Diversity of Cantharellus (Cantharellales, Basidiomycota) in China with Description of Some New Species and New Records

Zhang, Ming; Wang, Chao-Qun; Gan, Man-Shui; Li, Yi; Shao, Shi-Cheng; Qin, Wei-Qiang; Deng, Wang-Qiu; Li, Tai-Hui

doi:10.3390/jof8050483

Open AccessArticle

Diversity of Cantharellus (Cantharellales, Basidiomycota) in China with Description of Some New Species and New Records

by

Ming Zhang

¹,

Chao-Qun Wang

¹,

Man-Shui Gan

²,

Yi Li

³,

Shi-Cheng Shao

⁴,

Wei-Qiang Qin

⁵,

Wang-Qiu Deng

¹ and

Tai-Hui Li

^1,*

¹

State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou 510070, China

²

Bureau of Environmental Protection of Dinghai District, Zhoushan Municipality, Zhoushan 316000, China

³

School of Food Science and Engineering, Yangzhou University, Yangzhou 225127, China

⁴

CAS Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, China

⁵

School of Marxism, Jishou University, Zhangjiajie 427000, China

^*

Author to whom correspondence should be addressed.

J. Fungi 2022, 8(5), 483; https://doi.org/10.3390/jof8050483

Submission received: 7 April 2022 / Revised: 28 April 2022 / Accepted: 29 April 2022 / Published: 6 May 2022

(This article belongs to the Special Issue Fungal Taxonomy, Phylogeny, and Ecology: A Themed Issue Dedicated to Academician Wen-Ying Zhuang)

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Abstract

:

Cantharellus is a well-known genus of edible mushrooms, belonging to the family Hydnaceae in the class Agaricomycetes. In this study, a phylogenetic overview of Cantharellus subg. Cinnabarinus and C. subg. Parvocantharellus in China is carried out with the description of four new species. Species description are based on morphological characters of basidiomata and phylogenetic analyses of multi-locus dataset of 28S + tef1 + rpb2. Among the new species, two species, C. chrysanthus and C. sinocinnabarinus, belong to C. subg. Cinnabarinus and two new species, C. convexus and C. neopersicinus, belong to C. subg. Parvocantharellus. Species delimitation characters of the new taxa are compared with closely related species. In addition, three new records of Cantharellus are reported for China: C. albovenosus and C. citrinus of subg. Cinnabarinus and C. koreanus of subg. Parvocantharellus. A key to the species of subg. Cinnabarinus in China was provided.

Keywords:

chanterelle; East Asia; new species; phylogeny; taxonomy

1. Introduction

Cantharellus Fr. was firstly described by Fries [1] based on the type species Cantharellus cibarius Fr. Most Cantharellus species are popular edible mushrooms, especially beloved in Europe. Cantharellus is an ectomycorrhizal genus, forming symbiosis with various plants, such as the trees of Fagaceae, Pinaceae, Betulaceae, Salicaceae, Juglandaceae, Leguminosae, etc. [2,3,4,5,6,7,8]. Species in Cantharellus are widely distributed and are especially rich in subtropical to tropical zones [3,9,10]. Up to now, about 300 species of Cantharellus have been reported worldwide [7]. However, the species diversity is poorly known in Asia in the past decades, and many specimens were named after European or North American species [6,11,12,13]. In recent years, some new species were reported from Asia based on the combination of morphological characters and DNA phylogenetic analyses [6,7,11,12,13,14,15,16]. Recent phylogenetic studies demonstrated that Cantharellus is monophyletic and forms a sister relationship with Craterellus Pers. [3,4,7]. Species in Cantharellus were divided into seven subgenera based on multi-locus phylogenetic analyses in Buyck et al. [3], and a subsequent study in Cao et al. [7]. Cantharellus subg. Cinnabarinus Buyck & V. Hofst., typified by C. cinnabarinus (Schwein.) Schwein. was introduced for a monophyletic assemblage of mostly quite small, yellow, orange, pink or red species, sometimes mixed with lilac-purple or brownish tones in the pileus center, strongly veined in the lamellate hymenophore with principally thin-walled hyphal endings and abundant in clamp connections [3,17,18]. Species in subg. Cinnabarinus are widely distributed in Asia, Europe, North America, Australasia and Africa, and 16 species have been reported worldwide. In China, a large number of Cantharellus species have been reported, but only two species in the subg. Cinnabarinus were recorded, i.e., C. cinnabarinus and C. phloginus, by S.C. Shao & P.G. Liu. Cantharellus cinnabarinus, originally reported from North America, was recorded to be widely distributed in China [19,20,21]; C. phloginus was described as being from southwestern China [22].

In this study, a number of Cantharellus specimens were collected from China; further study proved that they represented eight distinct species, five of which belong to the subg. Cinnabarinus and three to the subg. Parvocantharellus. Four species are described below as new to science, which would make a contribution to understanding the species diversity of Cantharellus in China, and revealing the phylogenetic relationships of Cantharellus species.

2. Materials and Methods

2.1. Morphological Studies

Photographs of fresh basidiomata were taken in the field. Specimens were dried and deposited in the Fungarium of Guangdong Institute of Microbiology (GDGM). Descriptions of macro-morphological characters and habitats were obtained from photographs and field notes. The color codes followed Kornerup and Wanscher [23]. Microscopic observations were carried out on tissue sections stained with 5% aqueous KOH and 1% aqueous Congo red under a light microscope (Carl Zeiss Microscopy GmbH, Göttingen, Germany) with a magnification up to 1000×. For basidiospore descriptions, the notation (a–)b–c(–d) describes basidiospore dimensions, where the range b–c represented 90% or more of the measured values and ‘a’ and ‘d’ were the extreme values; L_m and W_m indicated the average length and width (±standard deviation) of the measured basidiospores, respectively; Q referred to the length/width ratio of an individual basidiospore and Q_m referred to the average Q value of all basidiospores ± sample standard deviation. All line-drawings of microstructures were made based on rehydrated materials.

2.2. DNA Extraction, PCR Amplification and Sequencing

Genomic DNA was extracted from the voucher specimens using the Sangon Fungus Genomic DNA Extraction kit (Sangon Biotech Co., Ltd., Shanghai, China) according to the manufacturer’s instructions. Primer pairs LROR/LR7 [24], tef1F/tef1R and RPB2-5FCanth/RPB2-7cRCanth [3,25] were used to amplify the LSU, tef1 and rpb2 region, respectively. PCR reactions were performed in a total volume of 25 μL containing 0.5 μL template DNA, 11 μL sterile deionized water, 0.5 μL of each primer and 12.5 μL 2 × PCR mix [DreamTaqtm Green PCR Master Mix (2×), Fermentas, USA]. Amplification reactions were performed in a Tprofessional Standard thermocycler (Biometra, Göttingen, Germany) under the following conditions: 95 °C for 4 min; then, 35 cycles of denaturation at 94 °C for 60 s, annealing at 53 °C (LSU)/50 °C (tef1)/52 °C (rpb2) for 60 s and extension at 72 °C for 60 s; with a final extension at 72 °C for 8 min. The PCR products were electrophoresed on 1% agarose gels and then send for sequencing on an ABI Prism^® 3730 Genetic Analyzer (PE Applied Biosystems, Foster, CA, USA) at the Beijing Genomic Institute (BGI) using the same PCR primers. The raw sequences were assembled and checked with SeqMan implemented in Lasergene v7.1 (DNASTAR Inc., Madison, WI, USA). The newly generated sequences in this study were submitted to GenBank.

2.3. Phylogenetic Analyses

Sequences generated in this study and those downloaded from GenBank were combined and used for phylogenetic reconstruction. Detailed information of specimens included in this study was given in Table 1. Three sequence matrices, i.e., nrLSU, tef1 and rpb2, were aligned separately with software MAFFT v6.853 using the E-INS-i strategy [26] and then manually adjusted in MEGA 6 [27]. The ambiguous aligned regions and introns of the two protein-coding genes of tef1 and rpb2 were retained in the final analyses.

Maximum Likelihood (ML) analyses were inferred using RAxML v7.2.6 [28], and all parameters were kept as defaults except for choosing GTRGAMMAI as the model; statistical supports were obtained using rapid non-parametric bootstrapping with 1000 replicates. Bayesian Inference (BI) phylogenies were inferred using MrBayes 3.2.6 [29]; the best models of the multi-locus datasets were searched via the PartitionFinder 2 [30] for each locus, i.e., K80 + I + G, SYM + I + G and SYM + I + G for 28S, tef1 and rpb2, respectively. BI analysis using 4 chains were conducted by setting generations to 20 million and stoprul command with the value of stopval set to 0.01; trees were sampled every 1000 generations, the first 25% generations were discarded as burn-in and posterior probabilities (PP) were then calculated from the posterior distribution of the retained Bayesian trees. Cantharellus cibarius Fr. was selected as the outgroup based on recent studies [3,13]. The phylogenetic trees were visualized using FigTree v1.4.23.

