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Article

Updated Taxonomy of Chinese Craterellus (Hydnaceae, Cantharellales) with Three New Species Described

by
Tian Jiang
1,2,†,
Lei Zhao
3,†,
Xu Zhang
2,
Hua-Zhi Qin
1,
Hui Deng
1,
Xiao-Dong Mu
4,* and
Nian-Kai Zeng
1,2,*
1
School of Pharmacy, Hainan Medical University, Haikou 571199, China
2
Ministry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou 571158, China
3
Hainan Smart Rainforest Center, Haikou 570203, China
4
Hainan Research Academy of Environmental Sciences, Haikou 571126, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Life 2025, 15(2), 157; https://doi.org/10.3390/life15020157
Submission received: 25 December 2024 / Revised: 18 January 2025 / Accepted: 21 January 2025 / Published: 23 January 2025
(This article belongs to the Collection Biodiversity and Ecology of Fungi in Terrestrial and Marine Ecosystems)
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Abstract

:
Species of Craterellus are interesting and important due to their mycorrhizal properties, medicinal value, and edibility. Despite extensive research on Craterellus in China, its taxonomy remains inadequately understood. This study presents three newly described species of Craterellus, namely C. albimarginatus, C. involutus, and C. longitipes, identified through morphological and phylogenetic analyses, with the goal of refining the taxonomy of Chinese Craterellus.

1. Introduction

Craterellus Pers. (Hydnaceae, Cantharellales), with C. cornucopioides (L.) Pers. as the type species, is distinguished by its small, funnel-shaped basidioma and hollow stem [1]. It is widely distributed in the temperate regions of the northern hemisphere and is frequently found in the tropics [2]. Ecologically, Craterellus usually forms ectomycorrhizal relationships with various host plants including species from Dipterocarpaceae, Fagaceae, Malvaceae, Myrtaceae, Pinaceae, and Salicaceae, contributing significantly to the biodiversity of forest ecosystems [3,4]. Furthermore, species of Craterellus are edible and medicinal, and they contain chemical components with pharmacological effects such as immunomodulatory, anti-inflammatory, and anti-mutagenic properties [5,6,7,8,9].
The genus Craterellus exhibits high species diversity, with approximately 173 recognized species (source: http://www.indexfungorum.org, accessed 10 December 2024). However, taxonomic classification within the genus is complicated by subtle morphological differences among species [2]. To clarify the confusion in the taxonomy of Craterellus species, analyses of phylogeny and morphological characteristics were performed by mycologists [10,11,12,13,14,15,16,17]. Moreover, six well-supported subgenera, viz. Cariosi T. Cao & H. S. Yuan, Craterellus, Imperforati T. Cao & H. S. Yuan, Lamelles T. Cao & H. S. Yuan, Longibasidiosi T. Cao & H. S. Yuan, and Ovoidei T. Cao & H. S. Yuan, were revealed [10].
In China, species of Craterellus have also attracted the attention of mycologists, and eighteen taxa of the genus have been identified or described [6,8,9,10,11,12,13,14,15,16,17]. However, the diversity of the genus still remains incompletely understood. In one previous study, three new species of this genus from tropical–subtropical regions of China were described by our research team [16]. Recently, new collections of Craterellus were made and studied using both morphological and molecular phylogenetic analyses. A multilocus phylogeny for Craterellus was constructed based on a combined dataset of 28S, ITS, and TEF1, aiming to update the taxonomy of Craterellus in China.

2. Materials and Methods

2.1. Morphological Studies

Digital photographs and field notes were systematically recorded from fresh basidiomata in the field, documenting their sizes, colorations, any color changes, and the associated symbiotic plant species. Specimens were subjected to drying at 50–60 °C [18], subsequently stored in a refrigerator at minus 20 degrees for two weeks, and finally deposited in the Hainan Biodiversity Science and Technology Museum (FHMU), Hainan Province of China. Color codes were referenced from Wanscher and Kornerup [19]. Sections of the pileipellis were excised from the pileus between the central and marginal areas and subsequently mounted in a 5% potassium hydroxide (KOH) solution; 1% Congo Red staining was used as an adjunct for observation. The specimens were then examined and measured using a bright-field microscope (CX23, Olympus, Tokyo, Japan). The notation is indicated as “n” basidiospores measured from “m” basidiomata of “p” collections [n/m/p]. The basidiospore dimensions are given as (a–)b–e–c(–d), where “b–c” denotes at least 90% of the measured values (5th to 95th percentile), and extreme values (a and d) are shown in parentheses whenever they occur (a < 5th percentile, d > 95th percentile); “e” stands for the average length/width of the basidiospores. The length/width ratio of basidiospores is denoted by “Q”, and the average “Q” of these basidiospores, along with its standard deviation, is denoted by “Qm”. The words that describe a basidioma’s size are derived from Bas [20].

