Morphological and Phylogenetic Evidences Reveal Four New Species of Cantharellus Subgenus Cantharellus (Hydnaceae, Cantharellales) From China.

Species of Cantharellus subgenus Cantharellus are interesting and important for their mycorrhizal properties, medicinal values, and edibility. In China, there are many undescribed species of the subgenus. In this study, four new species of subg. Cantharellus, viz. Cantharellus albopileatus, Cantharellus chuiweifanii, Cantharellus pinetorus, and Cantharellus ravus from Hainan and Hunan Provinces, respectively, were described based on morphological and phylogenetic evidence as a contribution to the knowledge of the species diversity in China. Detailed descriptions, color photographs of fresh basidiomata, and line drawings of microstructures of these four new species are presented as well as comparisons with related species.

Introduction

Species diversity, taxonomy, and phylogeny of macrofungi have been investigated in the recent years, and many new species have been discovered (Zeng et al., 2013; Han et al., 2016; Chai et al., 2019; Cui et al., 2019; Shen et al., 2019; Sun et al., 2020; Liu et al., 2021a,b, 2022; Wu et al., 2021; Ji et al., 2022; Xie et al., 2022). Species of Cantharellus Adans. ex Fr. (Hydnaceae, Cantharellales), interesting and important fungi, have also received a lot of attention by mycologists for their mycorrhizal properties, medicinal values, and edibility (Pilz et al., 2003; Yun and Hall, 2004; Shao et al., 2012). Molecular phylogeny has delimited abundant species within the genus and revealed unexpected species diversity (Buyck et al., 2011, 2013, 2014, 2016a,b; Foltz et al., 2013; Leacock et al., 2016). Until now, a large number of Cantharellus taxa have been described in Europe, Africa, and North America (Corner, 1966; Buyck et al., 2011, 2013, 2014, 2016a,b, 2018; Kumari et al., 2011, 2013; Suhara and Kurogi, 2015; De Kesel et al., 2016; Leacock et al., 2016).

In China, many species of Cantharellus have been uncovered (Chiu, 1973; Zang, 1980; Wei et al., 2008; Tian et al., 2009, 2012; Shao et al., 2011, 2012, 2014, 2016a,2021; Buyck et al., 2018; An et al., 2017; Jian et al., 2020; Cao et al., 2021; Zhang M. et al., 2021). They are well known to the public in the country because most of them have activities of anticancer, antimicrobial, immune regulation, and antioxidant (Dulger et al., 2004; Daniewskia et al., 2012; Nowacka-Jechalkea et al., 2018; Zhao et al., 2018). Interestingly, basidiocarps of Cantharellus such as Cantharellus yunnanensis W. F. Chiu are sold as edibles in markets in Yunnan Province, southwestern China (Figure 1), which generate good economic value (Watling, 1997; Wu and Lu, 2006).

FIGURE 1

Collections of chanterelle sold as edibles in the market of Yunnan Province, southwestern China. Photographs were taken by N. K. Zeng.

Recently, the genus Cantharellus has been divided into six subgenera including subg. Afrocantharellus Eyssart. and Buyck, subg. Cantharellus Adans. ex Fr., subg. Cinnabarinus Buyck and V. Hofst., subg. Parvocantharellus Eyssart. and Buyck, subg. Pseudocantharellus Eyssart. and Buyck, and subg. Rubrinus Eyssart. and Buyck (Buyck et al., 2014). Among them, subg. Cantharellus has received considerable attention, which is characterized by basidiomata that is medium- to large-sized; cap and stipe are usually smooth, sometimes with appressed squama; hymenophore is veined with blunt, mostly strongly forking-anastomosing ridges, rarely smooth or nearly so; hyphal endings are mostly thick-walled; clamp connections are abundant everywhere (Buyck et al., 2014). In China, although several taxa of subg. Cantharellus have been described or reported in previous studies (Chiu, 1973; Shao et al., 2011, 2016b,2021; An et al., 2017; Cao et al., 2021; Zhang Y. Z. et al., 2021), many more undescribed novel species probably exist in the country. Recently, many collections of subg. Cantharellus in China have been collected, and they were studied using morphological and molecular phylogenetic analyses, aiming to (i) describe new taxa and (ii) elucidate the species diversity of subg. Cantharellus in China.

Materials and Methods

Morphological Studies

Field notes and digital photographs were made from fresh specimens. Specimens examined in this study were deposited in the Fungal Herbarium of Hainan Medical University (FHMU), Haikou City, Hainan Province of China. Macroscopic descriptions are based on the detailed notes and photographs taken from fresh basidiomata. Color codes follow Kornerup and Wanscher (1981). Samples were hand-sectioned and mounted in 5% KOH solution and 1% congo red. Sections of the pileipellis were cut radial-perpendicularly and halfway between the center and the margin of the pileus. The following notations [n/m/p] indicate that n basidiospores measured m basidiomata of p collections. Dimensions of basidiospores were presented in the form (a–)b–e–c(–d), where the range b–c contains at least 90% of the measured values, “a” and “d” were the extreme values, and “e” refers to the average length/width of basidiospores. Q refers to the length/width ratio of basidiospores; Q refers to the average Q of basidiospores and is given with standard deviation. For basidiospore shape, Q = 1.15–1.3 describes “broadly ellipsoid,” Q = 1.3–1.6 “ellipsoid,” and Q = 1.6–2.0 “elongate” (Yang, 2005). The terms referring to the size of basidioma are based on Bas (1969).

Molecular Procedures

Total genomic DNA was obtained with the Plant Genomic DNA Kit (CWBIO, Beijing, China) according to the manufacturer’s instructions from collections dried with silica gel. Primer pairs used for amplification were as follows: nuc 28S rDNA D1-D2 domains (28S) with LR0R/LR5 (Vilgalys and Hester, 1990; James et al., 2006) and the translation elongation factor 1-α gene (TEF1) with EF1-α-F/EF1-α-R (Mikheyev et al., 2006). Polymerase chain reaction (PCR) conditions followed the program of Zhang Y. Z. et al. (2021). PCR products were checked in 1% (w/v) agarose gels. Amplified PCR products were sequenced using an ABI 3730 DNA Analyzer (Guangzhou Branch of BGI, China) with the same primers. Forward or reverse sequences were compiled with BioEdit (Hall, 1999). All sequences newly obtained in this study were deposited to GenBank[1].