Table 1. Specimen information used in this study. Sequences newly generated in this study are in bold; HT, NT and ET refer to holotype, neotype and epitype, respectively.

Taxa	Voucher	Locality	GenBank Accession No.			Reference
Taxa	Voucher	Locality	LSU	tef1	rpb2	Reference
Cantharellus afrocibarius	BB 96.236	Zambia	KF294669	JX192994	KF294747	[3]
C. afrocibarius	BB 96.235 (HT)	Zambia	KF294668	JX192993	KF294746	[3]
C. albovenosus	1690 (HT)	South Korean	–	KY271942	–	[11]
C. albovenosus	1713	South Korean	–	MW124387	–	[11]
C. albovenosus	GDGM85853	China	OM978952	ON119062	ON119006	Present study
C. albovenosus	GDGM85846	China	OM978950	ON119060	ON119004	Present study
C. albovenosus	GDGM85142	China	OM978949	ON119059	ON229082	Present study
C. albovenosus	HMAS279296	China	OM978948	ON119066	ON119010	Present study
C. albovenosus	HMAS279284	China	ON212414	ON119064	ON119008	Present study
C. albovenosus	HMAS279292	China	ON212412	ON119065	ON119009	Present study
C. albovenosus	HMAS279262	China	OM978947	ON119063	ON119007	Present study
C. albovenosus	GDGM85852	China	OM978951	ON119061	ON119005	Present study
C. albus	HKAS107045 (HT)	China	MT782540	MT776015	MT776012	[12]
C. albus	GDGM81399	China	MZ605074	MZ613977	MZ614022	[13]
C. albus	GDGM81064	China	MZ605073	MZ613976	MZ614021	[13]
C. appalachiensis	GRSM77088	USA	DQ898690	–	DQ898748	[31]
C. appalachiensis	BB 07.123	USA	KF294635	GQ914979	KF294711	[3]
C. aurantinus	GDGM46278 (HT)	China	MZ766517	MZ766560		[13]
C. aurantinus	GDGM46279	China	MZ766518	MZ766561	MZ766571	[13]
C. aurantinus	GDGM81899	China	MZ766520	MZ766563	MZ766573	[13]
C. aurantinus	GDGM84974	China	MZ766521	MZ766564	MZ766572	[13]
C. austrosinensis	GDGM81303	China	MZ605084	MZ613986	MZ614029	[13]
C. austrosinensis	GDGM81249 (HT)	China	MZ605082	MZ613983	MZ614027	[13]
C. austrosinensis	GDGM80616	China	MZ605081	MZ613982	MZ614026	[13]
C. austrosinensis	GDGM81381	China	MZ605086	MZ613988	MZ614031	[13]
C. austrosinensis	GDGM81379	China	MZ605085	MZ613987	MZ614030	[13]
C. austrosinensis	GDGM81985	China	MZ605087	MZ613989	MZ614032	[13]
C. chrysanthus	GDGM45166	China	OM978959	ON119074	ON119011	Present study
C. chrysanthus	GDGM45937	China	OM978960	ON119075	ON119012	Present study
C. chrysanthus	GDGM85298	China	OM978975	ON119089	ON119025	Present study
C. chrysanthus	GDGM85305	China	OM978976	ON119090	ON119026	Present study
C. chrysanthus	GDGM53485	China	OM978962	ON119077	ON119014	Present study
C. chrysanthus	GDGM80220 (HT)	China	OM978970	ON119083	ON119019	Present study
C. chrysanthus	GDGM82511	China	OM978973	ON119087	ON119023	Present study
C. chrysanthus	GDGM82516	China	OM978974	ON119088	ON119024	Present study
C. chrysanthus	GDGM80436	China	OM978971	ON119084	ON119020	Present study
C. chrysanthus	GDGM80202	China	OM978965	ON119080	ON119016	Present study
C. chrysanthus	GDGM80204	China	OM978966	ON119081	ON119017	Present study
C. chrysanthus	HMAS279434	China	ON212413	ON119091	ON229079	Present study
C. chrysanthus	GDGM80438	China	–	ON119085	ON119021	Present study
C. chrysanthus	GDGM82473	China	OM978972	ON119086	ON119022	Present study
C. chrysanthus	GDGM77035	China	OM978964	ON119079	ON229081	Present study
C. chrysanthus	GDGM60524	China	OM978963	ON119078	ON119015	Present study
C. chrysanthus	GDGM80217	China	OM978969	ON119082	ON119018	Present study
C. chrysanthus	GDGM49628	China	OM978961	ON119076	ON119013	Present study
C. chrysanthus	GDGM87950	China	OM978968	–	ON119027	Present study
C. chrysanthus	GDGM87951	China	OM978967	–	ON119028	Present study
C. cibarius	GE 07.025	France	KF294658	GQ914949	KF294736	[3]
C. cibarius	BB 07.300	Slovakia	KF294641	GQ914950	KF294718	[3]
C. cinnabarinus	BB 04.263 (NT)	USA	–	GQ914983	–	[32]
C. cinnabarinus	BB 07.053	USA	KF294630	GQ914984	KF294705	[32]
C. cinnabarinus	BB 07.001	USA	KF294624	GQ914985	KF294698	[32]
C. citrinus	1691 (HT)	South Korean	–	MW124385	–	[16]
C. citrinus	1715	South Korean	–	MW124388	–	[16]
C. citrinus	1710	South Korean	–	MW124386	–	[16]
C. citrinus	1711	South Korean	–	MW124384	–	[16]
C. citrinus	GDGM86140	China	OM978955	ON119070	ON119032	Present study
C. citrinus	GDGM86141	China	OM978956	ON119071	ON119033	Present study
C. citrinus	GDGM80825	China	–	ON119069	ON119031	Present study
C. citrinus	GDGM86142	China	OM978957	ON119072	ON119034	Present study
C. citrinus	GDGM80724	China	OM978954	ON119068	ON119030	Present study
C. citrinus	GDGM86143	China	OM978958	ON119073	ON119035	Present study
C. citrinus	GDGM80723	China	OM978953	ON119067	ON119029	Present study
C. coccolobae	1064_RC. 14_24	Guadeloupe	KX857088	KX857020	KX856992	[33]
C. coccolobae	1065_RC. 11_25 (HT)	Guadeloupe	KX857089	KX857021	KX856993	[33]
C. congolensis	1645/BB16.044	Saharan Africa	KX857102	KX857075	KX857006	[33]
C. congolensis	1676/BB16.123	Saharan Africa	KX857106	KX857078	KX857010	[33]
C. aff. congolensis	BB 06.176	Madagascar	KF294606	–	KF294680	[3]
C. aff. congolensis	BB 06.197	Madagascar	KF294608	–	KF294683	[3]
C. convexus	GDGM54841	China	OM978940	ON119052	ON119036	Present study
C. convexus	GDGM70307 (HT)	China	OM978941	ON119053	ON119037	Present study
C. corallinus	1083_JJ_MO_CANT_2	USA	–	KX857031	–	[34]
C. corallinus	1086_JJ_MO_CANT_5	USA	–	KX857034	–	[34]
C. corallinus	FLAS_F_61106	USA	–	MK045368	–	[34]
C. curvatus	BRNM:825749 (HT)	South Korea		MW124390		[16]
C. cyphelloides	TNS F-61721 (HT)	Japan	NG059027	–	–	[35]
C. decolorans	BB 08.278 (HT)	Madagascar	KF294654	GQ914968	KF294731	[3]
C. fistulosus	DT_43	Tanzania	JQ976965	JX192997	–	[3]
C. friesii	AH44798	Spain	KR677522	KX828831	KX828752	[36]
C. friesii	VDKO 1165	Africa	–	KX834408	KX881922	[5]
C. galbanus	GDGM86249 (HT)	China	ZM766516	MZ766568	MZ766577	[13]
C. garnierii	BB 09.024	New Caledonia	KX857085	KX857017	KX856989	[34]
C. garnierii	BB 09.283	New Caledonia	KX857087	KX857019	KX856991	[34]
C. garnierii	BB 09.033	New Caledonia	KX857086	KX857018	KX856990	[34]
C. garnierii	RF33	New Caledonia	AY392768	–		[37]
C. garnierii	RF32	New Caledonia	AY392767	–		[37]
C. koreanus	1697	South Korea	–	KY271940	–	[11]
C. koreanus	1689 (HT)	South Korea	–	KY271941	–	[11]
C. koreanus	GDGM85306	China	OM978978	ON119093	ON229077	Present study
C. koreanus	GDGM79233	China	OM978977	ON119092	ON229078	Present study
C. koreanus	1693	South Korea	–	–		Unpublished
C. koreanus	1694	South Korea	–	–		Unpublished
C. koreanus	1696	South Korea	–	–		Unpublished
C. luteolus	GDGM60393 (HT)	China	ZM766515	MZ766566	MZ766575	[13]
C. luteolus	GDGM86247	China	MZ766513	MZ766567	MZ766576	[13]
C. luteolus	GDGM44258	China	ZM766514	MZ766566	MZ766570	[13]
C. luteovirens	GDGM81079	China	MZ605092	MZ613994	MZ614036	[13]
C. luteovirens	GDGM80672 (HT)	China	MZ605090	MZ613992	MZ614035	[13]
C. luteovirens	GDGM80680	China	MZ605091	MZ613993	–	[13]
C. minioalbus	GDGM78910	China	MZ605098	MZ613999	MZ614043	[13]
C. minioalbus	GDGM78901 (HT)	China	MZ605097	MZ613998	MZ614042	[13]
C. minioalbus	GDGM78916	China	MZ605100	MZ614001	MZ614045	[13]
C. minor	BB 07.057	USA	KF294632	JX192979	KF294707	[3]
C. minor	BB 07.002	USA	KF294625	JX192978	KF294699	[3]
C. neopersicinus	GDGM85145-1	China	OM978942	ON119054	ON119039	Present study
C. neopersicinus	GDGM85145-2	China	OM978945	ON119055	ON119040	Present study
C. neopersicinus	GDGM85145-3	China	OM978946	ON119056	ON119041	Present study
C. neopersicinus	GDGM87366-1 (HT)	China	OM978943	ON119057	ON119042	Present study
C. neopersicinus	GDGM87366-2	China	OM978944	ON119058	ON119043	Present study
C. phloginus	GDGM79007-1	China	OM978979	ON119094	ON119044	Present study
C. phloginus	GDGM79007-2	China	OM978980	ON119095	ON119045	Present study
C. phloginus	SSC99 (HT)	China	–	KF801096	–	[22]
C. phloginus	SSC98	China	–	KF801095	–	[22]
C. phloginus	Yuan14468	China	–	MW999424.	–	[7]
C. phloginus	Yuan14490	China	–	MW999425	–	[7]
C. phloginus	GDGM82514	China	–	ON119096	–	Present study
C. pseudominimus	JV 00.663	Portugal	KF294657	JX192991	KF294735	[3,10]
C. romagnesianus	AH44218	Spain	KX828807	KX828836	KX828757	[36]
C. roseofagetorum	AH44789	Georgia	KX828812	KX828839	KX828760	[36]
C. sinocinnabarinus	GDGM83229	China	OM978983	ON119098	ON119047	Present study
C. sinocinnabarinus	GDGM83238	China	OM978985	ON119101	ON119051	Present study
C. sinocinnabarinus	GDGM83023	China	OM978981	ON119097	ON119050	Present study
C. sinocinnabarinus	GDGM83232	China	–	ON119100	ON119049	Present study
C. sinocinnabarinus	GDGM83027	China	OM978982	–	ON119046	Present study
C. sinocinnabarinus	GDGM83230 (HT)	China	OM978984	ON119099	ON119048	Present study
C. sinocinnabarinus	HKAS58243	China	JF906727	–	–	[20]
C. sinominor	GDGM80788	China	MZ605105	MZ614004	MZ614048	[13]
C. sinominor	GDGM80842 (HT)	China	MZ605107	MZ614006	MZ614050	[13]
C. sinominor	GDGM80885	China	MZ605108	MZ614007	MZ614051	[13]
C. aff. subcyanoxanthus	BB 98.014	Tanzania	KF294615	JX192973	KF294689	[3]
C. tabernensis	BB 07.119	USA	KF294634	GQ914976	KF294709	[3]
C. tabernensis	BB 07.056 (ET)	USA	KF294631	GQ914974	KF294706	[3,38]
C. texensis	341/O7.120	USA	JN940601	GQ914987	KF294710	[3]
C. texensis	BB 07.018	USA	KF294626	GQ914988	KF294701	[3]
C. xanthocyaneus	1751	Congo	MT006309	MT002277	–	[39]
C. xanthocyaneus		Congo	MT006310	MT002278	–	[39]
C. zangii	GDGM82389	China	MZ605110	MZ614009	MZ614053	[13]
C. zangii	GDGM82393	China	MZ605111	MZ614010	MZ614054	[13]
C. zangii	GDGM82374	China	MZ605109	MZ614008	MZ614052	[13]