2.2. Molecular Procedures

To obtain materials for DNA extraction from the fresh basidiomata, a small piece of the pileus was excised, subsequently wrapped in paper, and finally placed in a sealed bag with silica gel. Total genomic DNA was extracted from 10 to 20 mg of dried basidiomata using the Magnetic Beads Genomic DNA Extraction Kit (Magen, Guangzhou, China), following the manufacturer’s protocol. After extraction, 2 µL of the DNA sample was aliquoted, and its concentration and purity were assessed using a NanoDrop 8000 spectrophotometer (Thermo Fisher Scientific, Waltham, MA, USA). To check DNA integrity, 2 µL of the DNA sample was mixed with 2 µL of bromophenol blue loading dye and loaded onto a 1% agarose gel in TAE buffer for electrophoresis. The gel was run at a constant voltage of 100 V for (20 min). Negative controls were included in each batch of DNA extractions to rule out contamination.
Large subunit ribosomal DNA (28S), the nuclear ribosomal internal transcribed spacer (ITS), and translation elongation factor 1-α (TEF1) gene fragments were amplified by PCR using the universal primer pairs ITS5/ITS4 [21], LR0R/LR5 [22,23], and tefF/tefR [24], respectively. PCR procedures were conducted according to the methods outlined by An et al. [25] and Zhang et al. [26]. The PCR reaction was performed in a 30 µL mixture containing 1 µL of DNA template (approximately 20 ng), 2 µL of each forward and reverse primer (5 pmol/µL), 15 µL of 2 × Taq PCR Master Mix, and 10 µL of ddH2O. The amplification program included an initial denaturation at 95 °C for 5 min, followed by 35 cycles of 95 °C for 30 s, 50 °C for 30 s (annealing), and 72 °C for 1 min (extension). PCR products were verified by electrophoresis on a 1% (w/v) agarose gel.
The PCR products were sequenced using an ABI 3730xL DNA Analyzer (Huayu Gene, Wuhan, China). Forward and reverse sequences were assembled using BioEdit v7.0.9 [27]. The successfully sequenced and assembled fragments were compared against the NCBI nt (nucleotide)/nr (non-redundant protein) databases using BLAST (Basic Local Alignment Search Tool) to identify closely related sequences. All newly acquired sequences were submitted to GenBank (Table 1).

2.3. Dataset Assembly

A total of 39 DNA sequences (15 from 28S, 11 from ITS, and 13 from TEF1) were newly generated from 24 collections in the present study (Table 1). These sequences were included in a concatenated dataset (28S, ITS, and TEF1) and cross-referenced with sequences from previous research and GenBank (Table 1). According to Zhang et al. [16], Hydnum minus Yanaga & N. Maek and H. cremeoalbum Liimat. & Niskanen were selected as the outgroup. A separate alignment of the sequences of 28S, ITS, and TEF1 regions was performed to check for phylogenetic disagreement. Phylogenetic tree diagrams, constructed using a single DNA sequence for each analysis, exhibited the same topologies, showing that there were no contradictions between the signals derived from the different gene segments. The alignment of the three datasets (28S, ITS, and TEF1) was performed using MUSCLE v3.6 [45], followed by concatenation using Phyutility v2.2 for subsequent analyses [46].

2.4. Phylogenetic Analyses

Methods of maximum likelihood (ML) and Bayesian inference (BI) were applied to analyze the integrated nuclear dataset. RAxML 7.2.6 was employed to construct the maximum likelihood tree and perform bootstrap (BS) analysis [47]. In the ML analysis, default parameter values were applied, except for the model, which was set to GTRGAMMA. Nonparametric bootstrapping with 1000 replicates was employed to derive statistical support. BI was carried out with the CIPRES Science Gateway portal using MrBayes v3.1 [48,49]. MrModeltest v2.3 was employed to identify the most appropriate models of nucleotide substitution for 28S (GTR + I + G), ITS (HKY + I + G), and TEF1 (SYM + G) according to the Akaike information criterion [50]. For the combined nuclear dataset (28S, ITS, and TEF1), Bayesian analysis was run for 30 million generations, with an average deviation of split frequencies of 0.004598. The initial 25 percent of sampled generations were discarded to account for burn-in, and the Bayesian posterior probabilities (PP) were estimated for the majority consensus tree based on the retained Bayesian trees.

3. Results

3.1. Molecular Data

The dataset, combining 28S, ITS, and TEF1, included 109 sequences with 2644 nucleotide positions, with the alignment available in TreeBASE (31766) [https://treebase.org/treebase-web/home.html (accessed on 22 October 2024)]. The Bayesian analyses produced topologies identical to those of the ML analysis, with slight differences in statistical support (Figure 1). Based on the molecular data, sixteen independent lineages were identified within the Chinese species of Craterellus (Figure 1). Three new lineages were discovered in the current study (Lineages 6, 8, and 14). Lineage 6, with strong statistical support (BS = 100%, PP = 1.0), comprised three new collections (FHMU7705, FHMU7706, and FHMU7707) from southeastern China; in lineage 8, two collections (FHMU7708 and FHMU7709) also from southeastern China grouped together with 100% RAxML likelihood bootstrap and 0.8 posterior probability; in lineage 14, two collections (FHMU7715 and FHMU7716) from southern China were clustered together with high statistical support (BS = 98%, PP = 1.0).

