 32 cycles of 40 s denaturation at 94°C, annealing at 56°C for 40 s for ITS and 52°C for 30 s for LSU, extension for 1 min at 72°C and final extension at 72°C for 10 min. The PCR products were verified on 1% agarose electrophoresis gels stained with ethidium bromide. The purification and sequencing of the PCR products was conducted by Sangon Biotech Limited Company (Shanghai, China).

Molecular phylogenetic analyses

ITS was used for the analysis of the diversity of Truncocolumella species in this study because ITS appears to be a useful locus for the delimitation of Truncocolumella species. Thirty ITS sequences from NCBI and this study representing two species of Truncocolumella and selected accessions from the closely-related genera Chroogomphus, Gomphidius, Rhizopogon, Suillus (Table 1), including Gastroboletus vividus Trappe & Castellano, Gastroboletus subalpinus Trappe & Thiers and Gastroboletus ruber (Zeller) Cázares & Trappe as outgroup taxa were used. The sequences of the Truncocolumella species generated in this study were submitted to the GenBank database. We first used the Basic Local Alignment Search Tool for the GenBank database to recheck whether the newly-generated sequences were amplified from the contaminant or not and examined clusters with closely-related sequences. DNA sequences were retrieved and assembled using SeqMan. The ITS gene was analysed using BioEdit v. 7 (Hall 2007), sequence alignments were aligned using MAFFT version 7 (Katoh and Standley 2013) and Maximum Likelihood (ML) analysis was performed using RAxML-HPC2 v. 8.2.12 (Stamatakis 2014) as implemented on the CIPRES portal (Miller et al. 2011), with the GTR+G+I model and 1,000 rapid bootstrap (BS) replicates for all genes. A reciprocal 70% bootstrap support approach was used to check for conflicts between the tree topologies from the gene. As the topology of the ML tree and the Bayesian tree are similar, the ITS1, ITS2 and 5.8s sequences were combined using SequenceMatrix (Vaidya et al. 2011) partitioned phylogenetic analyses. For Bayesian Inference (BI), the best substitution model for each partition was determined by MrModelTest 2.2 (Nylander et al. 2004). The result suggested that ITS1: JC+I, 5.8S: GTR+G+I, ITS2: K80+I+G were the best models.. Bayesian analysis was performed using MrBayes ver. 3.2.7a (Ronquist et al. 2011) on the CIPRES Science Portal (Miller et al. 2011) and four parallel runs were performed for 10 million generations sampling every 100^th generation for the single gene trees. Parameter convergence > 200 was verified in Tracer v. 1.7 (Rambaut et al. 2018). The phylogenetic clade was strongly supported if the bootstrap support value (BS) was ≥ 70% and/or a posterior probability (PP) < 0.01.

Table 1.

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CSV

XLSX

Taxa information and GenBank accession numbers of the sequences used in this study. Newly-generated sequences are in bold.