3. Results

3.1. Molecular Phylogeny

For phylogenetic analyses, a total of 152 sequences were newly produced in this study, containing 49 nrLSU, 51 tef1 and 52 rpb2, and 185 reliable sequences were downloaded from the GenBank database based on previous studies [3,13]. The combined dataset (LSU + tef1 + rpb2) contained 2892 characters (1311, 707 and 874 for LSU, tef1 and rpb2, respectively), of which 2013 were conserved and 708 were parsimony-informative. ML and BI analyses of the concatenated data set resulted in almost identical topologies, and no strongly-supported conflicts between ML and BI analyses were discovered; thus, only the tree inferred from ML analysis was displayed (Figure 1). Our phylogenetic analyses indicated that members of C. subg. Cinnabarinus formed a highly support monophyletic group (MLB/BPP = 100%/1.0). Five well-supported clades in the subg. Cinnabarinus were identified based on samples newly collected from China, including two new species, two species newly recorded in China and a known species in China. Besides, three well-supported clades in the subg. Parvocantharellus were firstly discovered in China, containing two new species and a newly recorded species from China.

3.2. Taxonomy

3.2.1. Cantharellus subgen. Cinnabarinus Buyck & V. Hofst.

Cantharellus chrysanthus Ming Zhang, C.Q. Wang & T.H. Li sp. nov.; Figure 2 and Figure 3.

MycoBank: MB843657.

GenBank: OM978970 for LSU, ON119083 for tef1 and ON119019 for rpb2.

Etymology—refers to the color of pileus similar to the yellow chrysanthemum flower.

Diagnosis—This species is characterized by its orange to orange-yellow pileus, pinkish white to orange white hymenophore, thin-walled pileipellis terminal hyphae, broadly ellipsoid basidiospores (7.5–9 × 5–6.5 μm) and long basidia up to 100 μm.

Type—CHINA. Guangdong Province, Shaoguan City, Ruyuan town, Nanling National Natural Reserve, alt. 500 m, 10 June 2020, Ming Zhang (GDGM80220).

Basidiomata small-sized. Pileus 20–60 mm broad, convex, with involute margin when young, then gradually to nearly applanate or broadly infundibuliform with depressed center and inflexed to straight, irregularly undulate or slightly cracked at maturity; surface dry or hygrophanous, glabrous or finely subtomentose, orange (5A7–6A7) to deep orange (5A8–6A8) when young, slightly fading to orange yellow to yellow (3A7–4A7) when mature. Context yellowish white to orange white (4A2–6A2), 1–2 mm thick in the center of the pileus, sharply attenuate towards margin, unchanging when exposed. Hymenophore decurrent, subdistant, composed of bifurcate, 2–3 mm high venose folds, particularly towards pileus margin, pinkish white (7A2–10A2), but in some specimens yellowish white to orange white, unchanging when bruised. Stipe 20–60 × 3–14 mm, central, cylindrical or slightly tapering towards base, solid, glabrous or finely pubescent, concolorous with pileus or paler, unchanging when handled. Odor fruity and pleasant. Taste mild.

Basidiospores 7.5–9 × 5–6.5 μm, L_m × W_m = 8.45(±0.47) × 5.98(±0.42) μm, Q = (1.25)1.28–1.6(1.64), Q_m = 1.42 ± 0.1; broadly elliptical to subglobose, smooth, guttulate, thin-walled. Basidia 55–100 × 7–11 μm, 2–6-spored, narrowly clavate, colorless to hyaline in KOH; sterigmata 6–10 μm long. Pileipellis a cutis with long, repent and occasionally interwoven hyphae, subcylindrical cells that are 6–12 μm wide, thin-walled. Stipitipellis a cutis of cylindrical, parallel hyphae, 3–8 μm wide. Clamp connections abundant in all tissues.

Habitat and distribution—Solitary or scattered under Fagaceae trees mixed with other broadleaf trees in subtropical forests. Known from southern and southwestern China.