3.2. Taxonomy

Craterellus albimarginatus N.K. Zeng, T. Jiang & Xu Zhang, sp. nov.
MycoBank: MB 856885
Figure 2a,b and Figure 3.
Etymology—Latin “albi-”, meaning white, and “marginatus”, meaning margin, refer to the white margin of the new species.
Holotype—CHINA. Hainan Province: Wuzhishan, Hainan Tropical Rainforest National Park, elev. 600 m, 9 June 2022, X. Zhang039 (FHMU7715). GenBank accession number: 28S = PQ604676, ITS = PQ611003.
Diagnosis—Craterellus albimarginatus is distinguished from the closest species of Craterellus by its very small basidioma, the distinct boundary between the pileus and stipe, a grayish-brown pileus with a pure white margin, a white hymenophore tinged with violet, smaller basidiospores, and its association with Fagaceae trees.
Description—Pileus 0.7–2.2 cm diameter, center strongly depressed, margin broadly wavy or unevenly folded; surface dry and slightly rough, grayish-brown (5D6), but margin pure white (1A1); context very thin, grayish white. Hymenophore slightly veined, spreading down; folds approximately 0.05 cm broad, white (1A1) tinged with violet (15A2). Stipe 0.7–1.5 × 0.1–0.4 cm, central, hollow, subcylindrical; surface dry, beige-almond (2B2); basal mycelium white (1A1). Odor indistinct. Spore print not obtained.
Basidiospores [40/2/2] 7–7.9–9(–9.5) × 5–5.6–6.5 µm, Q = (1.23–)1.27–1.60(–1.80), Qm = 1.41 ± 0.11, ellipsoid, rarely subglobose, smooth, inamyloid, marginally thickened walls (up to 0.5 µm), yellowish in KOH. Basidia 46–65 × 5–7 µm, 3–5-spored, subcylindrical, somewhat curving, marginally thickened walls (up to 0.5 µm), yellowish in KOH; sterigmata measuring 4.5–9 µm long. Cystidia absent. Pileipellis a cutis made up of hyphae 4–7.5 µm in width, subcylindric, marginally thickened walls (up to 0.5 µm), interwoven to subparallel, pale yellow in KOH; terminal cells 25–47 × 4–8 µm, subclavate to subcylindrical with a rounded-off apex. Clamp connections were not observed in all tissues.
Habitat—Solitary to scattered on the ground of forests dominated by fagaceous trees.
Known distribution—Southern China (Hainan Province).
Additional specimen examined—CHINA. Hainan Province: Wuzhishan, Hainan Tropical Rainforest National Park, elev. 600 m, 9 June 2022, X. Zhang039-1(FHMU7716).
Notes—Our molecular data indicated that the new species C. albimarginatus falls into subg. Imperforati (Figure 1). Moreover, the morphological features of the new species are also consistent with the concept of the subgenus defined by Cao et al. [10]. Morphologically, C. albimarginatus is similar to some other species of subg. Imperforati, viz. Chinese C. badiogriseus T. Cao & H.S. Yuan, Indian C. albostrigosus C.K. Pradeep & K.B. Vrinda, C. parvogriseus U. Singh, K. Das & Buyck, and C. indicus Deepika, Upadhyay & Reddy, which all share the common features including a small basidioma, a smooth or slightly wrinkled hymenophore, broadly ellipsoid basidiospores, and an absence of clamp connections. However, C. badiogriseus has a darker pileus, a smooth, brownish gray to gray hymenophore, larger basidiospores (8–10.5 × 6.8–7.5 µm), and its distribution in temperate China [10]; C. albostrigosus has a basidioma with white strigose hairs, larger basidiospores (9–11.5 × 6–8 µm), and its association with trees of Dipterocarpaceae [29]; C. parvogriseus has a much paler, white to grayish white hymenophore and larger basidiospores (7–12 × 6.5–9 µm) [40]; C. indicus has a light brownish to sand-colored pileus, a yellowish gray stipe, larger basidiospores (7.5–10.5 × 6–7 µm), and its association with trees of Pinaceae [33]. Phylogenetically, these species referred to above formed a well-supported clade (BS = 99%, PP = 1.0) (Figure 1). A BLAST comparison of the C. albimarginatus sequences with those available in GenBank revealed that the 28S sequence showed 96.70%, 95.77%, 95.75%, and 95.42% similarity to those of C. albostrigosus, C. badiogriseus, C. parvogriseus, and C. indicus, respectively. The highest similarity for the ITS sequence was observed with C. atratus (Corner) Yomyart, Watling, Phosri, Piap. & Sihan. (96.39% identity).
Craterellus involutus N.K. Zeng & T. Jiang, sp. nov.
MycoBank: MB 856896
Figure 2c,d and Figure 4.
Etymology—Latin “involutus”, meaning curly, refers to the incurved margin of the new species.
Holotype—CHINA. Fujian Province: Sanming Prefecture-level City, Jiangle County, Longqishan National Nature Reserve, elev. 600 m, 21 August 2023, N.K. Zeng8178 (FHMU7709). 28S = PQ604686, TEF1 = PQ641589.
Diagnosis—Craterellus involutus is differentiated from the closest Craterellus species by a basidioma without a distinct boundary between the pileus and stipe, an incurved pileal margin, smaller basidiospores, a trichodermal pileipellis made up of uninflated hyphae, and its connection with Fagaceae trees.
Description—Pileus 1.3–4.7 cm diameter, infundibuliform; margin obviously incurved; surface dry, velutinate, pale brown (4D7) to brownish-black (4F7); context exceedingly thin, grayish-brown (4E7). Hymenophore nearly smooth, with slight rugulose, ashen gray (5C1). Stipe 1.2–5 × 0.4–1.4 cm, axial, hollow, unified with the pileus; dry surface, ashen gray (5C1). Odor not distinctive. Spore print not obtained.
Basidiospores [200/10/3] 8–9.25–10.5(–11.5) × 5–5.95–7 µm, Q = 1.36–1.80(–1.82), Qm = 1.56 ± 0.02, globose to subglobose, sometimes broadly ellipsoid, smooth, marginally thickened walls (up to 0.5 µm), yellowish coloration in KOH. Basidia 50–62 × 6.5–8.5 µm, 2–5-spored, subclavate to subcylindrical, somewhat curving, marginally thickened walls (up to 0.5 µm), faintly yellow in KOH; sterigmata measuring 5.5–8 µm long. Cystidia absent. Pileipellis a trichoderm made up of hyphae 3–11 µm in width, subcylindric, marginally thickened walls (0.5–1.0 µm), yellowish in KOH; terminal cells 35–85 × 5.5–12 µm, subclavate to subcylindrical with a rounded-off apex. Clamp connections were not observed in all tissues.
Habitat—Gregarious on the ground of forests dominated by fagaceous trees.
Known distribution—Southeastern China (Fujian Province).
Additional specimens examined—CHINA. Fujian Province: Sanming Prefecture-level City, Jiangle County, Longqishan National Nature Reserve, elev. 600 m, 21 August 2023, N.K. Zeng8119 (FHMU7708).
