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. 2025 Jan 23;15(2):157. doi: 10.3390/life15020157

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

Tian Jiang 1,2,†, Lei Zhao 3,†, Xu Zhang 2, Hua-Zhi Qin 1, Hui Deng 1, Xiao-Dong Mu 4,*, Nian-Kai Zeng 1,2,*
Editor: Pabulo Rampelotto
PMCID: PMC11857064  PMID: 40003566

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.

Keywords: molecular phylogeny, morphology, new taxa, taxonomy, trumpet mushroom

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).

Table 1.

Taxa, vouchers, locations, and GenBank accession numbers of DNA sequences used in this study.

Taxon Voucher Locality GenBank Accession Nos. References
28S ITS TEF1
Craterellus albidus HGASMF01-3581 China MT921161 — — [28]
C. albidus HGASMF01-10046 China MT921162 — — [28]
C. albimarginatus ZX039 (FHMU7715) (holotype) China PQ604676 PQ611003 — Present study
C. albimarginatus ZX039-1 (FHMU7716) China — PQ611004 — Present study
C. albostrigosus CAL 1624 India MG593194 — — [29]
C. atratoides TH8243 Guyana — KT339209 — [30]
C. atratoides MCA1313 Guyana JQ915119 JQ915093 — [30]
C. atratoides TH9232 Guyana JQ915137 JQ915111 — [30]
C. atratoides TH8473 Guyana JQ915129 JQ915103 — [30]
C. atratoides AMV1965a Colombia KT724157 KT724106 — Unpublished
C. atratoides AMV1959 Colombia KT724156 — — Unpublished
C. atratoides AMV1870 Colombia — KT354698 — Unpublished
C. atratoides AMV1990 Colombia — KT354699 — Unpublished
C. atratus AMV1832 Colombia KT724158 KT724107 — Unpublished
C. atratus TH9203 Guyana JQ915133 JQ915107 — [30]
C. atratus MCA990 Guyana JQ915126 JQ915100 — [30]
C. atratus MCA1070 Guyana JQ915118 JQ915092 — [30]
C. atrobrunneolus Yuan13878 China MN894058 MN902353 — [15]
C. atrobrunneolus N.K. Zeng8189 (FHMU7704) China PQ604677 PQ611005 PQ641578 Present study
C. atrocinereus Arora15001 United States — KR560049 — [31]
C. atrocinereus JLF3750 United States — KR560048 — [31]
C. aureus N.K. Zeng1057 (FHMU2407) China OL439672 OM469019 PQ641579 [16]
C. aureus N.K. Zeng3141 (FHMU2102) China OL439674 OM469020 PQ641580 [16]
C. badiogriseus Yuan 14779 China MW979533 MW980549 MW999433 [10]
C. caeruleofuscus MH17001 United States MT237468 MH558300 — [15]
C. calicornucopioides JLF3744 United States — KR560046 — [31]
C. calicornucopioides Arora 15002 United States — KR560047 — [31]
C. calyculus Mushroom Observer # 321697 United States — MK607596 — Unpublished
C. carolinensis FLAS-F-59997 United States — KY654712 — [32]
C. cinereofimbriatus TH9264 Guyana JQ915138 JQ915112 — [30]
C. cinereofimbriatus TH9075 Guyana JQ915131 JQ915105 — [30]
C. cinereus 107-08 India JF412276 JF412278 — [33]
C. cinereus AST2015 Pakistan — MF374488 — [34]
C. cornucopioides HbO-53302 Norway AF105301 — — [2]
C. cornucopioides UPSF-11792 Sweden AF105297 — — [2]
C. cornucopioides WA0000071019 Poland — MK028881 — [35]
C. cornucopioides — China AJ279572 — — [12]
C. cornucopioides CNF 1/7292 Croatia — MK169230 — [36]
C. croceialbus Yuan 14623 China MW979529 MW980572 MW999430 [10]
C. croceialbus Yuan 14647 China MW979530 MW980573 MW999431 [10]
C. cornucopioides var. mediosporus 268-06 India JF412275 JF412277 — [33]
C. connatus HMJAU 61462 (T) China OM509448 — ON125915 [17]
C. connatus HMJAU 61462 China — — ON125916 [17]
C. excelsus TH8235 Guyana JQ915128 JQ915102 — [30]
C. excelsus TH7515 Guyana JQ915127 JQ915101 — [30]
C. fallax PBM3290 United States — GU590923 — [37]
C. fulviceps MHHNU10567 (FHMU6553) Hunan, central China OL439678 OL439548 — [16]
C. fulviceps N.K. Zeng7833 (FHMU7710) China PQ604678 PQ611006 PQ641581 Present study
C. fulviceps N.K. Zeng7833-1 (FHMU7711) China PQ604679 PQ611007 PQ641582 Present study
C. fulviceps N.K. Zeng7940 (FHMU7712) China PQ604680 — PQ641583 Present study