Additional specimen examined—China. Guangdong Province, Shaoguan City, Ruyuan town, Nanling National Natural Reserve, alt. 500 m, 7 June 2017, Ming Zhang (GDGM49628); same location, alt. 500 m, 21 July 2017, Ming Zhang (GDGM60524); same location, alt. 500 m, 9 June 2020, Ming Zhang (GDGM80436, GDGM80438); same location, alt. 500 m, 10 June 2020, Ming Zhang (GDGM80202, GDGM80204, GDGM80217, GDGM80220,); Huizhou city, Xiangtoushan National Natural Reserve, alt. 550 m, 17 May 2016, Ting Li (GDGM45937); Hunan Province, Rucheng town, Jiulongjiang National Forest Park, alt. 300 m, 4 September 2016, Ming Zhang (GDGM53485); Zhejiang province, Jinhua city, Wuyi Town, 23 August 2015, Tai-Hui Li (GDGM45166); Hangzhou City, Laohushan, 15 July 2021, Bao-Juan Ling (GDGM85298, GDGM85305); Qingyuan Town, Baishanzu National Natural Reserve, alt. 29 July 2020, Tai-Hui Li (GDGM82473); Longquan City, Fengyangshan National Natural Reserve, 25 August 2016, Rui-Lin Zhao (ZRL20161616, HMAS279434); Quzhou City, Kaihua County, He Tian township, Chi Keng village, 24 May 2021, Yi Li (GDGM87950); Quzhou City, Kaihua County, Shengtangou Scenic Spot, 30 May 2021, Yi Li (GDGM87951); Anhui Province, Huangshan City, Huangshan scenic spot, 11 August 2020, Ming Zhang (GDGM82511), same location, 13 August 2020, Ming Zhang (GDGM82516); Guizhou Province, Guiyang City, Longli County, Guanyin Village, bought from a wild mushroom market, 2 August 2019, alt. 1000 m, Yong He (GDGM77035).

Notes—Cantharellus chrysanthus is different from other Cantharellus species by the combined features of the orange to orange-yellow pileus, the pinkish white to orange white hymenophore, the thin-walled terminal hyphae of pileipellis, the broadly ellipsoid basidiospores (7.5–9 × 5–6.5 μm) and the long basidia up to 100 μm.

Phylogenetically, C. chrysanthus is related to C. albovenosus and C. phloginus in the analyses of the multi-locus datasets. However, C. albovenosus differs in its orange to reddish orange pileus with tomentoum or fibrilla, white to orange white and better-developed hymenophore, orange to reddish orange stipe, smaller basidiospores (7–8.5 × 5–6 μm) and shorter basidia (48–63 × 7–9 μm) [11]; Cantharellus phloginus, reported from southwest China, differs in its pastel red to pastel pink pileus and stipe, pale yellow to light yellow hymenophore, larger basidiospores [6.8–9.5 (–12) × 5–7 μm] and shorter basidia (60–95 × 8–10 μm) [22].

Cantharellus sinocinnabarinus Ming Zhang, S.C. Shao & T.H. Li sp. nov.; Figure 4 and Figure 5.

MycoBank: MB843658.

GenBank: OM978984 for LSU, ON119099 for tef1 and ON119048 for rpb2.

Etymology—Refers to the species distributed in China and is similar to C. cinnabarinus in morphology.

Diagnosis—This species is characterized by its small basidiomata, reddish orange to yellowish red pileus covered with white minute fibrils, yellowish orange to orange hymenophore and elongate elliptical basidiospores measuring (6.5–) 7–8 (9) × (4.5) 5–6 μm.

Type—China. Yunnan Province, Lijiang City, Yulong County, Jiuhe Village, 1 September 2020, alt. 2400 m, Ming Zhang (GDGM83230).

Basidiomata small-sized. Pileus 5–15 mm broad, applanate with a depressed center, not perforate; margin slightly incurved when young, applanate to reflexed with age; surface dry, orange, reddish orange to yellowish red (6A7–8A7), locally with white minute fibrils. Context thin, 0.5–1.5 mm thick, fleshy to fibrous, yellowish orange to reddish orange, unchanging when bruised. Hymenophore subdecurrent, with a clearly delimitation from stipe surface; lamellate ridges subdistant to close, well-developed, 1–2 mm high, appropriately bifurcate, with low interconnected low venose folds, particularly at pileus margin, yellowish orange to orange (4A7–6A7), unchanging when bruised. Stipe 10–15 mm long, 1–2.5 mm thick, subcylindrical, slightly tapering downward, glabrous or with obscure white minute fibrils, hollow, concolorous with pileus. Odor pleasant.

Basidiospores (100/4/4) (6.5)7–8(9) × (4.5)5–6 μm, L_m × W_m = 7.47(±0.5) × 5.21(±0.39) μm, Q = (1.25)1.27–1.6(1.67), Q_m = 1.43 ± 0.09; elliptical to elongate elliptical. Basidia 50–75 × 10–12 μm, clavate, with 4–8 sterigmata. Pileipellis a cutis, composed of procumbent hyphae; hyphae 4–13 μm in diam., colorless, thin-walled. Hymenophoral trama composed of cylindrical hyphae 5–10 μm in diam. Stipitipellis a cutis, composed of procumbent, branched hyphae; hyphae 4–12 μm in diam., mostly 7 μm in diam. Cystidia absent. Clamp connections common.

Habitat and distribution—Gregarious on soil in subalpine mixed forest dominated by Cyclobalanopsis delavayi (Franch.) Schott. and Pinus yunnanensis Franch. Currently known from southwest China.

Additional specimens examined—China. Yunnan Province, Jianchuan County, Qianshi Mountain, 7 September 2009, alt. 2491 m, Yu23 (HKAS58243); Lijiang City, Yulong County, Jiuhe Village, 1 September 2020, alt. 2400 m, Ming Zhang (GDGM83229, GDGM83232, GDGM83027), Li-Qiang Wu (GDGM83238).

Notes—Cantharellus sinocinnabarinus can be easily recognized in the field by its small reddish orange basidiomata. Morphologically, C. sinocinnabarinus is similar to C. cinnabarinus, C. persicinus R.H. Petersen and C. texensis. However, the latter three species were all originally reported from North America; C. cinnabarinus and C. persicinus differ in their larger basidiomata (pileus up to 40 mm), thicker-walled hyphae of pileipellis terminal cells, and different sizes of basidiospores (6.7–7.57 × 3.82–4.68 μm for C. cinnabarinus, and 10.2–11.9 × 6.3–7.2 μm for C. persicinus) [32]; C. texensis differs in its robust basidiomata and longer but narrower basidiospores (8–8.95 × 3.7–4.3 μm), with a larger Q value (1.8–2.2) [32].

Shao et al. [20] has described a specimen (HKAS58243) under the name C. cinnabarinus on the basis of the LSU sequence, which is geographically close to C. sinocinnabarinus in southwest China. In this study, the specimen (HKAS58243) was re-examined; the morphological features and molecular phylogenetic analyses all demonstrated that it is actually C. sinocinnabarinus.

In the multi-locus phylogentic trees, specimens of C. sinocinnabarinus formed a well-supported independent terminal branch (BS = 100%, BPP = 1.0) in the subg. Cinnabarinus, and are closely related to C. cinnabarinus. However, they can be easily distinguished by the morphological features and large genetic distance.

Cantharellus albovenosus Buyck, Antonín & Ryoo, in Antonín, Hofstetter, Ryoo, Ka and Buyck, Mycol. Progr. 16(8): 757 (2017); Figure 6 and Figure 7.

Basidiomata small-sized. Pileus 20–55 mm broad, convex at first, then broad applanate with a depressed centre, subinfundibuliform when mature or old; margin inflexed to straight when young, then undulate; surface tomentose when young, then glabrescent and radially (innately) fibrillose to finely striate and rugulose, orange, deep orange to reddish orange (5A6–7A6, 5A8–7A8), then pallescent to light orange at margin. Hymenophore decurrent, with a clearly delimitation from stipe surface; lamellate ridges, subdistant to distant, relatively well-developed, 1–1.5 mm high, appropriately bifurcate and interconnected with low veined folds, particularly towards pileus margin, white to orange white (5A2–6A2), unchanging when bruised. Stipe 25–50 × 2.5–9 mm, cylindrical and slightly clavate to bulbose at base, finely tomentose when young, then glabrous or with finely longitudinally fibrillose, concolorous with pileus, orange to reddish orange, sometimes paler to light orange in some specimens. Context white, orangish under pileipellis, solid, becoming hollow-fibrous in stipe. Odor spicy. Taste mild.

Basidiospores 7–8.5 × 5–6 μm, L_m × W_m = 7.9(±0.48) × 5.5(±0.34) μm, Q = (1.33)1.4–1.5(1.54), Q_m = 1.44 ± 0.05; ellipsoid to subglobose, thin-walled, sometimes with granulose contents. Basidia 48–63 × 7–9 μm, 2–6-spored, clavate, sometimes subcapitate. Hymenial trama hyphae cylindrical to subinflated, sometimes irregular, thin-walled, 3–8 μm wide. Pileipellis a cutis composed of cylindrical, rarely subinflated, thin-walled, 4–10 μm wide hyphae; terminal cells 37–87 × 5–8 μm, adpressed, cylindrical, clavate or subfusoid. Stipitipellis a cutis of cylindrical, parallel, thin-walled, clamped, 3–7 μm wide hyphae.

Habitat and distribution—Scattered or gregarious on soil under mixed forest dominated by Fagaceae trees. Known to be from eastern China and Korea.