Species name	Voucher	Origin	GenBank No.		Reference
Chroogomphus roseolus	HKAS 50552	China	EF423620	Li et al. (2009)
Chroogomphus ochraceus	OKM 25472	USA	AH009858	Miller et al. (2002)
Gastroboletus ruber	OSC 79741	USA	EU697272	GenBank
Gastroboletus ruber	OSC 69644	USA	EU837224	GenBank
Gastroboletus ruber	OSC 74672	USA	EU837223	GenBank
Gastroboletus subalpinus	Trappe607-holotype	USA	EU231989	Dentinger et al. (2010)
Gastroboletus vividus	JLF4456	USA	MH213058	GenBank
Gomphidius borealis	IB:NR19990532-holotype	USA	NR_132800	Miller et al. (2002)
Gomphidius nigricans	OKM 27830	USA	AY077474	Miller et al. (2002)
Rhizopogon colossus	MICH AHS49480-holotype	USA	AH011348	Grubisha et al. (2002)
Rhizopogon diabolicus	MICH AHS68424-paratype	USA	AH011349	Grubisha et al. (2002)
Rhizopogon ellenae	MICH AHS66137-holotype	USA	AH011350	Grubisha et al. (2002)
Rhizopogon evadens	MICH AHS65484-holotype	USA	AF062927	Grubisha et al. (2002)
Rhizopogon flavidus	YAAS L2957	China	NR_158904	Li et al. (2016)
Rhizopogon jiyaozi	YAAS L2929	China	NR_158906	Li et al. (2016)
Rhizopogon ochraceorubens	MICH AHS59643-holotype	USA	AF062928	Grubisha et al. (2002)
Rhizopogon sinoalbidus	YAAS L2949	China	NR_158905	Li et al. (2016)
Rhizopogon songmaodan	HKAS 106767	China	NR_174900	Wang et al. (2021)
Suillus americanus	C0075059F	USA	KU663184	Zhang et al. (2022)
Suillus flavidus	KM171907	Scotland	KU721177	Zhang et al. (2022)
Suillus granulatus	KM172141	Italy	KU721242	Zhang et al. (2022)
Truncocolumella citrina	JLF 2149	USA	MH217566	GenBank
Truncocolumella citrina	TDB-2001	USA	L54097	Kretzer et al. (1996)
*Truncocolumella pseudocolumella*	HKAS131259	China	KP090063	This study
*Truncocolumella pseudocolumella*	HKAS131259	China	KP090064	This study
*Truncocolumella pseudocolumella*	HKAS95533	China	OR631922	This study
*Truncocolumella pseudocolumella*	HKAS95534	China	OR631923	This study
Truncocolumella sp1.	OSC 67369	USA	KT968570	GenBank
Truncocolumella sp2.	MR3D88-RHITRU1	USA	OM459721	GenBank
Truncocolumella sp3.	OSC 111948	USA	KF206337	GenBank

Taxon treatment

Truncocolumella pseudocolumella L. Li, S.H. Li & Y. Wang, sp. nov.

MycoBank 851721

Materials Download as CSV

Holotype:

taxonID:
MB 851721
; scientificNameID:
Truncocolumella pseudocolumella
; continent:
Asia
; country:
China
; stateProvince:
Sichuan
; municipality:
Ganzi
; locality:
Yala Snow Mountain
; verbatimElevation:
3772.4 m
; verbatimLatitude:
30°31′N
; verbatimLongitude:
101°37′E
; year:
2012
; month:
August
; day:
19
; habitat:
in the forest of Quercus guyavifolia H. Lév.
; catalogNumber:
HKAS 131259
; recordNumber:
L2327
; recordedBy:
Shu-Hong Li
; associatedSequences:
KP090063, KP090064
; identificationID:
HKAS 131259
; identifiedBy:
Lin Li
; occurrenceID:
C1F523CC-76F3-573A-8065-139715C2CC02

Other materials:

scientificName:
Truncocolumella pseudocolumella
; higherGeography:
Hengduan Mountains area
; country:
China
; stateProvince:
Sichuan
; county:
Ganzi
; year:
2014
; month:
August
; day:
22
; habitat:
in the forest of Pinus
; catalogNumber:
HKAS 95533
; recordedBy:
Shan-Ping Wan
; associatedSequences:
GenBank: OR631922
; identificationID:
HKAS 95533
; identifiedBy:
Lin Li
; occurrenceID:
E10A3DB1-A334-5221-8BED-5D60FE32F4DA
scientificName:
Truncocolumella pseudocolumella
; higherGeography:
Hengduan Mountains area
; country:
China
; stateProvince:
Sichuan
; county:
Ganzi
; year:
2014
; month:
August
; day:
22
; habitat:
in the forest of Pinus
; catalogNumber:
HKAS 95534
; recordedBy:
Shan-Ping Wan
; associatedSequences:
GenBank: OR631923
; identificationID:
HKAS 95534
; identifiedBy:
Lin Li
; occurrenceID:
9ACD3595-0888-58BC-9057-6F0AECF08031

Description

Basidiomata irregularly depressed-globose to pyriform, with a yellowish-tawny (4C8) rhizomorphic base, 1.5–3.0 cm in diameter, the surface typically smooth and dry in appearance, light yellowish-tawny (4C5) with yellowish-brown (4C8) rhizomorphs, colour unchanged on bruising or exposure, elastic, very mature basidiomata deliquesce like Rhizopogon (Fig. 1A). Odour light and pleasant.

Figure 1.