Dataset Assembly

A total of sixty-nine DNA sequences (34 of 28S, and 35 of TEF1) from 36 collections were newly generated. Edited sequences were deposited in GenBank; the GenBank accession numbers are listed in Table 1. For the concatenated dataset, the sequences of 28S and TEF1 from new collections were aligned with selected sequences of subg. Cantharellus from previous studies and GenBank (Table 1); Cantharellus ibityensis Buyck, Randrianj. and V. Hofst. was chosen as an outgroup inferred from Buyck et al. (2014). To test for phylogenetic conflict among 28S and TEF1, single-gene phylogenetic trees based on each of these two fragments were analyzed. The results of analyses showed that 28S and TEF1 were not in conflict. Thus, two datasets (28S and TEF1) were aligned with MUSCLE v3.6 (Edgar, 2004) and manually optimized on BioEdit v7.0.9 (Hall, 1999); then, the two datasets were concatenated using Phyutility v2.2 for further analyses (Smith and Dunn, 2008).

TABLE 1

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

Taxon	Voucher	Locality	GenBank accession nos.		References
			28S	TEF1
Cantharellus albopileatus	N.K. Zeng3026 (FHMU1987)	Hainan, Southern China	OM691480	OM811321	Present study
Cantharellus albopileatus	W.F. Lin7 (FHMU6850)	Zhejiang, Eastern China	OM691481	OM811322	Present study
Cantharellus alborufescens	BIO-Fungi 11689	Spain	KX828802	KX828832	Olariaga et al. (2017)
Cantharellus altipes	BB 07.019	United States	KF294627	GQ914939	Buyck et al. (2011, 2014)
Cantharellus altipes	BB 07.162	United States	KF294636	GQ914945	Buyck et al. (2011, 2014)
Cantharellus altipes	BB 07.005	United States	—	GQ914938	Buyck et al. (2011)
Cantharellus altipes	BB 07.055	United States	—	GQ914940	Buyck et al. (2011)
Cantharellus altipes	BB 07.112	United States	—	GQ914941	Buyck et al. (2011)
Cantharellus amethysteus	BB 07.284	Slovakia	KF294639	GQ914953	Buyck et al. (2011, 2014)
Cantharellus amethysteus	BB 07.309	Slovakia	KF294642	GQ914954	Buyck et al. (2011, 2014)
Cantharellus anzutake	C-2	Japan	LC085416	LC085470	Ogawa et al. (2017)
Cantharellus anzutake	C-84	Japan	LC085415	LC179800	Ogawa et al. (2017)
Cantharellus applanatus	PUN 3964	India	HM750918	—	Kumari et al. (2013)
Cantharellus californicus	OSC122878	United States	KX828795	KX828820	Olariaga et al. (2017)
Cantharellus camphoratus	12.09.06.av01	United States	KX592734	KX592735	Thorn et al. (2017)
Cantharellus cascadensis	OSC75917	United States	AY041158	—	Dunham et al. (2003)
Cantharellus chicagoensis	1073/JJMO-CANT-1	United States	—	KX857025	Buyck et al. (2016a)
Cantharellus chuiweifanii	N.K. Zeng3474 (FHMU5335)	Hainan, Southern China	OM717946	OM811340	Present study
Cantharellus chuiweifanii	N.K. Zeng4596 (FHMU6846)	Hainan, Southern China	OM717947	OM811341	Present study
Cantharellus chuiweifanii	N.K. Zeng4559 (FHMU6847)	Hainan, Southern China	OM717948	OM811342	Present study
Cantharellus chuiweifanii	N.K. Zeng2608 (FHMU1703)	Hainan, Southern China	OM717949	OM811343	Present study
Cantharellus chuiweifanii	N.K. Zeng3452 (FHMU5260)	Hainan, Southern China	OM717950	OM811344	Present study
Cantharellus chuiweifanii	N.K. Zeng4558 (FHMU6848)	Hainan, Southern China	OM717951	OM811345	Present study
Cantharellus chuiweifanii	N.K. Zeng4897 (FHMU6849)	Hainan, Southern China	OM717952	OM811346	Present study
Cantharellus chuiweifanii	N.K. Zeng1524 (FHMU2412)	Hainan, Southern China	OM717953	OM811347	Present study
Cantharellus chuiweifanii	N.K. Zeng3463 (FHMU2839)	Hainan, Southern China	OM717954	OM811348	Present study
Cantharellus chuiweifanii	N.K. Zeng5322 (FHMU3236)	Hainan, Southern China	OM717955	OM811349	Present study
Cantharellus chuiweifanii	N.K. Zeng3392 (FHMU5268)	Hainan, Southern China	OM717956	OM811350	Present study
Cantharellus cibarius	WXH 2580	Jilin, NE China	—	KM893847	Unpublished
Cantharellus cibarius	BB 07.300	Slovakia	KF294641	GQ914950	Buyck et al. (2011, 2014)
Cantharellus cibarius	GE 07.025	France	KF294658	GQ914949	Buyck et al. (2011, 2014)
Cantharellus cibarius	WXH 2296	Finland	—	KM893842	Unpublished
Cantharellus cibarius	AFTOL-ID 607	Germany	—	DQ059050	Matheny et al. (2007)
Cantharellus deceptivus	1079/JJ NC-CANT-5	United States	—	KX857030	Buyck et al. (2016a)
Cantharellus elongatipes	PUN 3966	India	HM750929	—	Kumari et al. (2013)
Cantharellus ferruginascens	BB 07.283	Slovakia	KF294638	GQ914952	Buyck et al. (2011, 2014)
Cantharellus ferruginascens	BB 07.221	Slovakia	KF294637	GQ914951	Buyck et al. (2011, 2014)
Cantharellus flavolateritius	1078/JJ NC-CANT-4	United States	—	KX857029	Buyck et al. (2016a)
Cantharellus flavolateritius	1076/JJ NC-CANT-2	United States	—	KX857027	Buyck et al. (2016a)
Cantharellus flavus	C067	United States	—	JX030416	Foltz et al. (2013)
Cantharellus formosus	OSC 75930	United States	AY041164	—	Dunham et al. (2003)
Cantharellus formosus	OSC 76054	United States	AY041165	—	Dunham et al. (2003)
Cantharellus hainanensis	N.K. Zeng2289(FHMU1931)	Hainan, Southern China	KY407524	KY407536	An et al. (2017)
Cantharellus ibityensis	BB 08.196	Madagascar	KF294650	GQ914980	Buyck et al. (2011, 2014)
Cantharellus ibityensis	BB 08.203	Madagascar	KF294651	JX192985	Buyck et al. (2013, 2014)
Cantharellus indicus	PUN 3962	India	HM750924	—	Kumari et al. (2013)
Cantharellus iuventateviridis	1542/SH13.7.2012	United States	—	KX857063	Herrera et al. (2018)
Cantharellus iuventateviridis	1543/SH14.7.2012	United States	—	KX857064	Herrera et al. (2018)
Cantharellus laevihymeninus	Yuan 13900	Yunnan, SW China	MW979520	MW999418	Cao et al. (2021)
Cantharellus laevihymeninus	Yuan 13902	Yunnan, SW China	MW979521	MW999419	Cao et al. (2021)
“Cantharellus lateritius”	PUN 3958	India	HM750919	—	Kumari et al. (2013)
Cantharellus lateritius	BB 06.319	United States	—	GQ914958	Buyck et al. (2011)
Cantharellus lateritius	BB 07.004	United States	—	GQ914955	Buyck et al. (2011)
Cantharellus lateritius	BB 07.025	United States	KF294628	GQ914957	Buyck et al. (2011, 2014)
Cantharellus lateritius	BB 07.058	United States	KF294633	GQ914959	Buyck et al. (2011, 2014)
Cantharellus lewisii	BB 02.197	United States	KF294623	GQ914961	Buyck et al. (2011, 2014)
Cantharellus lewisii	BB 07.003	United States	JN940597	GQ914962	Unpublished; Buyck et al. (2011)