Specimens examined—China. Jiangsu Province, Nanjing City, Purple Mountain, 19 June 2021, alt. 150 m, Zi-Hang Zhang (GDGM85846); same location, 28 June 2021, Zi-Hang Zhang (GDGM85852, GDGM85853); Anhui Province, Huangshan National Scenic Area, 26 August 2021, alt. 1400 m, Chen-Jie Jiang (GDGM85142). Zhejiang Province, Lishui City, Jingning Town, Wangdongyang Alpine Wetland Nature Reserve 22 September 2016, Rui-Lin Zhao (HMAS279296, HMAS279292); same location, 23 September 2016, Rui-Lin Zhao (HMAS279262, HMAS279284).

Notes—Cantharellus albovenosus, recently reported from South Korea, is characterized by the combined features of the orange to reddish orange pileus, white to orange white and relatively well-developed lamellate hymenophore, the orange to reddish orange stipe, and the ellipsoid to nearly globose basidiospores (7–8.5 × 5–6 μm) [11]. Phylogenetically, C. albovenosus and C. phloginus clustered together in an almost similar phylogenetic position, and cannot be separated in our multi-locus phylogenetic tree (Figure 1). Morphologically, C. phloginus can be distinguished by its pastel red to pastel pink pileus and stipe, pale yellow to yellowish orange hymenophore and large basidiospores [6.8–9.5 (–12) × 5–7 μm] [22]. Ecologically, C. albovenosus is known from subtropical regions of South Korea and eastern China; meanwhile, C. phloginus is currently only known from tropical regions of southwest China. The distinguishable morphological features and different growth habits supported them as two distinct species, but some more effective molecular markers are needed to distinguish the two species.

Cantharellus citrinus Buyck, R. Ryoo & Antonín, in Buyck, Hofstetter, Ryoo, Ka and Antonín, MycoKeys 76: 35 (2020); Figure 8 and Figure 9.

Basidiomata small-sized. Pileus 15–45 mm broad, convex, with involute margin when young, then gradually to broadly infundibuliform with depressed center, irregularly undulate or slightly cracked margin when old; surface dry or hygrophanous, glabrous or finely subtomentose, greenish yellow, light yellow, yellow to yellowish orange (1A4–4A4, 1A7–4A7). Context yellowish white, 1 mm thick in the center of the pileus, sharply attenuate towards margin, unchanging when exposed. Hymenophore decurrent, subdistant, composed of bifurcate, less than 1 mm high veined folds, particularly towards pileus margin, white to yellowish white (1A2–3A2), unchanging when bruised. Stipe 15–30 × 3–5 mm, central, cylindrical or slightly tapering towards base, hollow, glabrous, concolorous with pileus or paler, unchanging when handled. Odor fruity and pleasant. Taste mild.

Basidiospores 7–9 × 5–6(6.5) μm, L_m × W_m = 7.77(±0.47) × 5.29(±0.40) μm, Q = (1.17)1.23–1.6(1.64), Q_m = 1.47 ± 0.11; broadly elliptical to subglobose, smooth, guttulate, thin-walled. Basidia 55–65 × 7–8 μm, 4–6-spored, narrowly clavate, colorless to hyaline in KOH; sterigmata 5–10 μm long. Pileipellis a cutis with long, repent and occasionally interwoven hyphae, subcylindrical cells that are 5–15 μm wide, thin-walled. Stipitipellis a cutis of cylindrical, parallel hyphae, 5–10 μm wide. Clamp connections abundant in all tissues.

Habitat and distribution—Gregarious on soil under mixed forests in southwest China. Known from southwest China and Korea.

Specimen examined—China. Guizhou Province, Guiyang City, Longli County, Guanyin Village, bought from a wild mushroom market, 1 July 2020, alt. 1000 m, Ming Zhang (GDGM80825); Same location, 16 June 2020, Ting Li (GDGM80724, GDGM80723); 7 July 2021, Ming Zhang (GDGM86140, GDGM86141, GDGM86142, GDGM86143).

Notes—Cantharellus citrinus, recently reported from Korea [11], is characterized by its small basidiomata, greenish yellow to yellowish orange pileus, white to yellowish white hymenophore strongly bifurcate at pileus margin, glabrous and hollow stipe, and broadly elliptical to subglobose basidiospores [7–9 × 5–6 (6.5) μm]. In the multi-locus phylogentic tree, samples of C. citrinus formed a well-supported monophyletic terminal clade, and can be easily distinguished from other Cantharellus species.

Morphologically, C. citrinus might be easily identified as a species in the subg. Parvocantharellus by the small basidioma with a greenish yellow to yellowish orange pileus, and similar to C. galbanus Ming Zhang, C.Q. Wang & T.H. Li and C. luteovirens Ming Zhang, C.Q. Wang & T.H. Li. However, C. galbanus, recently reported from tropical China, differs in its smaller basidiomata, relatively well-developed hymenophore, and smaller basidiospores (6–7.5 × 4.8–5.5 µm) [13]; C. luteovirens, recently reported from subtropical China, differs in its yellow to yellowish-orange pileus, yellowish white to pale yellow hymenophore and smaller basidiospores (6–7.5 × 4.5–6 µm) [13].

Cantharellus phloginus S.C. Shao & P.G. Liu, in Shao, Buyck, Tian, Liu and Geng, Mycoscience 57(2): 146 (2016); Figure 10 and Figure 11.

Basidiomata small to medium-sized. Pileus 20–60 mm broad, applanate with a concave center, margin incurved at first, then becoming applanate or slightly reflexed with age, glabrous, pastel red to pastel pink (7A4–11A4); Context 2–3 mm thick, white, with pinkish hues under pileipellis, unchanging when bruised; Hymenophore decurrent, well-developed, lamellate ridges with anastomosing veins, forking towards pileus margin, pale yellow to light yellow (3A3–4A3), unchanging when touched. Stipe 20–40 × 4–8 mm, central, solid, subcylindrical, or slightly tapering towards base, glabrous, concolorous with pileus or paler to pinkish with yellowish hues, unchanging when handled. Odor fruity. Taste pleasant.

Basidiospores 6.8–9.5 (–12) × 5–7 μm, L_m × W_m = 8.49(±1.09) × 5.71(±0.69) μm, Q = (1.33)1.36–1.6(1.7), Q_m = 1.49 ± 0.18; broadly ellipsoid to subglobose, smooth, guttulate. Basidia 60–95 × 8–10 μm, 2–6-spored, narrowly clavate, colorless to hyaline in KOH; sterigmata 3–7 μm long. Hymenophoral trama composed of cylindrical interwoven hyphae 3–13 μm in diam. Pileipellis a subcutis, composed of long, repent, branched, and slightly interwoven hyphae, with subcylindrical cells in 3–13 μm wide, thin-walled. Clamp connections abundant in all tissues.

Habitat and distribution—Gregarious or caespitose under mixed forests, dominated by Pinus sp. and Castanopsis in the tropical forest. Currently known to be southwest China.

Specimens examined—China. Yunnan Province, Puer City, alt. 1500 m, 26 August 2009, S.C. Shao 98 (HKAS58208, holotype); Puer City, bought from a mushroom market, alt. 1500 m, 28 September 2019, Ming Zhang (GDGM79007).

Notes—Cantharellus phloginus, recently reported from southwest China, is characterized by its pastel red to pastel pink pileus and stipe, pale yellow to yellowish orange, well-developed hymenophore, and ellipsoid basidiospores [6.8–9.5 (–12) × 5–7 μm] [22]. Morphologically, C. phloginus is similar to C. cinnabarinus and C. texensis Buyck & V. Hofst with the pinkish red pileus color. However, C. cinnabarinus differs in its small basidiomata, reddish pink pileus, small basidiospores [(6.4) 6.7–7.5 (8.1) × (3.7) 3.8–4.6 (5.2) μm] and thick-walled pileipellis [32]; C. texensis differs in its slender basidiomata, reddish pink pileus, relatively well developed hymenophore, small basidiospores [8–8.95 (9.4) × (3.3) 3.7–4.3 μm], and thinner-walled pileipellis that is faintly covered with zebroid incrustation [32]. Ecologically, C. phloginus occurs under trees of Pinus sp. and Castanopsis sp. in tropical regions of southwest China, while C. cinnabarinus and C. texensis occur on sandy loam in oak-pine forests in temperate regions of North America [32].

3.2.2. Cantharellus subgen. Parvocantharellus Eyssart. & Buyck

Cantharellus convexus Ming Zhang & T.H. Li sp. nov.; Figure 12 and Figure 13.

MycoBank: MB843659.

GenBank: OM978941 for LSU, ON119053 for tef1 and ON119037 for rpb2.

Etymology— “convexus” refers to the convex of the pileus center.

Diagnosis—This species can be easily distinguished from others in Cantharellus by its small basidiomata, yellowish white pileus, distant and well-developed lamellate hymenophore with or without bifurcate low veins and smaller basidiospores at 6–7 × 4.5–5 μm.

Type—China. Guangdong Province, Shaoguan City, Nanling National Nature Reserve, alt. 800 m, 29 July 2017, Ming Zhang (GDGM70307).