Truncocolumella pseudocolumella. A Basidiomata; B, C Dry peridium turning black when stained with 5% KOH; D A section of basidiomata in 5% KOH; E A section of the hymenium in lactophenol cotton blue; G-I Basidia in 5% KOH (H. 4-spored basidia, I. 2-spored basidia); F, J Basidiospores in 5% KOH. Scale bars: A = 1 cm; B, C = 0.5 cm; D = 50 μm; E, G, H, I = 20 μm; F, J = 10 μm.

Peridium 102–160 μm thick, not separating or evanescent from the gleba at maturity, composed of two layers: outer layer 52–73 μm thick, reddish-tawny (7D7) interwoven hyphae of 1–1.5 μm diameter. The inner layer 40–86 µm thick, consisting of brownish-hyaline nearly parallel interwoven hyphae of 0.5–1.5 μm diameter (Fig. 1D). The boundary between the inner and outer layers gradually transitioning, with the changes in hyphae arrangement direction and hyphae colour. The clamp connection clearly visible, dry peridium becoming black (4F4) when encountering 5% KOH (Fig. 1B and C). Gleba pale white when immature, light brown to tawny at maturity, unchanging on bruising or exposure, cavities relatively small, spongy, lacking obvious columnar or dendroid radiating columella (Fig. 1A). Trama (56.0–) 62.5–85.0 μm, composed of hyaline almost parallel hyphae. Hymenium present on cavities surface. Basidia narrowly clavate, (15.0–) 17.2–19.5 (–22.4) × 3.5–6.5 (–7.0) μm, 2-4-spored. Sterigmata 2–3 μm (Fig. 1E, G, H and I). Basidiospore ellipsoid, smooth, 7.5–10.0 (–11.0) × 4.0–5.0 (–5.6) μm, grey to brownish (7D5) in mass, as seen individually, almost hyaline, typically 1–2 guttulate, infrequently 3-guttulate (Fig. 1F and J), changing to blue in lactophenol cotton blue, not obvious discolouration in Melzer's reagent.

Diagnosis

Differs from other species in the genus Truncocolumella in the basidiomata devoid of any columnar.

Etymology

Pseudocolumella, referring to the absence of the columella.

Distribution

China, Sichuan Province.

Ecology

Gregarious in the soil associated with Quercus guyavaefolia and Pinus sp.

Notes

Notes: The genus Truncocolumella currently includes three species: T. citrina, T. occidentalis and the newly described T. pseudocolumella in this study. Based on the original literature descriptions of the species T. citrina (Zeller 1939, Smith and Singer 1959) and the re-examination of the type specimens of T. citrina and T. occidentalis by Malençon and Zeller (Malençon and Zeller 1940), we compared the key distinguishing features of these three species. In terms of macroscopic characteristics, T. pseudocolumella differs from other species in the genus Truncocolumella in the basidiomata devoid of any columnar. Furthermore, the basidiomata of T. citrina have a diameter of 2–4 cm, which is comparable in size to those of T. pseudocolumella (1.5–3 cm), but they are two to three times larger than T. occidentalis. The basidiomata surfaces of T. citrina are distinctly citrine yellow, those of T. pseudocolumella are yellowish-tawny, while T. occidentalis has white basidiomata, although the colour of T. occidentalis remains uncertain due to preservation in alcohol. Microscopically, T. citrina has ellipsoid spores measuring 6–10 × 3.5–5.0 μm, with individual spores appearing nearly hyaline. Similarly, T. pseudocolumella has ellipsoid spores measuring 7.5–10.0 × 4.0–5.0 μm, also nearly hyaline, showing close resemblance between the two. According to Malençon's description (Malençon and Zeller 1940), the spores of T. citrina are clearly shorter, more oval and of more irregular shape than those of T. occidentalis, in which these bodies are long-elliptic or sometimes subcylindrical. Molecular analysis further demonstrates that T. pseudocolumella is distinct from T. citrin, with high support for their separation into different species.

Analysis

Phylogenetic analysis

The ML and Bayesian analyses of the 30 ITS sequences are shown in Fig. 2 with associated bootstrap supports for branches.

Figure 2.

Phylogeny derived from a Maximum Likelihood (ML) analysis of the nrDNA-ITS sequences from Suillineae, including Truncocolumella species, using Gastroboletus as outgroup. Values next to nodes present Maximum Likelihood bootstrap support values (BS), left and Bayesian posterior probabilities (PP), right. The names of novel species and samples with newly-generated sequences are in bold.