C. fulviceps N.K. Zeng8033 (FHMU7713) China PQ604681 PQ611008 PQ641584 Present study
C. fulviceps N.K. Zeng8163 (FHMU7714) China PQ604682 PQ611009 PQ641585 Present study
C. ignicolor UPSF-11794 United States AF105314 — — [2]
C. indicus PUN3884 India HM113529 HM113530 — [33]
C. indicus MSR6 India — HQ450769 — [33]
C. inusitatus CAL 1625 India MG593195 — — [29]
C. involutus N.K. Zeng8119 (FHMU7708) China PQ604685 — PQ641588 Present study
C. involutus N.K. Zeng8178 (FHMU7709) (holotype) China PQ604686 — PQ641589 Present study
C. longitipes N.K. Zeng8131 (FHMU7705) (holotype) China PQ604683 PQ611010 PQ641586 Present study
C. longitipes N.K. Zeng8131-1 (FHMU7706) China — PQ611011 PQ641587 Present study
C. longitipes N.K. Zeng8131-2 (FHMU7707) China PQ604684 PQ611012 — Present study
C. lutescens ma023 Italy MN592820 MN595294 — [38]
C. lutescens L.P. Tang1647 (FHMU6547) China OL439679 OL439549 — [16]
C. lutescens W.H. Zhang441-1 (FHMU6544) China OL439681 OL439550 — [16]
C. luteus GDGM46432 China MG727898 MG727897 — [11]
C. luteus GDGM48105 China MG701171 MG727896 — [11]
C. macrosporus Yuan 14782 China MW979531 MW979531 — [10]
C. melanoxeros SS576 Sweden JQ976983 — — [39]
C. minor 420526MF0891 China MG712381 — — Unpublished
C. minor MHHNU32505 (FHMU6554) China OL439684 OL439553 PQ641597 [16]
C. odoratus 14026h2 United States MN227279 — — Unpublished
C. odoratus 14026h1 United States MN227278 — — Unpublished
C. odoratus UPSF-11799 United States AF105306 — — [2]
C. olivaceoluteus TH9205 Guyana JQ915135 JQ915109 — [30]
C. olivaceoluteus MCA3186 Guyana JQ915124 JQ915098 — [30]
C. parvogriseus CAL1533 India MF421098 MF421099 — [40]
C. parvogriseus KNPS_WC18158 Korea MT974136 — — [41]
C. parvopullus N.K. Zeng4913 (FHMU6555) China OL439685 OM334829 PQ641592 [16]
C. parvopullus N.K. Zeng4912 (FHMU6556) China OL439686 OM334828 PQ641590 [16]
C. parvopullus N.K. Zeng4911 (FHMU6557) China OL439687 OM334827 PQ641591 [16]
C. parvopullus N.K. Zeng7557 (FHMU7717) China PQ604687 — PQ641593 Present study
C. parvopullus N. K. Zeng7521 (FHMU7718) China PQ604688 — PQ641594 Present study
C. parvopullus N. K. Zeng7512 (FHMU7719) China PQ604689 — — Present study
C. pleurotoides MCA3124 Guyana JQ915123 JQ915097 — [30]
C. pleurotoides TH9220 Guyana JQ915136 JQ915110 — [30]
C. shoreae CAL_F_1396 India KY290585 — — [15]
C. sinuosus TF1802 United States U87992 — — [42]
Craterellus sp. MHHNU32154 (FHMU6552) China OL439677 OL439547 PQ641595 [16]
Craterellus sp. N.K. Zeng8042 (FHMU7703) China PQ604690 PQ611013 PQ641596 Present study
C. squamatus Yuan 14520 China MW979534 MW980571 MW999434 [10]
C. squamatus Yuan 14721 China MW979535 MW980570 MW999435 [10]
C. strigosus TH9204 Guyana JQ915134 JQ915108 — [30]
C. strigosus MCA1750 Guyana JQ915120 JQ915094 — [30]
C. striatus HMJAU 61463 (T) China OM509446 — ON125913 [17]
C. striatus HMJAU 61463 China OM509447 — ON125914 [17]
C. tubaeformis DAVFP26257 Canada — HM468491 — [43]
C. tubaeformis UPS-11797 United States AF105311 — — [2]
C. tubaeformis TRTC52516 Belgium — HM468496 — [43]
C. tubaeformis UPSF-11793 Sweden AF105307 — — [2]
C. tubaeformis BB 07.293 Slovakia KF294640 — — [44]
C. tubaeformis TRTC52235 Belgium — HM468497 — [43]
C. tubaeformis BR089347 Canada — HM468493 — [43]
C. tubaeformis OSC-41280 United States AF105313 — — [2]
C. tubaeformis GCB1905 Belgium — MT004784 — [2]
C. tubaeformis UPSF-11795 United States AF105308 — — [2]
Hydnum minus N.K. Zeng2819 (FHMU2461) China KY407528 KY407533 KY407534 [25]
H. cremeoalbum N.K. Zeng2511 (FHMU2153) China KY407527 KY407532 KY407535 [25]
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Bold GenBank numbers highlight the newly generated sequences.