Cantharellus macrocarpus	N.K. Zeng4036(FHMU3303)	Hainan, Southern China	MT986060	MT990633	Zhang Y. Z. et al., 2021
Cantharellus macrocarpus	N.K. Zeng4050(FHMU3304)	Hainan, Southern China	MT986061	MT990634	Zhang Y. Z. et al., 2021
Cantharellus macrocarpus	N.K. Zeng5235 (FHMU6385)	Hainan, Southern China	OM717945	OM811339	Present study
Cantharellus natarajanii	PUN 3963	India	HM750926	—	Kumari et al. (2013)
Cantharellus pallens	AH44799	Spain	KR677537	KX828833	Olariaga et al. (2015, 2017)
Cantharellus pallens	AH39124	Morocco	KX828804	KX828834	Olariaga et al. (2017)
Cantharellus pallens	BB 09.441	Italy	KX907218	KX834411	De Kesel et al. (2016)
Cantharellus pallens	BB 09.430	Italy	KX907217	KX834410	De Kesel et al. (2016)
Cantharellus persicinus	1085/JJ MO-CANT-4	United States	—	KX857033	Buyck et al. (2016a)
Cantharellus persicinus	1685/MH 15.001	United States	—	KX857080	Buyck et al. (2016a)
Cantharellus phasmatis	C057	United States	JX030431	JX030417	Foltz et al. (2013)
Cantharellus phasmatis	C074	United States	—	JX030418	Foltz et al. (2013)
Cantharellus pinetorus	N.K. Zeng4180 (FHMU3759)	Hunan, Central China	OM691482	OM811323	Present study
Cantharellus pinetorus	N.K. Zeng4181 (FHMU3749)	Hunan, Central China	OM691483	OM811324	Present study
Cantharellus pseudoformosus	SMR-2009a	India	GU237071	—	Kumari et al. (2011)
Cantharellus quercophilus	BB 07.097	United States	KF294644	JX192981	Buyck et al. (2013, 2014)
Cantharellus ravus	N.K. Zeng4176 (FHMU6845)	Hunan, Central China	OM717944	OM811338	Present study
Cantharellus roseocanus	CC29	United States	—	JX030415	Foltz et al. (2013)
Cantharellus roseocanus	DAOM220723	Canada	KX828810	KX828837	Olariaga et al. (2017)
Cantharellus roseocanus	DAOM220724	Canada	KX828811	KX828838	Olariaga et al. (2017)
Cantharellus roseocanus	MO 245717	—	—	MF784581	Unpublished
Cantharellus roseofagetorum	AH44786	Georgia	KX828813	KX828840	Olariaga et al. (2017)
Cantharellus roseofagetorum	AH44789	Georgia	KX828812	KX828839	Olariaga et al. (2017)
Cantharellus sp.	C-53	Japan	LC085421	LC085475	Ogawa et al. (2017)
Cantharellus sp.	C-141	Japan	LC085422	LC085476	Ogawa et al. (2017)
Cantharellus sp.	N.K. Zeng4113 (FHMU3834)	Guangdong, Southern China	OM691493	OM811334	Present study
Cantharellus sp.	N.K. Zeng3406 (FHMU5266)	Hainan, Southern China	OM691494	OM811335	Present study
Cantharellus sp.	S. Jiang106 (FHMU4592)	Hainan, Southern China	OM691495	OM811336	Present study
Cantharellus sp.	C-106	Japan	LC085418	LC085473	Ogawa et al. (2017)
Cantharellus spectaculus	C081	United States	JX030421	JX030414	Foltz et al. (2013)
Cantharellus subalbidus	OSC81782	United States	KX828814	KX828841	Olariaga et al. (2017)
Cantharellus subamethysteus	DS 06.218	Malaysia	KF294664	—	Buyck et al. (2014)
Cantharellus subvaginatus	1692	Korea	MG450678	—	Buyck et al. (2018)
Cantharellus tenuithrix	BB 07.035	United States	KF294629	GQ914946	Buyck et al. (2011, 2014)
Cantharellus tenuithrix	BB 07.125	United States	JN940600	GQ914947	Unpublished; Buyck et al. (2011)
Cantharellus tenuithrix	BB 14.099	United States	—	KX857054	Buyck et al. (2016a)
“Cantharellus umbonatus”	PUN 3968	India	HM750916	—	Kumari et al. (2013)
Cantharellus vaginatus	HKAS 55728	Yunnan, SW China	HM594680	—	Shao et al. (2011)
Cantharellus vaginatus	HKAS 55730	Yunnan, SW China	HM594681	—	Shao et al. (2011)
Cantharellus vaginatus	HKAS 55731	Yunnan, SW China	HM594682	—	Shao et al. (2011)
Cantharellus vaginatus	LWF-1-1 (FHMU6851)	Zhejiang, Eastern China	OM691484	OM811325	Present study
Cantharellus vaginatus	LWF-1-2 (FHMU6852)	Zhejiang, Eastern China	OM691485	OM811326	Present study
Cantharellus vaginatus	M.S. Su201 (FHMU6853)	Jiangxi, Eastern China	OM691486	OM811327	Present study
Cantharellus vaginatus	M.S. Su200 (FHMU6855)	Jiangxi, Eastern China	OM691492	OM811333	Present study
Cantharellus vaginatus	N.K. Zeng3000 (FHMU1961)	Hainan, Southern China	OM691487	OM811328	Present study
Cantharellus vaginatus	N.K. Zeng3009 (FHMU1970)	Hainan, Southern China	OM691488	OM811329	Present study
Cantharellus vaginatus	N.K. Zeng2281 (FHMU1533)	Hainan, Southern China	OM691489	OM811330	Present study
Cantharellus vaginatus	N.K. Zeng2521 (FHMU1638)	Hainan, Southern China	OM691490	OM811331	Present study
Cantharellus vaginatus	Z.H. Chen MHHNU31942 (FHMU6854)	Hunan, Central China	OM691491	OM811332	Present study
Cantharellus velutinus	BB 14.038 (PC0142227)	United States	KX896789	KX857049	Buyck et al. (2016b)
Cantharellus velutinus	WR WV07.074	United States	—	KX857068	Buyck et al. (2016b)
Cantharellus velutinus	DM WV13.36	United States	—	KX857070	Buyck et al. (2016b)
Cantharellus versicolor	KUN-HKAS 55761	Yunnan, SW China	—	KM893856	Shao et al. (2016b)
Cantharellus versicolor	KUN-HKAS 58242	Yunnan, SW China	—	KM893857	Shao et al. (2016b)
Cantharellus violaceovinosus	Bandala 4513	Mexico	MF616524	MF616520	Herrera et al. (2018)
Cantharellus violaceovinosus	Corona 648	Mexico	MF616525	MF616521	Herrera et al. (2018)
Cantharellus yunnanensis	XieXD174	Yunnan, SW China	KU720333	KU720337	Unpublished
Cantharellus yunnanensis	ZhangJP117	Yunnan, SW China	KU720336	—	Unpublished
Cantharellus yunnanensis	SSC 1	Yunnan, SW China	—	KM893834	Shao et al. (2021)
Cantharellus yunnanensis	N.K. Zeng2778(FHMU1767)	Hainan, Southern China	OK570080	OK562592	Tian et al. (2022)
Cantharellus yunnanensis	N.K. Zeng2777 (FHMU1766)	Yunnan, SW China	OM319633	—	Present study
Cantharellus yunnanensis	N.K. Zeng4084 (FHMU3735)	Guangdong, Southern China	OM319632	OM811337	Present study
Cantharellus yunnanensis	N.K. Zeng5040 (FHMU6841)	Yunnan, SW China	OM319634	OM321043	Present study
Cantharellus yunnanensis	N.K. Zeng3875 (FHMU6842)	China	OM319635	OM321044	Present study
Cantharellus yunnanensis	Z.H. Chen MHHNU31318 (FHMU6843)	Yunnan, SW China	OM319636	OM321045	Present study
Cantharellus yunnanensis	Z.H. Chen MHHNU32137 (FHMU6844)	Hubei, Central China	OM319637	OM321046	Present study
Cantharellus yunnanensis	Yuan 13983	China	MW979527	MW999428	Cao et al. (2021)
Cantharellus yunnanensis	Yuan 13985	China	MW979528	MW999429	Cao et al. (2021)
Cantharellus yunnanensis	Yuan 14539	China	MW979514	MW999422	Cao et al. (2021)
Cantharellus yunnanensis	Yuan 14636	China	MW979515	MW999423	Cao et al. (2021)