In the phylogenetic tree, the 25 ITS sequences from Suillineae revealed the phylogenetic relationship of two species of Truncocolumella and five Gastroboletus sequences are used as outgroups. Since there are few Truncocolumella sequences in GenBank and these sequences belong to only one species T. citrina, we selected sequences of Suillineae for phylogenetic analysis. The analytics include three sequences of the genus Suillus; nine sequences of the genus Rhizopogon; two sequences of the genus Chroogmophus; two sequences of the genus Gomphidus; and nine sequences of the genus Truncocolumella. Two clades were revealed in the genus Truncocolumella; Clade I includes five sequences of T. citrina from the USA; Clade II includes four sequences of a new species, T. pseudocolumella from China. The phylogenetic analysis shows that the new species is distinct from T. citrina, the type species of Truncocolumella. In addition to the ITS sequences used in this phylogenetic analysis, the LSU sequences were amplified from the newly-recorded specimens in this study and uploaded to NCBI for future study.

Discussion

Truncocolumella is an ancient, small genus with only two known species, T. citrina and T. occidentalis, which were found exclusively on the west Pacific coast of North America until the discovery of the third member, T. pseudocolumella, almost a century later in Sichuan, China. Truncocolumella is closely related to the epigeous fungi Suillus and both genera are currently classified within the family Suillaceae. The genus Truncocolumella is characterised by its prominent, stump-dendroid-like columella, a key morphological feature. However, the new species T. pseudocolumella has almost no columella, making it similar to species of Rhizopogon, although molecular analysis clearly places it within the genus Truncocolumella. In addition to the absence of columella in the basidiomata of T. pseudocolumella, which is a notable distinguishing feature, T. citrina and T. pseudocolumella also differ in several morphological characteristics: the basidiomata surface of T. citrina is distinctly citrine yellow (Zeller 1939, Smith and Singer 1959), while that of T. pseudocolumella is yellowish-tawny. The peridium of T. citrina is 70–100 μm thick, whereas that of T. pseudocolumella is thicker, reaching 102–160 μm and is differentiated into two layers based on the orientation of hyphae and changes in hyphal colouration. Additionally, the sterigmata of T. citrina are 3–5 μm in length, while those of T. pseudocolumella are shorter, measuring 1–2 μm in length. Similarly, based on the re-examination of the morphological structures of the type specimens of T. citrina and T. occidentalis by Malençon and Zeller (Malençon and Zeller 1940) and their descriptions, it is evident that T. pseudocolumella has larger basidiomata with a yellowish-tawny surface compared to T. occidentalis. Additionally, the spores of T. occidentalis are long-elliptic, sometimes almost subcylindrical and are longer than those of both T. citrina and T. pseudocolumella. Truncocolumella occidentalis was reclassified from Dodgea occidentalis and its description is based on a holotype specimen that was preserved in alcohol for 17 years. Since then, no additional reports of this species have been recorded. Unfortunately, molecular data are not available. It is hoped that future collections of this species will help clarify its identity.

Truncocolumella pseudocolumella differs significantly from the North American species, which can be attributed to bio-evolutionary geographical isolation and the unique ecological environment of the Hengduan Mountains in China. Truncocolumella citrina is found in coniferous forests of the Pacific Northwest mountains at altitudes around 1200 m (Zeller 1939, Smith and Singer 1959), whereas T. pseudocolumella is distributed in alpine Quercus guyavifolia and Pinus forests at 3700 m in the Hengduan Mountains region of China.

Acknowledgements

This study was financially supported by the National Natural Science Foundation of China (No. 31800009, 32060008) and the Yunnan Fundamental Research Project (grant No. 2017FD135, 202201AT070268). Thanks to the Fungal Diversity Conservation and Utilization Team in Northwest Yunnan for providing the research platform and to team members for their help.

Author contributions

Conceptualisation, Lin Li, Shan-Ping Wan and Yun Wang; methodology, Lin Li; formal analysis, Lin Li; investigation, Lin Li; resources, Shu-Hong Li and Yun Wang; data curation, Lin Li; writing—original draft preparation, Lin Li; writing—review and editing, Naritsada Thongklang, Zong-Long Luo and Shu-Hong Li; funding acquisition, Shu-Hong Li. All authors have read and agreed to the published version of the manuscript.

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Supplementary material

Endnotes