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).

Figure 1.

Figure 1

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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.

3.2. Taxonomy

Craterellus albimarginatus N.K. Zeng, T. Jiang & Xu Zhang, sp. nov.

MycoBank: MB 856885

Figure 2a,b and Figure 3.

Figure 2.

Figure 2

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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 3.

Figure 3

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Microscopic structures of Craterellus albimarginatus (FHMU7715, holotype). (a) Basidiospores. (b) Basidia. (c) Pileipellis. Scale bars: (a–c) = 10 µm. Drawing by T. Jiang.

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.

Figure 4.

Figure 4

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Microscopic structures of Craterellus involutus (FHMU7709, holotype). (a) Basidiospores. (b) Basidia. (c) Pileipellis. Scale bars: (a–c) = 10 µm. Drawing by T. Jiang.

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.

Figure 5.

Figure 5

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Microscopic structures of Craterellus longitipes (FHMU7705, holotype). (a) Basidiospores. (b) Basidia. (c) Pileipellis. Scale bars: (a–c) = 10 µm. Drawing by T. Jiang.

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).

Table 2.

Subgenera and accepted species of Craterellus in China.

Subgenus Species Locality Reference
Cariosi C. lutescens Europe [16]
Craterellus C. croceialbus Liaoning NE China [10]
C. involutus Fujian, SE China Present study
C. macrosporus Liaoning NE China [10]
C. squamatus Liaoning NE China [10]
Imperforati C. albidus Guizhou, SW China [28]
C. albimarginatus Hainan, southern China Present study
C. badiogriseus Liaoning, NE China [10]
Lamelles C. fulviceps Hunan, central China [16]
C. minor Hunan, central China [16]
Ovoidei C. aureus Hong Kong, southern China [16]
C. parvopullus Hainan, southern China [16]
— C. atrobrunneolus Yunnan, SW China [15]
C. connatus/striatus Liaoning, NE China [17]
C. longitipes Fujian, SE China Present study
C. yunnanensis Yunnan, SW China [52]
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SW: southwestern, NE: northeastern, SE: southeastern.

Key to accepted Craterellus taxa in China

1. Absence of obvious demarcation between pileus and stipe 2
1. Presence of obvious demarcation between pileus and stipe 8
2. Pileus colored with vivid yellow to orange C. aureus
2. Pileus colored with gray brown, brown, dark brown to almost black 3
3. Pileal surface covered with scabrous C. squamatus
3. Pileal surface subglabrous to glabrous 4
4. Basidiospores average length <8 µm, occurring in tropical regions C. parvopullus
4. Basidiospores average length >8 µm, occurring in subtropical or temperate regions 5
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 regions C. badiogriseus
6. Basidia shorter (up to 62 µm), pileipellis a trichoderm, and distributed in subtropical regions C. involutus
7. Margin of pileus colored with dark brown, basidiospores larger measuring 12.8–14.5 × 9–11 µm C. macrosporus
7. Margin of pileus colored with orange-white, basidiospores smaller measuring 10–12 × 6.8–8 µm C. croceialbus
8. Basidomata very pale, whitish, grow on dead wood C. albidus
8. Basidomata brown, yellow, grow on ground 9
9. Hyphal clamp connections absent 10
9. Hyphal clamp connections abundant 13
10. Hymenophore slightly veined, white tinged with violet, stipe beige-almond, and distributed in tropical regions C. albimarginatus
10. Hymenophore with well-developed veins, gray, stipe brown, and distributed in subtropical or temperate regions 11
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 regions 12
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 smooth C. lutescens
14. Pileus colored with grayish-yellow to fulvous, hymenophore veined, never smooth 15
15. Hymenophore colored with yellowish, stipe colored with egg-yolk yellow C. fulviceps
15. Hymenophore colored with white to pale, stipe colored with pale lemon yellow C. minor
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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.

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.

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.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Funding Statement

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).

Footnotes

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

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Associated Data

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

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.

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