GenBank numbers in bold indicate the newly generated sequences; SW Southwestern China, NE Northeastern China.

Phylogenetic Analyses

The combined nuclear dataset (28S + TEF1) was analyzed using maximum likelihood (ML) and Bayesian inference (BI). Maximum likelihood tree generation and bootstrap analyses were performed with the program RAxML7.2.6 (Stamatakis, 2006) running 1,000 replicates combined with an ML search. Bayesian analysis with MrBayes 3.1 (Huelsenbeck and Ronquist, 2005) implementing the Markov chain Monto Carlo (MCMC) technique and parameters predetermined with MrModeltes 2.3 (Nylander, 2004) was performed. The best-fit likelihood model of 28S and TEF1 was GTR + I + G and SYM + I + G, respectively. Bayesian analysis of the combined nuclear dataset (28S + TEF1) was repeated for 20 million generations and sampled every 100 generations. Trees sampled from the first 25% of the generations were discarded as burn-in, and Bayesian posterior probabilities (PP) were then calculated for a majority consensus tree of the retained Bayesian trees. Runs were terminated once the average standard deviation of split frequencies went below 0.01.

Results

Molecular Data

The combined dataset (28S + TEF1) of subg. Cantharellus consisted of 129 taxa and 1,707 nucleotide sites, and the alignment was submitted to TreeBase (S29413). The phylogram with branch lengths generated from RAxML and support values is shown in Figure 2. The topologies of the phylogenetic trees based on the combined dataset generated from ML and BI analyses were almost identical, but there was a slight variation in statistical support.

FIGURE 2

Phylogram inferred from a combined dataset (28S and TEF1) of the Cantharellus subg. Cantharellus using RAxML. RAxML likelihood bootstrap (BS ≥ 50%) and Bayesian posterior probabilities (PP ≥ 0.95) are indicated above or below the branches as RAxML BS/PP.

The present molecular data indicate that the Chinese species of subg. Cantharellus were grouped into fourteen independent lineages (Figure 2). A total of seven new lineages were identified in this study (Lineages 1–7 of Figure 2). Lineage 1 was comprised of one collection (FHMU6845) from central China; lineage 2 was comprised of one material (FHMU4592) from southern China; lineage 3, with strong statistical support (BS = 100%, PP = 1.0), was comprised of eleven collections (FHMU5335, FHMU6846, FHMU6847, FHMU1703, FHMU5260, FHMU6848, FHMU6849, FHMU2412, FHMU2839, FHM3236, and FHMU5268) from southern China; lineage 4, with high statistical support (BS = 98%, PP = 1.0), was comprised of two specimens (FHMU3749 and FHMU3759) both from central China; lineage 5, with strong statistical support (BS = 100%, PP = 1.0), was comprised of two materials (FHMU1987 and FHMU6850) from southern China and eastern China, respectively; lineage 6 was comprised of one collection (FHMU5266) from southern China; and lineage 7 was comprised of one specimen (FHMU3834) also from southern China (Figure 2).