Notes—Our molecular data indicated that the new species C. involutus is embedded in subg. Craterellus (Figure 1). Moreover, the morphological attributes are also in agreement with the concept of the subgenus [10]. Morphologically, C. involutus is similar to some other species of subg. Craterellus, viz. Chinese C. croceialbus T. Cao & H.S. Yuan, C. macrosporus T. Cao & H.S. Yuan, and C. squamatus T. Cao & H.S. Yuan, European C. cornucopioides s.s., North American C. fallax A.H. Sm., and C. calicornucopioides D. Arora & J.L. Frank, which all share common features including a dark-color pileus, a smooth or wrinkled hymenophore, and an absence of a distinct boundary between the pileus and stipe. However, C. croceialbus, C. macrosporus, and C. squamatus are distributed in temperate China [10]. Moreover, C. croceialbus has a pileus that is brownish gray to grayish brown, with an orange-white margin, and larger basidiospores (10–12 × 6.8–8 µm) [10]; C. macrosporus has a brownish gray to grayish brown pileus and larger basidiospores (12.8–14.5 × 9–11 µm) [10]; C. squamatus has a smaller, light brown to dark brown pileus and larger basidiospores (12–13.8 × 8.5–9.5 µm) [10]. Craterellus cornucopioides s.s. has larger basidiospores (13–14 × 7–8 µm) and occurs in temperate regions [51]; C. fallax has larger basidiospores (10–13 × 7–9 µm) and is associated with trees of Pinaceae [37]; C. calicornucopioides has a larger basidioma (up to 20 cm) with a wavy pileal margin, larger basidiospores (11–14 × 8–10 µm), and an occurrence of numerous clamp connections [31]. Phylogenetically, these species referred to above formed a well-supported clade (BS = 92%, PP = 1.0). The 28S sequence data showed 95.95%, 95.21%, 94.96%, and 94.65% similarity to those of C. squamatus, C. croceialbus, C. fallax, and C. macrosporus, respectively, while the TEF1 sequence data show 96.46%, 94.8%, and 90.53% similarity to those of C. squamatus, C. fallax, and C. croceialbus, respectively.
Craterellus cornucopioides var. mediosporus Corner and C. verrucosus Massee, two taxa originally described from Malaysia, also exhibit morphological similarities to C. involutus. Nevertheless, C. cornucopioides var. mediosporus has a cutis pileipellis and is distributed in tropical areas [1]; C. verrucosus has a pale-color pileus, a thicker hymenophore, and a pileipellis that typically consists of broader hyphae (up to 20 µm) [1].
Craterellus longitipes N.K. Zeng & T. Jiang, sp. nov.
MycoBank: MB 856897
Figure 2e,f and Figure 5.
Etymology—Latin “longi-”, meaning long, “tipes”, meaning stipe, refer to the long stipe of the new species.
Holotype—CHINA. Fujian Province: Sanming Prefecture-level City, Jiangle County, Longqishan National Nature Reserve, elev. 350 m, 21 August 2023, N.K. Zeng8131 (FHMU7705). 28S = PQ604683, ITS = PQ611010, TEF1 = PQ641586.
Diagnosis—Craterellus longitipes is differentiated from its closest relatives in Craterellus by a pale brown to brown basidioma, a prominent separation between pileus and stipe, a long stipe, a pileipellis made up of uninflated hyphae, and its relationship with Fagaceae trees.
Description—Pileus 2–5.3 cm in diameter, center strongly depressed; margin broadly wavy or unevenly folded; surface dry, slightly rugose, pale brown to brown (4D7); context very thin, blackish-brown (4E7). Hymenophore veined, decurrent; folds 0.05–0.1 cm broad, usually forked, commonly anastomosing, distant, ashen gray (4B2). Stipe 4.2–7 × 0.4–0.7 cm, central, hollow, subcylindrical, frequently flexuous, with prominent separation between pileus and stipe; dry surface, blackish-brown (4F5). Odor not distinctive. Spore print not obtained.
Basidiospores [180/9/3] 6–7.1–8(–9) × 4.5–5.03–5.5(–6) µm, Q = 1.27–1.60(–1.70), Qm = 1.41 ± 0.01, subglobose to ellipsoid or broadly ellipsoid, smooth, marginally thickened walls (up to 0.6 µm), yellowish in KOH. Basidia 36–70 × 4–9 µm, 3–6-spored, subclavate to subcylindrical, marginally thickened walls (up to 0.5 µm), colorless or yellowish in KOH; sterigmata measuring 4.5–10 µm long. Cystidia absent. Pileipellis a cutis made up of hyphae 4.5–8 µm in width, mostly cylindrical, occasionally branched, thin to marginally thickened walls (up to 1 µm), yellowish in KOH; terminal cells 27–74.5 × 7–11.5 µm, subcylindrical or clavate with a rounded-off apex. Clamp connections were not observed in all tissues.
Habitat—Gregarious on the ground of forests dominated by fagaceous trees.
Known distribution—Southeast China (Fujian Province).
Additional specimens examined—CHINA. Fujian Province: Sanming Prefecture-level City, Jiangle County, Longqishan National Nature Reserve, elev. 600 m, 21 August 2023, N.K. Zeng8131-1(FHMU7706); same geographical location and date, N.K. Zeng8131-2 (FHMU7707).
Notes—Our molecular data indicated that the subgeneric rank of the new species C. longitipes should be further defined (Figure 1). It is worth noting that the closely related taxa of C. longitipes, viz. C. connatus G.P. Zhao, J.J. Hu, B. Zhang & Y. Li and C. striatus G.P. Zhao, J.J. Hu, B. Zhang & Y. Li, both described from northeastern China, are in the same species-level phylogenetic branches with strong support (BS = 100%, PP = 1.0). (Figure 1: lineage 3). By comparing the 28S and TEF1 sequences of C. conatus and C. striatus in GenBank, high identities of 99.89% and 99.74% were observed, respectively. Moreover, the two taxa do not exhibit any major morphological differences [17]. And thus, we are sure that C. striatus is synonymous with C. connatus. Morphologically, C. longitipes is similar to C. atrobrunneolus T. Cao & H.S. Yuan and C. conatus/striatus; both share the common features including a brown pileus, a gray hymenophore, and an absence of clamp connections. However, C. atrobrunneolus has a dark brown to almost black pileus, a shorter stipe, and wider hyphae in pileipellis (up to 11 µm) [15]; C. conatus/striatus has a hymenophore sometimes with a strongly anastomosing vein, a shorter stipe, and wider hyphae in pileipellis (up to 16 µm), and its distribution is in temperate areas [17]. Phylogenetically, the 28S sequence data showed 97.63% and 97.10% similarity to those of C. conatus/striatus and C. atrobrunneolus, respectively, while the ITS sequence showed 98.85% similarity with C. atrobrunneolus, and the TEF1 sequence showed 97.51% similarity with C. conatus/striatus.