Basidiomata small-sized. Pileus 5–12 mm broad, convex when young, then gradually to nearly applanate with a central shallow depression at maturity; surface dry, tomentosus, mostly yellowish white, pale yellow to pale orange (2A2, 2A3–5A3), but in some specimens can be yellowish brown to brown, with a deeper center to olive brown to yellowish brown (4E5–5E5); margin wavy, incurved when young, decurved to slightly upturned at maturity, unchanging when handled. Context yellowish white, thin, unchanging when exposed. Hymenophore decurrent, lamellate ridges distant, relatively well developed, occasionally forking towards pileus margin, with or without bifurcate low veins between ridges, yellowish white to pale yellow (2A2–4A2, 2A3–4A3), unchanging when bruised. Stipe 10–20 × 1.5–3 mm, central, cylindrical or slightly tapering towards base, glabrous or faintly scaly, concolorous with pileus or paler, unchanging when handled. Odor not distinct.

Basidiospores (50/2/2) 6.0–7.0 × 4.5–5.0 μm, L_m × W_m = 5.71(±0.64) × 4.87(±0.49) μm, Q = (1)1.1–1.27(1.37), Q_m = 1.17 ± 0.07, broadly ellipsoid to subglobose, smooth, guttulate. Basidia 32–50 × 7–9 μm, 4–6-spored, narrowly clavate, colorless to hyaline in KOH, sterigmata 3–7 μm long. Hymenophoral trama irregular, composed of colorless and branched hyphae, 5–22 μm wide, septate, thin-walled. Pileipellis a cutis with long, repent, branched, and usually interwoven hyphae consisting of subcylindrical cells in 3–15 μm wide, thin-walled; terminal cells appressed to suberect, mostly cylindrical, up to 110 μm long, 5–15 μm wide. Stipitipellis a cutis of cylindrical, parallel hyphae, 3–10 μm wide; terminal cells clavate or cylindrical. Clamp connections abundant in all tissues.

Habitat and distribution—Gregarious or scattered under broadleaf forests (dominated by Fagaceae trees) in subtropical China. Currently known from Guangdong and Hunan Province, Southern China.

Additional specimens examined—China. Hunan Province, Chenzhou City, Sanjiangkou Town, Jiulongjiang National Forest Park, under Castanopsis hystrix mixed with other broadleaf trees, alt. 200 m, 3 August 2017, Ming Zhang (GDGM54841).

Notes—Cantharellus convexus is characterized by its small basidiomata, convex pileus covered with fibrillose scales, distant and well-defined lamellate hymenophore without anastomosis between the folds, broad elliptic to subglobose basidiospores and thin-walled hyphae of the pileipellis. These traits taxonomically enable the placement of C. convexus into subg. Parvocantharellus.

Phylogenetically, two specimens of C. convexus formed an isolated lineage in subg. Parvocantharellus, and are closely related to C. tabernensis. A BLAST result of ITS sequence in the GenBank database also demonstrated that the similarity between C. convexus and C. tabernensis (JN944012, O7.064) is 93.7%. However, C. tabernensis, originally reported from North America, differs in its more robust basidiomata, dull orange-yellow to yellowish-brown pileus, vivid orange-yellow hymenophore and stipe and larger basidiospores (6–9 × 4.4–5.9 µm) [40]. Additionally, C. tabernensis, currently only known from Texas, Louisiana and Mississippi in North America, occurs in well-drained (sandy) soil in mixed woods, and near to Pinus elliottii Engelm. Meanwhile, C. convexus was found in broadleaf forests in southern China, close to Fagaceae trees. Another North America species, C. appalachiensis, also demonstrates a close relationship with C. convexus. However, C. appalachiensis differs in its larger and more robust basidiomata, with a drab yellow to dull brown pileus applanate with the center depressed, surface locally dull-grayish due to aggregate minute fibrils and with larger basidiospores (6.6–8.9 × 4.4–5.9 µm) [41,42].

Morphologically, C. convexus is similar to C. austrosinensis Ming Zhang, C.Q. Wang & T.H. Li, C. koreanus Buyck, Antonín & Ryoo and C. luteovirens. However, C. austrosinensis differs in its pastel yellow to greyish-yellow pileus, usually with a greyish-orange to brownish-orange center, broader basidiospores (6–8 × 4.8–6 µm) and strictly associated with coniferous trees (Pinus massoniana) [13]; C. koreanus, originally described from the temperate region of the Republic of Korea, differs in its dirty yellow-brown to pale brown pileus usually with a brown to dark brown center and larger basidiospores [6–8 (–9) × 4.2–5.5 (–6.5) μm] [11]; C. luteovirens differs in its yellow to orange pileus, greyish-yellow to greyish-orange hymenophores, broadly ellipsoid to subglobose basidiospores (7–8 × 5.2–6.5 μm) and is currently only found be associated with Acacia trees [13].

Cantharellus neopersicinus Ming Zhang, T.H. Li & X.Y. Chen sp. nov. Figure 14 and Figure 15.

MycoBank: MB843660

GenBank: OM978943 for LSU, ON119057 for tef1 and ON119042 for rpb2

Etymology—refers to the color similar to Cantharellus persicinus.

Diagnosis—The pastel red to pink pileus, white to pinkish hymenophore with strongly bifurcate low veins and ellipsoid to subglobose [(6–)7–8.5(–9) × (4–)4.5–5.5(–6) μm], make C. neopersicinus easily distinguished from other species in the subg. Parvocantharellus.

Type—China. Guangdong Province, Leizhou City, Fangcha Village, under Eucalyptus robusta, alt. 105 m, 16 October 2021, Xiu-Yuan Chen (GDGM87366).

Basidiomata small-sized. Pileus 15–45 mm broad, convex when young, then gradually to nearly applanate with a central shallow depression at maturity; surface dry, glabrous, pastel red, pastel pink to pink (8A4–12A4); margin incurved when young, reflexed with age, wavy, sometimes irregularly split; unchanging when touched. Context thin, reddish white or pinkish (8A2–12A2), unchanging when exposed. Hymenophore decurrent, but clearly demarcated with stipe, lamellate ridges close to subdistant, poorly-developed, strongly forking towards pileus margin, with bifurcate low veins between ridges, white to pinkish, unchanging when bruised. Stipe 15–40 × 3–8 mm, central, cylindrical or slightly tapering towards base, hollow, glabrous, concolorous with pileus, unchanging when handled. Odor fruity. Taste mild.

Basidiospores (50/2/2) (6–)7–8.5(–9) × (4–)4.5–5.5(–6) μm, L_m × W_m = 7.78(±0.64) × 4.871(±0.46) μm, Q = (1.2)1.4–1.77(2), Q_m = 1.6 ± 0.15, ellipsoid to subglobose, smooth, guttulate. Basidia 45–62 × 7–9 μm, 4–6-spored, narrowly clavate, colorless to hyaline in KOH, sterigmata 3–7 μm long. Hymenophoral trama irregular to subregular, composed of colorless and branched hyphae, 8–16 μm wide, septate, thin-walled. Pileipellis a cutis with long, repent to suberect, branched, and slightly interwoven hyphae, subcylindrical cells in 8–15 μm wide, thin-walled; terminal cells appressed, mostly cylindrical, up to 100 μm long, 5–15 μm wide. Stipitipellis a cutis of cylindrical, parallel hyphae, 3–8 μm wide, terminal cells cylindrical. Clamp connections abundant in all tissues.

Habitat and distribution—Gregarious or scattered under Eucalyptus robusta Smith in tropical China. Currently known from Guangdong Province, Southern China.

Additional specimens examined—China. Guangdong Province, Leizhou City, Fangcha Village, alt. 105 m, 25 October 2021, Xiu-Yuan Chen (GDGM85145).

Notes—Cantharellus neopersicinus is characterized by its small basidiomata, pastel red to pink pileus, poorly-developed lamellate hymenophore with strongly bifurcate low veins and ellipsoid to subglobose basidiospores [(6–) 7–8.5 (–9) × (4–) 4.5–5.5 (–6) μm]. Phylogenetic analyses based on multi-locus datasets demonstrated that C. neopersicinus was well nested into the subg. Parvocantharellus, formed a well-supported terminal clade, and was closely related to C. albus S.P. Jian & B. Feng and C. luteolus. However, C. albus, recently reported from China, can be easily distinguished by its white basidiomata slightly changing to yellowish when bruised, a spicy taste and smaller basidiospores (5.5–7.5 × 4.5–6 µm) [12,13]; C. luteolus differs in its small basidiomata, yellow to orange pileus, greyish-yellow to greyish-orange hymenophore and oval to subglobose basidiospores (7–8 × 5.2–6.5 μm) [13].