Taxonomy

N.K. Zeng, Y.Z. Zhang, and W.F. Lin, sp. nov.

Figures 3A,B, 4.

FIGURE 3

Basidiomata of Cantharellus subg. Cantharellus species. (A,B) Cantharellus albopileatus (A) FHMU1987, holotype; (B) FHMU6850; (C–E) Cantharellus chuiweifanii (C,D) FHMU5335; (E) FHMU2839; (F,G) Cantharellus pinetorus (F) FHMU3759, holotype; (G) FHMU3749; (H) Cantharellus ravus (FHMU6845, holotype). Photographs: (A,C–H) N. K. Zeng; (B) W. F. Lin.

FIGURE 4

Microscopic features of Cantharellus albopileatus (FHMU1987, holotype). (A) Basidiospores. (B) Basidia. (C) Pileipellis. Scale bars = 10 μm. Drawings by Y. Z. Zhang.

MycoBank: MB843063

Diagnosis: It differs from other species of subg. Cantharellus by a cream to off-white basidioma, a well-developed hymenophore, and ellipsoid basidiospores.

Etymology: Latin “albo-” means white, “pileatus” means pileus, referring to the off-white pileus of our new species.

Holotype: China. Hainan Province: Yinggeling of Hainan Tropical Rainforest National Park, elev. 750 m, 28 May 2017, N. K. Zeng3026 (FHMU1987). GenBank accession number: 28S = OM691480, ITS = OM835804, TEF1 = OM811321.

Basidiomata are very small to small-sized. Pileus is 2.5–5 cm in diameter and convex with a depressed center; the margin was strongly incurved, irregular, often wavy, and lobed; the surface is smooth, slightly greasy, and cream (3A1) to off-white (4A1) in color; the context above stipe was 0.3 cm in thickness, whitish (4A1), unchanging in color when injured. Hymenophore is composed of relatively well-developed, decurrent gill folds, branched to furcate, which becomes strongly intervened with age; these folds are about 0.1 cm broad and are yellowish (2A2) to white (4A1) in color. Stipe is 2–3 × 0.4–0.6 cm, central, subcylindrical, young solid, hollowing with age, and curved at the base; the surface was dry, whitish (4A1) to very pale cream (3A1), and nearly concolorous with hymenophore; the context is fleshy, firm, and whitish (3A1). Taste and odor is not distinctive. Spore print is not obtained.

Basidiospores [40/2/2] 6–7.18–8 × 5–5.46–6(–6.5) μm, Q = (1.09–)1.15–1.50(–1.6), Q = 1.32 ± 0.12, are ellipsoid, smooth, slightly thick-walled (0.5 μm), yellowish in KOH. Basidia is 43–65 × 5–10 μm, narrowly clavate, slightly thick-walled (up to 0.5 μm), 4-5-6-spored, and yellowish in KOH; sterigmata is 4–6 μm in length. Cystidia is absent. Pileipellis has a cutis that is 30–70 μm thick, is composed of mostly interwoven, cylindrical hyphae, is 6–12 μm wide, is thick-walled (up to 1 μm), and is faintly pale yellow in KOH; terminal cells are 21–108 × 5–10 μm in length, thin to slightly thick-walled (up to 0.5 μm), subcylindrical to subclavate, with obtuse apex. Clamp connections are present in all parts of basidioma.

Habitat: Solitary, scattered, or gregarious on the ground in forests dominated by fagaceous trees such as Castanopsis fissa (Champion ex Bentham) Rehder et E. H. Wilson.

Known distribution: southern and eastern China.

Other specimens were examined: China. Zhejiang Province: Hangzhou City, Tianmushan Nature Reserve, elev. 1100 m, 22 July 2020, W. F. Lin7 (FHMU6850).

Notes: Cantharellus albus S. P. Jian and B. Feng, originally described from Yunnan, southwestern China, has a white basidioma. However, by presenting the features such as a stipe turning yellow when bruised and a lower value of Q, it is a member of subg. Parvocantharellus Eyssart. and Buyck (Jian et al., 2020). The white basidioma makes Cantharellus albopileatus somewhat similar to the American Cantharellus subalbidus A. H. Sm. and Morse; however, this latter species in addition to being associated with trees of Pinaceae (Smith and Morse, 1947) possesses larger basidioma [pileus 5–10 (–14) cm], and it is also distinctly differentiated at the molecular level (Figure 2).

In the phylogenetic analyses, Cantharellus albopileatus forms a well-supported (BS = 100%, PP = 1.0) monophyletic clade, together with the newly described Cantharellus chuiweifanii, equally a tropical species, and Cantharellus pinetorus from central China (Figure 2), which is quite different from any of the other northern hemisphere species in subg. Cantharellus. However, Cantharellus pinetorus is associated with trees of Pinaceae (refer to the descriptions under Cantharellus pinetorus); both Cantharellus pinetorus and Cantharellus chuiweifanii have a yellow pileus (refer to the descriptions under Cantharellus chuiweifanii).

N.K. Zeng, Y.Z. Zhang, and Zhi Q. Liang, sp. nov.

Figures 3C–E, 5.

FIGURE 5

Microscopic features of Cantharellus chuiweifanii (FHMU2412, holotype). (A) Basidiospores. (B) Basidia. (C) Pileipellis. Scale bars = 10 μm. Drawings by Y. Z. Zhang and D. Y. An.

MycoBank: MB843062

Diagnosis: It differs from other species of subg. Cantharellus by an egg-yolk yellow to bright yellow, shiny pileus, a whitish stipe, a well-developed hymenophore, ellipsoid basidiospores, and a distribution in tropical Asia.

Etymology: Latin “chuiweifanii” is named after Chinese mycologist W. F. Chiu; for that, he published the first new species of Cantharellus in China, i.e., Cantharellus yunnanensis.

Holotype: China. Hainan Province: Limushan of Hainan Tropical Rainforest National Park, elev. 650 m, 11 May 2014, N. K. Zeng1524 (FHMU2412). GenBank accession number: 28S = OM717953, TEF1 = OM811347.