4. Discussion

With more and more molecular data, numerous previously published taxa have been re-assessed, which have updated the taxonomy of Craterellus [2,15,16,17,39]. As an example, the European C. cornucopioides, distinguished by its brown to black pileus and smooth hymenophore, was once considered a widely distributed species [1]. However, recent studies have showed that collections named “black trumpet species” represent multiple taxa rather than a single widely distributed species. In China, many specimens labeled as “C. cornucopioides” were re-evaluated; several species such as C. badiogriseus, C. croceialbus, C. involutus, C. parvopullus, C. macrosporus, and C. squamatus were described in previous or present studies [10,15,16].
In present study, the species richness of Craterellus in China was uncovered, revealing seventeen species-level phylogenetic branches (Figure 1). Three lineages (6, 8, and 14) were classified as previously unrecorded taxa, viz. C. albimarginatus, C. involutus, and C. longitipes; twelve (lineages 1, 3–5, 9–13, 15–17) are classified as previously described species, viz. C. albidus, C. atrobrunneolus, C. aureus, C. badiogriseus, C. croceialbus, C. lutescens, C. macrosporus, C. connatus/striatus, C. minor, C. parvopullus, C. fulviceps, and C. squamatus; and two (lineages 2, 7) remain undescribed due to the paucity of materials. Geographically, C. badiogriseus, C. connatus/striatus, C. croceialbus, C. macrosporus, and C. squamatus occur in temperate areas of China, and other representatives of the group, viz. C. albidus, C. albimarginatus, C. atrobrunneolus, C. aureus, C. fulviceps, C. involutus, C. longitipes, C. lutescens, C. minor, C. parvopullus, and C. yunnanensis (W.F. Chiu) Buyck, are from subtropical/tropical China.
In previous studies, six subgenera of Craterellus were described [10]. The systematic positions of most Chinese Craterellus species have been defined; they are members of subg. Cariosi, subg. Craterellus, subg. Imperforati, subg. Lamelles, and subg. Ovoidei (Table 2). Besides C. yunnanensis, one species being absent of molecular data, the systematic position of C. atrobrunneolus, C. connatus/striatus, and C. longitipes should be further defined (Figure 1).
Key to accepted Craterellus taxa in China
1. Absence of obvious demarcation between pileus and stipe2
1. Presence of obvious demarcation between pileus and stipe8
2. Pileus colored with vivid yellow to orangeC. aureus
2. Pileus colored with gray brown, brown, dark brown to almost black3
3. Pileal surface covered with scabrousC. squamatus
3. Pileal surface subglabrous to glabrous4
4. Basidiospores average length <8 µm, occurring in tropical regionsC. parvopullus
4. Basidiospores average length >8 µm, occurring in subtropical or temperate regions5
5. Pileal surface colored with blackish brown, blackish to almost black, basidiospores average length <11 µm.6
5. Pileal surface colored with brown, gray-brown to dark brown, lacking any black tinge, basidiospores average length >11 µm. 7
6. Basidia longer (up to 106 µm), pileipellis a cutis, and distributed in temperate regionsC. badiogriseus
6. Basidia shorter (up to 62 µm), pileipellis a trichoderm, and distributed in subtropical regionsC. involutus
7. Margin of pileus colored with dark brown, basidiospores larger measuring 12.8–14.5 × 9–11 µmC. macrosporus
7. Margin of pileus colored with orange-white, basidiospores smaller measuring 10–12 × 6.8–8 µmC. croceialbus
8. Basidomata very pale, whitish, grow on dead woodC. albidus
8. Basidomata brown, yellow, grow on ground9
9. Hyphal clamp connections absent10
9. Hyphal clamp connections abundant13
10. Hymenophore slightly veined, white tinged with violet, stipe beige-almond, and distributed in tropical regionsC. albimarginatus
10. Hymenophore with well-developed veins, gray, stipe brown, and distributed in subtropical or temperate regions11
11. Stipe shorter (up to 3.5 cm), hymenophore with strongly anastomosing vein, and distributed in temperate regions C. connatus/striatus
11. Stipe longer (up to 5 cm), hymenophore veined, and distributed in subtropical regions12
12. Pileus colored with pale brown to brown, pileipellis composed of narrower hyphae (up to 8 µm)C. longitipes
12. Pileus colored with dark brown to almost black, pileipellis composed of wider hyphae (up to 11 µm)C. atrobrunneolus
13. Basidiospores shorter (6–7.5 µm), terminal cells wider (up to 19 µm)C. yunnanensis
13. Basidiospores longer (8–11.5 µm), terminal cells narrower (up to 10 µm)14
14. Pileus colored with brown, hymenophore veined, or sometimes smoothC. lutescens
14. Pileus colored with grayish-yellow to fulvous, hymenophore veined, never smooth15
15. Hymenophore colored with yellowish, stipe colored with egg-yolk yellowC. fulviceps
15. Hymenophore colored with white to pale, stipe colored with pale lemon yellowC. minor