Morphologically, the pastel red to pink pileus color is easily reminiscent of the species C. cinnabarinus, C. coccolobae Buyck, P.-A. Moreau & Courtec., C. phloginus and C. persicinus. However, the former three species belong to the subg. Cinnabarinus, and can be easily distinguished from C. neopersicinus by the genetic distances. Besides, C. cinnabarinus differs in its cinnabar red to bright orange pileus, thick-walled hyphal terminal cells of pileipellis and smaller basidiospores (6.7–7.57 × 3.82–4.68 μm) [32]. Cantharellus coccolobae differs in its salmon orange hymenophore, white stipe context partly changing to yellowish when cut, large basidiospores [(7.9) 8.3–9.3 (9.8) × (4.8) 5.3–5.9 (6) µm], longer basidia up to 120 µm and the thick-walled hyphae of the pileipellis. Additionally, C. coccolobae was reported to be strictly associated with Coccoloba trees, while C. neopersicinus is under Eucalyptus trees [33]. Cantharellus phloginus is redescribed in this study and differs in its darker pileus color, pale yellow to light yellow hymenophore, white context and larger basidiospores [6.8–9.5 (–12) × 5–7 μm]. Cantharellus persicinus, originally reported from North America, differs in its more robust basidiomata, larger basidiospores (9.6–10.9 × 6.3–7.1 μm), and thick-walled cells of pileipellis. In addition, C. persicinus is reported to be associated with oaks or eastern hemlock [32,43,44].

Cantharellus koreanus Buyck, Antonín & Ryoo, in Antonín, Hofstetter, Ryoo, Ka and Buyck, Mycol. Progr. 16(8): 755 (2017); Figure 16 and Figure 17.

Basidiomata small-sized. Pileus 15–40 mm broad, convex at first, then gradually applanate with slightly an umbilicate centre; margin involute at first, undulate; surface dry, glabrous or finely tomentose-fibrillose at centre, mostly pale yellow to light yellow (1A3–4A3,1A4–4A4), olive brown to light brown (4D4–5D4) at centre, with obscurely sulcate at margin. Hymenophore with lamellate ridges; ridges broadly adnate to subdecurrent, with a clearly delimitation from the stipe surface, well-developed, bifurcate and with interconnected low veins, up to 1 mm high, yellowish white (2A2–4A2), unchanging when bruised. Stipe10–40 mm long, 2–5 mm thick, subcylindrical to cylindrical, slightly enlarged downward, but sometimes tapering towards base, glabrous or with faintly scaly, hollow, concolorous with pileus, darker and more somber than lamellae ridges. Odor fruity. Taste mild.

Basidiospores 5–8 × (4–) 4.5–6 μm, L_m × W_m = 7.05(±0.51) × 5.192(±0.34) μm, Q = (1.08)1.2–1.45(1.6), Q_m = 1.36 ± 0.097, ellipsoid, broadly ellipsoid, thin-walled. Basidia 40–70 × 8–12 μm, 4–6-spored, narrowly clavate, sometimes subcapitate, thin-walled, clamped. Hymenophoral trama composed of clavate, subcylindrical, subregular, branched, thin-walled, clamped hyphae 5–12 μm wide. Pileipellis a cutis, composed of cylindrical, thin-walled hyphae, 5–15 μm wide; terminal cells clavate, fusoid to cylindrical, up to 100 μm long. Stipitipellis a cutis of cylindrical, parallel, branched, thin-walled hyphae 2–9 μm wide. Clamp connections abundant in all tissues.

Habitat and distribution—Gregarious or scattered under broadleaf forests (dominated by Fagaceae trees) in subtropical regions of China. Known from Hunan Province, China and Korea.

Specimens examined—China, Hunan Province, Zhangjiajie City, Zhangjiajie National Forest Park, alt. 1200 m, 17 July 2020, Wei-Qiang Qin (GDGM79233); same location, alt. 1100 m, 5 July 2021, Wei-Qiang Qin (GDGM85306).

Notes—Cantharellus koreanus, recently reported from Korea, is firstly reported from China in this study. It is characterized by the small basidiomata, the dirty yellow-brown to pale brown pileus with a brown to dark brown center, the well-development hymenophoral ridges with yellow tinge, and the ellipsoid to broadly ellipsoid basidiospores 6–8 (–9) × 4.2–5.5 (–6.5) μm in Antonín et al. [11] and 5–8 × (4–) 4.5–6 μm in this study.

Phylogenetically, C. koreanus is closely related to C. appalachiensis, C. austrosinensis and C. tabernensis. Indeed, C. koreanus is similar to C. appalachiensis, C. austrosinensis and C. tabernensis in morphology. However, C. appalachiensis differs in its larger and more robust basidiomata (pileus up to 50 mm broad), drab yellow to dull brown pileus, narrower basidia (5.5–9 μm in diam.), shorter and slightly thickened end cell of pileipellis, narrower hyphae of hymenophoral trama, and association with oaks and other hardwoods [41,45,46]; C. austrosinensis differs in its smaller basidiomata, pastel yellow to greyish-yellow pileus with a greyish-orange to brownish-orange center, shorter and narrower basidia (50–55 × 7–9 μm), interwoven hyphae of pileipellis, and symbiosis with coniferous trees [13]; C. tabernensis differs in its dull orange yellow to yellowish brown pileus, vivid orange yellow hymenophore and stipe, shorter and narrower basidia (35–55 × 5–8 μm), and distribution in North America [40,42,46].

In addition, several species were recently reported from China, and are also similar to C. koreanus in morphology, such as C. galbanus, C. luteolus Ming Zhang, C.Q. Wang & T.H. Li, C. luteovirens and C. sinominor Ming Zhang, C.Q. Wang & T.H. Li [13], but they can be easily separated from each other by the large genetic distances.

3.3. Key to Species of Subgenus Cinnabarinus in China

1 Basidiomata with pastel red or reddish orange tinge...................................................2

1’ Basidiomata without red tinge........................................................................................4

2 Pileus: small, always <20 mm broad..............................................C. sinocinnabarinus

2’ Pileus: relatively large, usually >20 mm wide...............................................................3

3 Basidiospores: 7–8.5 × 5–6 μm..................................................................C. albovenosus

3’ Basidiospores: 6.8–9.5 (–12) × 5–7 μm.........................................................C. phloginus

4 Pileus: greenish yellow to yellowish orange, hymenophore white to yellowish white; basidiospores: 7–9 × 5–6(6.5) μm.....................................................................C. citrinus

4’ Pileus: orange to orange-yellow, hymenophore pinkish white to orange white; basidiospores: 7.5–9 × 5–6.5 μm, basidia up to 100 μm....................................C. chrysanthus

4. Discussion

In this study, the species diversity of C. subg. Cinnabarinus from China were examined. Five species were identified based on morphological characters and multi-locus phylogenetic analyses, containing two new species C. chrysanthus and C. sinocinnabarinus, two newly recorded species C. albovenosus and C. citrinus to China, and a known species, C. phloginus. In addition, three species belonging to the subg. Parvocantharellus were firstly discovered from China, including two new species C. convexus and C. neopersicinus, and a new recorded species, C. koreanus.

In the past, the knowledge of species diversity of Cantharellus in China was poor and the specimens with large and yellow to orange basidiomata were mostly misidentified as the type species of the genus C. cibarius; meanwhile, specimens with small and yellow to orange red basidiomata were often inaccurately treated as C. minor Peck or C. cinnabarinus. However, a recent study proved that the distribution of C. cibarius is limited to northeast China, and the so-called “C. cibarius” reported from southwest China is actually C. yunnanensis W.F. Chiu [8]; meanwhile, the specimens labeled as “C. minor” in China were also proven to be misidentified, several new species with small basidiomata have been reported from China, and the distribution of C. minor with correctly identified specimens has not been found in China [13]. Cantharellus cinnabarinus was widely reported in China [19,21], but those photos of C. cinnabarinus used in the two literatures look like C. albovenosus; the correctly identified specimens of C. cinnabarinus in China have not been found in the present study. However, three morphologically similar species were discovered. The specimen HKAS58243 from southwest China, firstly identified as C. cinnabarinus in Shao et al. [20], was proven to be a native species of C. sinocinnabarinus in the present study. In addition, C. sinocinnabarinus seems to be restricted to subalpine habitats, and prefers symbiosis with Cyclobalanopsis delavayi and Pinus yunnanensis. The other two species, C. albovenosus and C. phloginus, are easily misidentified as C. cinnabarinus by their small basidiomata and reddish pileus color. However, C. albovenosus, recently reported from Korea, has been also found in eastern China, and C. phloginus seems to be restricted to tropical to subtropical regions in southwest China. Thus, we speculate that the specimens of “C. cinnabarinus” in Anhui, Guangdong, Jiangsu and Zhejiang provinces could be C. albovenosus, the distribution of “C. cinnabarinus” from tropical to subtropical regions of southwest China could be C. phloginus and the collections of “C. cinnabarinus” from subalpine regions of southwest China could be C. sinocinnabarinus.