Basidiomata are very small to medium-sized. Pileus is 2–5 cm in diameter and plano-convex at first but soon depressed in the center; the margin was first very regular and strongly incurved and then became more wavy, the surface is smooth, pale yellow, egg-yolk yellow (1A5) to bright yellow (1A7), sometimes tinged with brownish, and shiny in color; the context above stipe was 0.05–0.15 cm in thickness, yellowish (3A3) to orange yellow (3A8), but unchanging in color when injured. Hymenophore is composed of well-developed, decurrent, well-spaced, and unequal gill folds, especially near the extreme cap margin with many very short lamellulae or also often forked; these folds are 0.1–0.2 cm broad and are pale yellow, egg-yolk yellow (1A4) to orange yellow in color (2A7). Stipe is 1.2–4 × 0.4–1.0 cm, central, cylindrical; surface dry, whitish (5A1), or yellowish-brown (1A2) in color; the context is fleshy, firm, and yellowish (2A2). Taste and odor is not distinctive. Spore print is not obtained.

Basidiospores [173/18/11] 6–7.05–8 × 4.5–5.03–5.5(–6) μm, Q = (1.18–)1.27–1.60(–1.67), Q = 1.41 ± 0.10, are ellipsoid, smooth, slightly thick-walled (0.5 μm), yellowish in KOH. Basidia is –57-67 × 8-10 long, narrow, subcylindric, slightly thick-walled (0.5–0.7 μm), 4-5-6-spored, yellowish in KOH; sterigmata is 5–7 μm in length. Cystidia is absent. Pileipellis has a cutis that is 70–180 μm thick, is composed of mostly interwoven, cylindrical hyphae, is 5–8 μm wide, is slightly thick-walled (0.5–0.8 μm), and is faintly pale yellow in KOH; terminal cells are 52–148 × 4–7 μm in length, slightly thick-walled (0.5–0.8 μm), subcylindrical to subclavate, with obtuse apex. Clamp connections are present in all parts of basidioma.

Habitat: Solitary, scattered, or gregarious on the ground in forests dominated by fagaceous trees such as Lithocarpus spp.

Known distribution: southern China.

Other specimens were examined: China. Hainan Province: Yinggeling of Hainan Tropical Rainforest National Park, elev. 750 m, 5 August 2015, N. K. Zeng2608 (FHMU1703); Jianfengling of Hainan Tropical Rainforest National Park, elev. 850 m, 27 June 2018, N. K. Zeng3392 (FHMU5268); same location, 28 June 2018, N. K. Zeng3452, 3463, 3474 (FHMU5260, FHMU2839, FHMU5335); same location, 10 August 2020, N. K. Zeng4558, 4559 (FHMU6848, FHMU6847); same location, 11 August 2020, N. K. Zeng4596 (FHMU6846); same location, 29 July 2021, N. K. Zeng5322 (FHMU3236); Wanning County, Bofangling, elev. 70 m, 29 August 2020, N. K. Zeng4897 (FHMU6849).

Notes: Cantharellus chuiweifanii looks like Cantharellus subcibarius Corner and Cantharellus yunnanensis. However, Cantharellus subcibarius has a yellow stipe, a context turning yellow to orange-brown when bruised, and larger basidiospores [(7.3–)7.5–7.89–8.3(–8.5) × (5.2–)5.6–6.10–6.5(–6.9) μm, Q = (1.12–)1.23–1.30–1.36(–1.40)] (Corner, 1966; Buyck et al., 2021); Cantharellus yunnanensis has a yellow stipe, wider basidiospores measuring (6.5–)7–8(–8.5) × 5–6(–6.5) μm (Shao et al., 2021), and it is also distinctly differentiated at the molecular level (Figure 2). Cantharellus chuiweifanii is phylogenetically associated with Cantharellus albopileatus and Cantharellus pinetorus (Figure 2), and the differences in the three taxa have been discussed under Cantharellus albopileatus.

N.K. Zeng, Y.Z. Zhang and Zhi Q. Liang, sp. nov.

Figures 3F,G, 6.

FIGURE 6

Microscopic features of Cantharellus pinetorus (FHMU3759, holotype). (A) Basidiospores. (B) Basidia. (C) Pileipellis. Scale bars = 10 μm. Drawings by Y. Z. Zhang.

MycoBank: MB843064

Diagnosis: It differs from other species of subg. Cantharellus by a bright yellow to orange-yellow pileus, a cream to grayish yellow stipe, a well-developed hymenophore, broadly ellipsoid to ellipsoid basidiospores, and it is associated with pine trees.

Etymology: Latin “pinetorus” refers to the association of the new species with pine forests.

Holotype: China. Hunan Province: Yizhang County, Mangshan National Nature Reserve, elev. 750 m, 30 July 2019, N. K. Zeng4180 (FHMU3759). GenBank accession number: 28S = OM691482, TEF1 = OM811323.

Basidiomata are small to medium-sized. Pileus is 3.5–5 cm in diameter and convex when young and then applanate with depressed center; the surface is smooth, bright yellow (3A5) to orange-yellow in color (3A6); the margin is incurved and irregularly wavy; the context above stipe is 0.35–0.55 cm in thickness, yellow (3A7), but unchanging in color when injured. Hymenophore is veined and decurrent; these folds are 0.05–0.2 cm broad and are lemon yellow (1A6) to pale yellow in color (4A2). Stipe is 2.5–3 × 0.5–0.6 cm, cylindrical, central, and hollow; the surface is dry and cream (4A1) to grayish yellow (4A2) in color; the context is white (3A2). Taste and odor is not distinctive. Spore print is not obtained.

Basidiospores [40/2/2] 6–6.98–7.5(–8) × 5–5.36–6 μm, Q = (1.09–)1.17–1.5, Q = 1.30 ± 0.09, are broadly ellipsoid to ellipsoid, smooth, slightly thick-walled (0.5 μm), yellowish in KOH. Basidia is 57–68 × 4–10 μm, long, narrow, subcylindric, slightly thick-walled (up to 0.5 μm), 3-4-5-spored, and yellowish in KOH; sterigmata is 2–4 μm in length. Cystidia is absent. Pileipellis has a cutis that is 100–150 μm thick, is composed of mostly interwoven, cylindrical hyphae, is 6–9 μm wide, is slightly thick-walled (up to 0.5 μm), and is faintly pale yellow in KOH; terminal cells are 40–61 × 4–6 μm in length, slightly thick-walled (0.5–0.7 μm), subcylindrical to subclavate, with obtuse apex. Clamp connections are present in all parts of basidioma.