Author Contributions

Conceptualization, N.-K.Z. and X.-D.M.; methodology, performing the experiment and formal analysis, T.J. and L.Z.; resources and data curation, N.-K.Z., T.J., X.Z. and L.Z.; writing—original draft preparation, T.J., H.-Z.Q., H.D., L.Z. and X.Z.; writing—review and editing, N.-K.Z. and X.-D.M.; supervision, N.-K.Z.; project administration, N.-K.Z.; funding acquisition, N.-K.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the National Natural Science Foundation of China (No. 32160001), the Special Fund Project for Environmental Protection of Hainan Province: Investigation and Assessment of Biodiversity in Wuzhishan City, and the Graduate Innovative Research Project of Hainan Medical University (HYYB2023A40, HYYB2023A41, HYYB2023A42).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The datasets presented in this study can be found in online accession number(s), which are as follows: National Center for Biotechnology Information (NCBI) GenBank, https://www.ncbi.nlm.nih.gov/genbank/, PQ604676-PQ604690, PQ611003-PQ611013, PQ641578-PQ641597 and MycoBank, https://www.mycobank.org/, MB856885, MB856896, MB856897.

Acknowledgments

The first author is very grateful to Yu-Zhuo Zhang, Gongyi Public Traditional Chinese Medicine Hospital, for her help with molecular data analyses and Yong-Guo Chen, Longqishan National Nature Reserve (Fujian Province, China), for his kind help during the field investigations.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