Cantharellus neopersicinus, newly discovered in this study, is a remarkable species in Cantharellus. Morphologically, C. neopersicinus can be easily identified as a member of subg. Cinnabarinus or subg. Cantharellus, due to its pastel red to pink pileus and white to pinkish hymenophore; however, phylogenetic analyses demonstrated that it belongs to the subg. Parvocantharellus, which makes it the first species reported from China with pastel red to pink tinge in the subg. Parvocantharellus. Ecologically, C. neopersicinus is distributed in tropical areas of southern China, and currently, the only known symbiosis is with Eucalyptus robusta.

Cantharellus subg. Parvocantharellus, mainly composed of small-sized species, was suggested to be a monophyletic group, and closely related to the subg. Cinnabarinus [3]. However, in the present study, the subgenus was proven to be paraphyletic or polyphyletic; two species of C. cyanoxanthus R. Heim ex Heinem. and C. subcyanoxanthus Buyck, Randrianj. & Eyssart formed an isolated clade in the multi-locus phylogenetic tree, and could represent a separate generic clade. The result is similar to previous studies [13,16].

Species in the two subgenera are difficult to separate in morphology because most species share similar characteristics of small basidiomata, abundant clamps and thin-walled hyphal ends at the pileus surface. However, they formed two separate clades in the multi-locus phylogenetic trees, and can be easily distinguished by molecular phylogenetic evidence. In addition, the species in subg. Cinnabarinus mostly own distinct orange, pink or red tinge, and can be distinguished from subg. Parvocantharellus. In future work, more detailed morphological observations are needed to provide new evidences for distinguishing the two subgenera.

Author Contributions

Conceptualization, M.Z. and T.-H.L.; methodology, M.Z. and C.-Q.W.; performing the experiment, M.Z.; phylogenetic analysis, M.Z. and Y.L.; validation, M.Z., C.-Q.W., Y.L., M.-S.G., S.-C.S., W.-Q.Q., W.-Q.D. and T.-H.L.; writing—original draft preparation, M.Z.; writing—review and editing, C.-Q.W., Y.L., S.-C.S. and T.-H.L.; visualization, M.Z.; supervision, T.-H.L.; project administration, M.Z.; funding acquisition, M.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (Nos. 32070020 and 32170010), the Science and Technology Planning Project of Guizhou Province, China [No. Qian Ke He Fu Qi (2019) 4007], and Biodiversity Survey, Observation and Evaluation Project (2019–2023) of the Ministry of Ecology and Environment of China.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Publicly available datasets were analyzed in this study. These data can be found here: (https://www.ncbi.nlm.nih.gov/; https://www.mycobank.org/page/Release%20names; accessed on 20 March 2022).

Acknowledgments

The authors sincerely thank the editors and anonymous reviewers for their efforts and contributions towards this manuscript. Sincere acknowledgments are expressed to the curators of the HMAS and HKAS for loan of the research specimens; to B. Bart (Muséum National d’Histoire Naturelle) for providing the sequences of Cantharellus koreanus; to W.Z. Ma (Kunming Institute of Botany, Chinese Academy of Sciences) and Z. Du (Institute of Microbiology, Chinese Academy of Sciences) for their assistance during the loan of specimens; to X.Y. Chen, Z.H. Zhang, and Y. He for the collaboration in the field.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Phylogenetic tree of representative species of Cantharellus inferred from LSU-tef1-rpb2 dataset by means of both ML and BI methods. Cantharellus cibarius Fr. served as outgroup. Bootstrap Supports (BS > 50%) and Bayesian Posterior Probabilities (BPP > 0.90) are shown on the supported branches. Bold names represent new species.

Figure 2. Basidiomata of Cantharellus chrysanthus. (a,b) GDGM80220, holotype. (c) GDGM60524. (d) GDGM80438. (e) GDGM82516. (f) GDGM80217. (g) GDGM49628. (h) GDGM80436. (i) GDGM60334. (j) GDGM80202. (k) GDGM45937. (l) GDGM85298. (m) GDGM82473. Bars = 2 cm.

Figure 3. Cantharelluschrysanthus (GDGM80220, Holotype). (a) Basidiospores. (b) Basidia, basidiola and elements of the subhymenium. (c) Pileipellis. Bars: (a,b) = 10 μm; (c) = 20 μm.

Figure 4. Basidiomata of Cantharellus sinocinnabarinus. (a,c) GDGM83230. (b) GDGM83232. (d) GDGM83229. (e) GDGM832296. (f) GDGM83027. (g) GDGM83238. (h) HKAS58243. Bars = 2 cm.

Figure 5. Cantharellus sinocinnabarinus. (a) Basidiospores. (b) Basidia, basidiola and elements of the subhymenium. (c) Pileipellis. Bars: (a,b) = 10 μm; (c) = 20 μm.

Figure 6. Basidiomata of Cantharellus albovenosus. (a,b) GDGM85852. (c,d) GDGM85846. (e) GDGM85142. Bars = 2 cm.

Figure 7. Cantharellus albovenosus. (a) Basidia, basidiola and elements of the subhymenium. (b) Basidiospores. (c) Pileipellis. Bars: (a,b) = 10 μm; (c) = 20 μm.

Figure 8. Basidiomata of Cantharellus citrinus. (a,b) GDGM86143. (c) GDGM86141. (d) GDGM80723. Bars = 2 cm.

Figure 9. Cantharellus citrinus. (a) Basidiospores. (b) Basidia, basidiola and elements of the subhymenium. (c) Pileipellis. Bars: (a,b) = 10 μm; (c) = 20 μm.

Figure 10. Basidiomata of Cantharellus phloginus (GDGM79007). Bar = 5 cm.

Figure 11. Cantharellus phloginus. (a) Basidiospores. (b) Basidia, basidiola and elements of the subhymenium. (c) Pileipellis. Bars: (a,b) = 10 μm; (c) = 20 μm.

Figure 12. Basidiomata of Cantharellus convexus. (a) GDGM70307. (b) GDGM54841. Bars = 2 cm.

Figure 13. Cantharellus convexus. (a) Basidiospores. (b) Basidia, basidiola and elements of the subhymenium. (c) Pileipellis. Bars: (a,b) = 10 μm; (c) = 20 μm.

Figure 14. Basidiomata of Cantharellus neopersicinus. (a–e) GDGM87366. (f,g) GDGM85145. Bars: (a,b,d–f) = 2 cm; (c,g) = 5 cm.

Figure 15. Cantharellusneopersicinus. (a) Basidiospores. (b) Basidia, basidiola and elements of the subhymenium. (c) Pileipellis. Bars: (a,b) = 10 μm; (c) = 20 μm.

Figure 16. Basidiomata of Cantharellus koreanus. (a,b) GDGM79233. (c,d) GDGM85306. Bars = 2 cm.

Figure 17. Cantharellus koreanus. (a) Basidiospores. (b) Basidia, basidiola and elements of the subhymenium. (c) Pileipellis. Bars: (a, b) = 10 μm; (c) = 20 μm.

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Zhang, M.; Wang, C.-Q.; Gan, M.-S.; Li, Y.; Shao, S.-C.; Qin, W.-Q.; Deng, W.-Q.; Li, T.-H. Diversity of Cantharellus (Cantharellales, Basidiomycota) in China with Description of Some New Species and New Records. J. Fungi 2022, 8, 483. https://doi.org/10.3390/jof8050483

AMA Style

Zhang M, Wang C-Q, Gan M-S, Li Y, Shao S-C, Qin W-Q, Deng W-Q, Li T-H. Diversity of Cantharellus (Cantharellales, Basidiomycota) in China with Description of Some New Species and New Records. Journal of Fungi. 2022; 8(5):483. https://doi.org/10.3390/jof8050483

Chicago/Turabian Style

Zhang, Ming, Chao-Qun Wang, Man-Shui Gan, Yi Li, Shi-Cheng Shao, Wei-Qiang Qin, Wang-Qiu Deng, and Tai-Hui Li. 2022. "Diversity of Cantharellus (Cantharellales, Basidiomycota) in China with Description of Some New Species and New Records" Journal of Fungi 8, no. 5: 483. https://doi.org/10.3390/jof8050483

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Diversity of Cantharellus (Cantharellales, Basidiomycota) in China with Description of Some New Species and New Records

Abstract

1. Introduction

2. Materials and Methods

2.1. Morphological Studies

2.2. DNA Extraction, PCR Amplification and Sequencing

2.3. Phylogenetic Analyses

3. Results

3.1. Molecular Phylogeny

3.2. Taxonomy

3.2.1. Cantharellus subgen. Cinnabarinus Buyck & V. Hofst.

3.2.2. Cantharellus subgen. Parvocantharellus Eyssart. & Buyck

3.3. Key to Species of Subgenus Cinnabarinus in China

4. Discussion

Author Contributions

Funding

Institutional Review Board Statement

Informed Consent Statement

Data Availability Statement

Acknowledgments

Conflicts of Interest

References

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