Habitat: Solitary, scattered, or gregarious on the ground, in forests dominated by Pinus massoniana Lamb.

Known distribution: central China.

Other specimens were examined: China. Hunan Province: Yizhang County, Mangshan National Nature Reserve, elev. 750 m, 30 July 2019, N. K. Zeng4181 (FHMU3749).

Notes: Malaysian Cantharellus ianthinus Corner and Cantharellus subcibarius are morphologically similar to Cantharellus pinetorus. However, Cantharellus ianthinus has purple fibrils on the surfaces of the pileus and stipe, and larger basidiospores measuring 8–10.5 × 5.5–7 μm (Corner, 1966); Cantharellus subcibarius has a context turning yellow to orange-brown when bruised, and it is not associated with trees of Pinaceae (Corner, 1966; Buyck et al., 2021). In the phylogenetic analyses, Cantharellus pinetorus is allied with Cantharellus albopileatus and Cantharellus chuiweifanii (Figure 2), the differences in the three taxa have been discussed under Cantharellus albopileatus.

N.K. Zeng, Y.Z. Zhang, and Zhi Q. Liang, sp. nov.

Figures 3H, 7.

FIGURE 7

Microscopic features of Cantharellus ravus (FHMU6845, holotype). (A) Basidiospores. (B) Basidia. (C) Pileipellis. Scale bars = 10 μm. Drawings by Y. Z. Zhang.

MycoBank: MB843065

Diagnosis: It differs from other species of subg. Cantharellus by a yellowish to grayish yellow, dull pileus, a well-developed hymenophore, and ellipsoid basidiospores.

Etymology: Latin “ravus” refers to the grayish yellow basidioma of our new species.

Holotype: China. Hunan Province: Yizhang County, Mangshan National Nature Reserve, elev. 550 m, 29 July 2019, N. K. Zeng4176 (FHMU6845). GenBank accession number: 28S = OM717944, TEF1 = OM811338.

Basidiomata are small to medium-sized. Pileus is 3.5–8 cm in diameter and plano-convex to infundibuliform; the surface is smooth, yellowish (1A2) to grayish yellow (2A4) in color, and dull; the margin is incurved or downward; the context above stipe is about 0.3 cm in thickness, yellowish (3A3), unchanging in color when injured. Hymenophore is veined and decurrent; these folds are about 0.1 cm high, forking, creamy yellow (1A4) to yellowish (3A2) in color. Stipe is 3–4 × 0.6–0.9 cm, central, cylindrical; surface dry, grayish yellow to fulvous (4A4), but whitish (5A1) at base. Taste and odor is not distinctive. Spore print is not obtained.

Basidiospores [37/2/1] (6–)6.5–7.04–7.5 × 4.5–5.24–5.5 μm, Q = (1.18–)1.2–1.5(–1.56), Q = 1.35 ± 0.08, are ellipsoid, smooth, slightly thick-walled (0.5 μm), yellowish in KOH. Basidia is 45–63 × 8–9 μm, long, narrow, subcylindric, slightly thick-walled (up to 0.5 μm), 4-5-6 spored, yellowish in KOH; sterigmata is 6–8 μm in length. Cystidia is absent. Pileipellis has a cutis composed of mostly cylindrical, that is 5–12 μm wide, is slightly thick-walled (up to 1 μm) hyphae, and is faintly pale yellow in KOH; terminal cells are 45–82 × 6–10 μm, slightly thick-walled (0.5–0.7 μm), subcylindrical to subclavate, with obtuse apex. Clamp connections are present in all parts of basidioma.

Habitat: Gregarious on the ground in forests dominated by fagaceous trees such as Lithocarpus spp.

Known distribution: central China.

Notes: Cantharellus subcibarius and Cantharellus yunnanensis are also morphologically similar to our new species. However, both Cantharellus subcibarius and Cantharellus yunnanensis have shiny pileal surfaces. Moreover, Cantharellus subcibarius has a context turning yellow to orange-brown when bruised, and larger basidiospores [(7.3–)7.5–7.89–8.3(–8.5) × (5.2–)5.6–6.10–6.5(–6.9) μm, Q = (1.12–)1.23–1.30–1.36(–1.40)] (Corner, 1966; Buyck et al., 2021); Cantharellus yunnanensis also has larger basidiospores measuring (6.5–) 7–8 (–8.5) × 5–6 (–6.5) μm (Shao et al., 2021), and it is distinctly differentiated at the molecular level (Figure 2). Our molecular data also indicated that Cantharellus ravus is closely related to the North American Cantharellus californicus D. Arora and Dunham and Cantharellus velutinus Buyck and V. Hofst (Figure 2). However, Cantharellus californicus has much larger basidiospores measuring 7–9.30–12 μm × 5–6.45–8 μm (Arora and Dunham, 2008); Cantharellus velutinus, a very variable species with yellow to pink fruiting bodies and pubescent pileus surface, has longer but narrower basidiospores measuring (6.7–)7.3–7.84–8.4(–9.2) × (3.7–)4.2–4.61–5.0(–5.2) μm and hyphal extremities of the pileipellis with conspicuously thickened cell walls (Buyck et al., 2016b).

Discussion

Morphological Features and Hosts of Cantharellus Subgenus Cantharellus

In agreement with the previous hypotheses (Buyck et al., 2014), most species in China have nearly glabrous pileus, with the exception of Cantharellus vaginatus S. C. Shao, X. F. Tian, and P. G. Liu and Cantharellus versicolor S. C. Shao and P. G. Liu having a squamulose cap (Shao et al., 2011, 2016b). As noted by Buyck et al. (2014), most taxa in subg. Cantharellus have yellow pileus. In China, Cantharellus chuiweifanii, Cantharellus cibarius Fr, Cantharellus hainanensis N. K. Zeng, Zhi Q. Liang, and S. Jiang, Cantharellus laevihymeninus T. Cao and H. S. Yuan, Cantharellus macrocarpus N. K. Zeng, Y. Z. Zhang, and Zhi Q. Liang, Cantharellus pinetorus, Cantharellus ravus, Cantharellus vaginatus, and Cantharellus yunnanensis also have pilei colored with yellow; Cantharellus albopileatus is characterized with white pileus; squamules on pileal surface of Cantharellus vaginatus are fulvous to brown (Shao et al., 2011), and sandy brown to dark brown in Cantharellus versicolor was observed (Shao et al., 2016b).