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Figure 1. A maximum likelihood (ML) phylogenetic tree of Craterellus was derived from the combined dataset (28S + ITS + TEF1). ML bootstrap values (BS ≥ 70%) and Bayesian posterior probabilities (PP ≥ 0.95) are shown at the nodes of individual branches.
Figure 1. A maximum likelihood (ML) phylogenetic tree of Craterellus was derived from the combined dataset (28S + ITS + TEF1). ML bootstrap values (BS ≥ 70%) and Bayesian posterior probabilities (PP ≥ 0.95) are shown at the nodes of individual branches.
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Figure 2. Basidiomata of Craterellus taxa. (a,b) C. albimarginatus (FHMU7715, holotype); (c,d) C. involutus (FHMU7709, holotype); (e,f) C. longitipes (FHMU7705, holotype). Scale bars: (a–f) = 1 cm. (a,b) photos by X. Zhang; (c–f) photos by N.K. Zeng.
Figure 2. Basidiomata of Craterellus taxa. (a,b) C. albimarginatus (FHMU7715, holotype); (c,d) C. involutus (FHMU7709, holotype); (e,f) C. longitipes (FHMU7705, holotype). Scale bars: (a–f) = 1 cm. (a,b) photos by X. Zhang; (c–f) photos by N.K. Zeng.
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Life 15 00157 g003
Figure 3. Microscopic structures of Craterellus albimarginatus (FHMU7715, holotype). (a) Basidiospores. (b) Basidia. (c) Pileipellis. Scale bars: (a–c) = 10 µm. Drawing by T. Jiang.
Figure 3. Microscopic structures of Craterellus albimarginatus (FHMU7715, holotype). (a) Basidiospores. (b) Basidia. (c) Pileipellis. Scale bars: (a–c) = 10 µm. Drawing by T. Jiang.
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Figure 4. Microscopic structures of Craterellus involutus (FHMU7709, holotype). (a) Basidiospores. (b) Basidia. (c) Pileipellis. Scale bars: (a–c) = 10 µm. Drawing by T. Jiang.
Figure 4. Microscopic structures of Craterellus involutus (FHMU7709, holotype). (a) Basidiospores. (b) Basidia. (c) Pileipellis. Scale bars: (a–c) = 10 µm. Drawing by T. Jiang.
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Figure 5. Microscopic structures of Craterellus longitipes (FHMU7705, holotype). (a) Basidiospores. (b) Basidia. (c) Pileipellis. Scale bars: (a–c) = 10 µm. Drawing by T. Jiang.
Figure 5. Microscopic structures of Craterellus longitipes (FHMU7705, holotype). (a) Basidiospores. (b) Basidia. (c) Pileipellis. Scale bars: (a–c) = 10 µm. Drawing by T. Jiang.
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Table 1. Taxa, vouchers, locations, and GenBank accession numbers of DNA sequences used in this study.
Table 1. Taxa, vouchers, locations, and GenBank accession numbers of DNA sequences used in this study.
TaxonVoucherLocalityGenBank Accession Nos.References
28SITSTEF1
Craterellus albidusHGASMF01-3581ChinaMT921161——[28]
C. albidusHGASMF01-10046ChinaMT921162——[28]
C. albimarginatusZX039 (FHMU7715) (holotype)ChinaPQ604676PQ611003—Present study
C. albimarginatusZX039-1 (FHMU7716)China—PQ611004—Present study
C. albostrigosusCAL 1624IndiaMG593194——[29]
C. atratoidesTH8243Guyana—KT339209—[30]
C. atratoidesMCA1313GuyanaJQ915119JQ915093—[30]
C. atratoidesTH9232GuyanaJQ915137JQ915111—[30]
C. atratoidesTH8473GuyanaJQ915129JQ915103—[30]
C. atratoidesAMV1965aColombiaKT724157KT724106—Unpublished
C. atratoidesAMV1959ColombiaKT724156——Unpublished
C. atratoidesAMV1870Colombia—KT354698—Unpublished
C. atratoidesAMV1990Colombia—KT354699—Unpublished
C. atratusAMV1832ColombiaKT724158KT724107—Unpublished
C. atratusTH9203GuyanaJQ915133JQ915107—[30]
C. atratusMCA990GuyanaJQ915126JQ915100—[30]
C. atratusMCA1070GuyanaJQ915118JQ915092—[30]
C. atrobrunneolusYuan13878ChinaMN894058MN902353—[15]
C. atrobrunneolusN.K. Zeng8189 (FHMU7704)ChinaPQ604677PQ611005PQ641578Present study
C. atrocinereusArora15001United States—KR560049—[31]
C. atrocinereusJLF3750United States—KR560048—[31]
C. aureusN.K. Zeng1057 (FHMU2407)ChinaOL439672OM469019PQ641579[16]
C. aureusN.K. Zeng3141 (FHMU2102)ChinaOL439674OM469020PQ641580[16]
C. badiogriseusYuan 14779ChinaMW979533MW980549MW999433[10]
C. caeruleofuscusMH17001United StatesMT237468MH558300—[15]
C. calicornucopioidesJLF3744United States—KR560046—[31]
C. calicornucopioidesArora 15002United States—KR560047—[31]
C. calyculusMushroom Observer # 321697United States—MK607596—Unpublished
C. carolinensisFLAS-F-59997United States—KY654712—[32]
C. cinereofimbriatusTH9264GuyanaJQ915138JQ915112—[30]
C. cinereofimbriatusTH9075GuyanaJQ915131JQ915105—[30]
C. cinereus107-08IndiaJF412276JF412278—[33]
C. cinereusAST2015Pakistan—MF374488—[34]
C. cornucopioidesHbO-53302NorwayAF105301——[2]
C. cornucopioidesUPSF-11792SwedenAF105297——[2]
C. cornucopioidesWA0000071019Poland—MK028881—[35]
C. cornucopioides—ChinaAJ279572——[12]
C. cornucopioidesCNF 1/7292Croatia—MK169230—[36]
C. croceialbusYuan 14623ChinaMW979529MW980572MW999430[10]
C. croceialbusYuan 14647ChinaMW979530MW980573MW999431[10]
C. cornucopioides var. mediosporus268-06IndiaJF412275JF412277—[33]
C. connatusHMJAU 61462 (T)ChinaOM509448—ON125915[17]
C. connatusHMJAU 61462China——ON125916[17]
C. excelsusTH8235GuyanaJQ915128JQ915102—[30]
C. excelsusTH7515GuyanaJQ915127JQ915101—[30]
C. fallaxPBM3290United States—GU590923—[37]
C. fulvicepsMHHNU10567 (FHMU6553)Hunan, central ChinaOL439678OL439548—[16]
C. fulvicepsN.K. Zeng7833 (FHMU7710)ChinaPQ604678PQ611006PQ641581Present study
C. fulvicepsN.K. Zeng7833-1 (FHMU7711)ChinaPQ604679PQ611007PQ641582Present study