Besides macro-morphology, some micro-morphological features can also be used to discriminate subg. Cantharellus species. For example, species of the subgenus usually have abundant clamps, and hyphal endings in pileipellis are mostly thick-walled (Buyck et al., 2014). Our four new species and previous taxa of subg. Cantharellus in China also possess clamp connections and thick-walled hyphal endings in pileipellis (Shao et al., 2011, 2016b,2021; An et al., 2017; Cao et al., 2021; Zhang Y. Z. et al., 2021).

In regard to ecological preference, many species such as Cantharellus altipes Buyck and V. Hofst, Cantharellus macrocarpus, and Cantharellus tenuithrix Buyck and V. Hofst were reported to grow in pine-oak woods (Buyck and Hofstetter, 2011; Shao et al., 2021; Zhang Y. Z. et al., 2021). In China, Cantharellus cibarius, Cantharellus vaginatus, and Cantharellus yunnanensis were also reported to grow in pine-oak forests (Shao et al., 2011, 2021); Cantharellus albopileatus, Cantharellus chuiweifanii, Cantharellus hainanensis, and Cantharellus ravus grow in forests dominated by fagaceous trees, whereas Cantharellus pinetorus and Cantharellus versicolor are associated with trees of Pinaceae (Shao et al., 2011, 2016b; An et al., 2017).

Most species of subg. Cantharellus sections Cantharellus and Amethystini Buyck and V. Hofstetter have well-developed hymenophore, section Sublaeves Buyck and V. Hofstetter harbors taxa with smooth hymenophore, and section Amethystini Buyck and V. Hofstetter usually has a pileus with appressed squama. Judging from the positions of our new species and Chinese previous taxa in the molecular phylogenetic tree (Figure 2), plus the morphological features, Cantharellus cibarius, Cantharellus macrocarpus, Cantharellus ravus, Cantharellus versicolor, and Cantharellus yunnanensis are the members of section Cantharellus, Cantharellus hainanensis, and Cantharellus laevihymeninus, also have ill-developed hymenophore (An et al., 2017; Cao et al., 2021), and belong to the section Sublaeves. Cantharellus vaginatus is a member of section Amethystini, and Cantharellus albopileatus, Cantharellus chuiweifanii, and Cantharellus pinetorus probably represent a new section, which will be further studied in the future.

Species Diversity of Cantharellus Subgenus Cantharellus

High species diversity of subg. Cantharellus in China was revealed in this study, and fourteen lineages were identified (Figure 2). A total of four (lineages 1, 3–5 of Figure 2) were here described as new species: Cantharellus albopileatus, Cantharellus chuiweifanii, Cantharellus pinetorus, and Cantharellus ravus; others represent previously described taxa: Cantharellus cibarius, Cantharellus hainanensis, Cantharellus laevihymeninus, Cantharellus macrocarpus, Cantharellus vaginatus, Cantharellus versicolor, and Cantharellus yunnanensis, whereas three lineages (lineages 2, 6–7 of Figure 2) remain still undescribed.

Up to now, taxa in subg. Cantharellus are all from northern hemisphere (Buyck et al., 2014). Most species of the subgenus included in the present dataset are from temperature areas of northern hemisphere including North America and Europe (Figure 2). In China, with the exception of Cantharellus cibarius and Cantharellus versicolor in temperate areas, most species, viz. Cantharellus albopileatus, Cantharellus chuiweifanii, Cantharellus hainanensis, Cantharellus macrocarpus, Cantharellus pinetorus, Cantharellus ravus, Cantharellus vaginatus, and Cantharellus yunnanensis, occur in subtropical or tropical China. With more field investigations, more taxa of the subgenus will be uncovered in the subtropical and tropical regions.

Phylogenetic Relationships and Geographic Divergence of Chinese Cantharellus Subgenus Cantharellus

Our molecular data based on two-locus DNA sequences (28S + TEF1) with many new specimens from China have contributed to our knowledge of subg. Cantharellus.

It is clear that there are several clades having taxa from both sides of the Pacific, and allied species from East Asia and North America are obviously inferred from this molecular phylogenetic tree (Figure 2). For example, Chinese Cantharellus versicolor is related to North American Cantharellus camphoratus R. H. Petersen and Cantharellus formosus Corner; our new species Cantharellus ravus is affiliated with Cantharellus californicus and Cantharellus velutinus, two species both described from United States; one collection tentatively named C. sp. (FHMU3834) appears closely related to North American-type collection of Cantharellus spectaculus Foltz and T. J. Volk (Figure 2), which is an earlier synonym of Cantharellus persicinus Petersen (Buyck et al., 2016c). Our study did not identify disjunct populations of the same purported taxon in the two areas (Figure 2). Similar scenarios have been documented for many other fungi (Zhang et al., 2004; Zeng et al., 2013, 2016).

Biogeographic connections between East Asia and Europe have also been discussed in other fungi such as Amanita Pers., Phylloporus Quél. and Rhodotus Maire (Zhang et al., 2004; Zeng et al., 2013; Tang et al., 2014). In this study, we found that Cantharellus cibarius occurs in northeastern China and Europe (Figure 2).

In addition, we also noted that Cantharellus hainanensis is associated with one specimen labeled as Cantharellus lateritius from India (Figure 2). Besides northeastern China and Europe, the geographical distribution range of Cantharellus cibarius also extends to Japan (Figure 2).

Data Availability Statement

The data presented in the study are deposited in the https://www.ncbi.nlm.nih.gov/GenBank and https://www.mycobank.org/page/Home/MycoBank repository, accession number of GenBank (28S: OM319632-OM319637, OM691480-OM691495, OM717944-OM717956; TEF1: OM321043-OM321046, OM811321-OM811350; and ITS: OM835791-OM835808) and MycoBank (MB843062-MB843065).

Author Contributions

Z-QL and N-KZ contributed to the conceptualization. Y-ZZ performed the methodology, wrote the original draft preparation, and carried out the formal analysis. Y-ZZ and D-YA performed the experiment. N-KZ, W-FL, M-SS, Z-HC, PZ, and SJ carried out the resources. N-KZ, BB, and Z-QL wrote, reviewed, and edited the manuscript. N-KZ and Z-QL supervised the data. N-KZ carried out the project administration and funding acquisition. All authors contributed to the article and approved the submitted version.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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