C. fulvicepsN.K. Zeng7940 (FHMU7712)ChinaPQ604680—PQ641583Present study
C. fulvicepsN.K. Zeng8033 (FHMU7713)ChinaPQ604681PQ611008PQ641584Present study
C. fulvicepsN.K. Zeng8163 (FHMU7714)ChinaPQ604682PQ611009PQ641585Present study
C. ignicolorUPSF-11794United StatesAF105314——[2]
C. indicusPUN3884IndiaHM113529HM113530—[33]
C. indicusMSR6India—HQ450769—[33]
C. inusitatusCAL 1625IndiaMG593195——[29]
C. involutusN.K. Zeng8119 (FHMU7708)ChinaPQ604685—PQ641588Present study
C. involutusN.K. Zeng8178 (FHMU7709) (holotype)ChinaPQ604686—PQ641589Present study
C. longitipesN.K. Zeng8131 (FHMU7705) (holotype)ChinaPQ604683PQ611010PQ641586Present study
C. longitipesN.K. Zeng8131-1 (FHMU7706)China—PQ611011PQ641587Present study
C. longitipesN.K. Zeng8131-2 (FHMU7707)ChinaPQ604684PQ611012—Present study
C. lutescensma023ItalyMN592820MN595294—[38]
C. lutescensL.P. Tang1647 (FHMU6547)ChinaOL439679OL439549—[16]
C. lutescensW.H. Zhang441-1 (FHMU6544)ChinaOL439681OL439550—[16]
C. luteusGDGM46432ChinaMG727898MG727897—[11]
C. luteusGDGM48105ChinaMG701171MG727896—[11]
C. macrosporusYuan 14782ChinaMW979531MW979531—[10]
C. melanoxerosSS576SwedenJQ976983——[39]
C. minor420526MF0891ChinaMG712381——Unpublished
C. minorMHHNU32505 (FHMU6554)ChinaOL439684OL439553PQ641597[16]
C. odoratus14026h2United StatesMN227279——Unpublished
C. odoratus14026h1United StatesMN227278——Unpublished
C. odoratusUPSF-11799United StatesAF105306——[2]
C. olivaceoluteusTH9205GuyanaJQ915135JQ915109—[30]
C. olivaceoluteusMCA3186GuyanaJQ915124JQ915098—[30]
C. parvogriseusCAL1533IndiaMF421098MF421099—[40]
C. parvogriseusKNPS_WC18158KoreaMT974136——[41]
C. parvopullusN.K. Zeng4913 (FHMU6555)ChinaOL439685OM334829PQ641592[16]
C. parvopullusN.K. Zeng4912 (FHMU6556)ChinaOL439686OM334828PQ641590[16]
C. parvopullusN.K. Zeng4911 (FHMU6557)ChinaOL439687OM334827PQ641591[16]
C. parvopullusN.K. Zeng7557 (FHMU7717)ChinaPQ604687—PQ641593Present study
C. parvopullusN. K. Zeng7521 (FHMU7718)ChinaPQ604688—PQ641594Present study
C. parvopullusN. K. Zeng7512 (FHMU7719)ChinaPQ604689——Present study
C. pleurotoidesMCA3124GuyanaJQ915123JQ915097—[30]
C. pleurotoidesTH9220GuyanaJQ915136JQ915110—[30]
C. shoreaeCAL_F_1396IndiaKY290585——[15]
C. sinuosusTF1802United StatesU87992——[42]
Craterellus sp.MHHNU32154 (FHMU6552)ChinaOL439677OL439547PQ641595[16]
Craterellus sp.N.K. Zeng8042 (FHMU7703)ChinaPQ604690PQ611013PQ641596Present study
C. squamatusYuan 14520ChinaMW979534MW980571MW999434[10]
C. squamatusYuan 14721ChinaMW979535MW980570MW999435[10]
C. strigosusTH9204GuyanaJQ915134JQ915108—[30]
C. strigosusMCA1750GuyanaJQ915120JQ915094—[30]
C. striatusHMJAU 61463 (T)ChinaOM509446—ON125913[17]
C. striatusHMJAU 61463ChinaOM509447—ON125914[17]
C. tubaeformisDAVFP26257Canada—HM468491—[43]
C. tubaeformisUPS-11797United StatesAF105311——[2]
C. tubaeformisTRTC52516Belgium—HM468496—[43]
C. tubaeformisUPSF-11793SwedenAF105307——[2]
C. tubaeformisBB 07.293SlovakiaKF294640——[44]
C. tubaeformisTRTC52235Belgium—HM468497—[43]
C. tubaeformisBR089347Canada—HM468493—[43]
C. tubaeformisOSC-41280United StatesAF105313——[2]
C. tubaeformisGCB1905Belgium—MT004784—[2]
C. tubaeformisUPSF-11795United StatesAF105308——[2]
Hydnum minusN.K. Zeng2819 (FHMU2461)ChinaKY407528KY407533KY407534[25]
H. cremeoalbumN.K. Zeng2511 (FHMU2153)ChinaKY407527KY407532KY407535[25]
Bold GenBank numbers highlight the newly generated sequences.
Table 2. Subgenera and accepted species of Craterellus in China.
Table 2. Subgenera and accepted species of Craterellus in China.
SubgenusSpeciesLocalityReference
CariosiC. lutescensEurope[16]
CraterellusC. croceialbusLiaoning NE China[10]
C. involutusFujian, SE ChinaPresent study
C. macrosporusLiaoning NE China[10]
C. squamatusLiaoning NE China[10]
ImperforatiC. albidusGuizhou, SW China[28]
C. albimarginatusHainan, southern ChinaPresent study
C. badiogriseusLiaoning, NE China[10]
LamellesC. fulvicepsHunan, central China[16]
C. minorHunan, central China[16]
OvoideiC. aureusHong Kong, southern China[16]
C. parvopullusHainan, southern China[16]
—C. atrobrunneolusYunnan, SW China[15]
C. connatus/striatusLiaoning, NE China[17]
C. longitipesFujian, SE ChinaPresent study
C. yunnanensisYunnan, SW China[52]
SW: southwestern, NE: northeastern, SE: southeastern.
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Jiang, T.; Zhao, L.; Zhang, X.; Qin, H.-Z.; Deng, H.; Mu, X.-D.; Zeng, N.-K. Updated Taxonomy of Chinese Craterellus (Hydnaceae, Cantharellales) with Three New Species Described. Life 2025, 15, 157. https://doi.org/10.3390/life15020157

AMA Style

Jiang T, Zhao L, Zhang X, Qin H-Z, Deng H, Mu X-D, Zeng N-K. Updated Taxonomy of Chinese Craterellus (Hydnaceae, Cantharellales) with Three New Species Described. Life. 2025; 15(2):157. https://doi.org/10.3390/life15020157

Chicago/Turabian Style

Jiang, Tian, Lei Zhao, Xu Zhang, Hua-Zhi Qin, Hui Deng, Xiao-Dong Mu, and Nian-Kai Zeng. 2025. "Updated Taxonomy of Chinese Craterellus (Hydnaceae, Cantharellales) with Three New Species Described" Life 15, no. 2: 157. https://doi.org/10.3390/life15020157

APA Style

Jiang, T., Zhao, L., Zhang, X., Qin, H.-Z., Deng, H., Mu, X.-D., & Zeng, N.-K. (2025). Updated Taxonomy of Chinese Craterellus (Hydnaceae, Cantharellales) with Three New Species Described. Life, 15(2), 157. https://doi.org/10.3390/life15020157

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