Taxonomy and Phylogeny of Peniophora Sensu Lato (Russulales, Basidiomycota)

Abstract

Peniophora is an old corticioid genus, from which two small satellite genera, Dendrophora and Duportella, were derived based on morphological differences. Molecular systematic studies showed that they belong to Peniophoraceae, Russulales, but the inter- and intra-generic phylogenetic relationships are still unclear. Moreover, the species diversity of this group in subtropical and tropical Asia has not been sufficiently investigated and studied. In this study, we carried out an intensive taxonomic and phylogenetic study on Peniophora sensu lato based on analyses of concatenated ITS1-5.8S-ITS2 (ITS, Internal Transcribed Spacer) and 28S (D1–D2 domains of nuc 28S rDNA) sequence data of all available species worldwide. In the phylogenetic trees, species of Peniophora s. l. (sensu lato) including types of Peniophora s.s. (sensu stricto), Dendrophora and Duportella were interspersed within a strongly supported clade. It means that the morphological delimitations of the three genera are not reliable, and they should be regarded as a large genus. As a result, eight species of Duportella were transferred to Peniophora, although five of them have not been sequenced. Four new distinct lineages, corresponding to Peniophora cremicolor, P. major, P. shenghuae and P. vietnamensis spp. nov., were recovered in the trees. Peniophora taiwanensis is treated as a later synonym of P. malaiensis based on morphological and molecular evidence. Duportella renispora is excluded from Peniophoraceae, because BLAST results of the ITS and 28S sequences of the holotype showed that it is closely related to Amylostereum. Descriptions and illustrations are provided for the four new species, and an identification key is given for all 25 species of Peniophora in China. Our results indicated that the species diversity of the corticioid fungi in Asia is rich and deserves further study.

1. Introduction

The genus Peniophora Cooke (Peniophoraceae, Russulales) introduced in 1879, typified by Thelephora quercina Pers. ex Fr., is one of the oldest genera of corticioid fungi. It is a cosmopolitan genus with a wide distribution from boreal to tropical areas, causing a white rot on both angiosperms and gymnosperms. Species of the genus prefer to grow on small branches especially those dead but still attached ones in the exposed and dry environments. At the beginning, mycologists adopted a broad concept, and many unrelated species were described in the genus. It includes 639 names in Index Fungorum (http://www.indexfungorum.org/Names/Names.asp, accessed on 20 November 2022), but most species have been moved to other genera, and the morphological circumscription of Peniophora has been narrowed [1]. Meanwhile, some intra-generic taxa were proposed and used, and two satellite genera Duportella Pat. and Dendrophora (Parmasto) Chamuris were separated from Peniophora s.l. and accepted by many mycologists [2,3,4,5]. In the morphological monograph of Peniophoraceae [5], Andreasen and Hallenberg accepted 70 species of Peniophora s.s., 12 species of Duportella and 2 species of Dendrophora and provided keys and descriptions for all the genera and species.

According to the modern concept, Peniophora s.s. includes species possessing resupinate basidiomes with a smooth hymenophore, a monomitic hyphal system with simple-septate or nodose-septate generative hyphae, both encrusted cystidia and gloeocystidia, and thin-walled, smooth basidiospores negative in Melzer’s reagents. Dendrophora differs from Peniophora s.s. by having effused-reflexed basidiomes and the presence of brown, thick-walled dendrohyphidia, while Duportella differs by the presence of brown lamprocystidia and skeletal hyphae (in some species). However, there are usually morphological overlaps among the three genera. Based on the analyses of ITS sequences of Aphyllophorales, Boidin et al. [4] found that species of Peniophora s.l. formed a relatively strongly supported group that they named ‘Peniophorales’. Later, phylogenetic studies showed that Peniophora s.l. belongs to Peniophoraceae, Russulales [6,7,8]. Nevertheless, no comprehensive molecular studies have been carried out for Peniophora s.l., and the inter- and intra-generic phylogeny is not clear.

The ITS and 28S sequences of many species of Peniophora s.l. including some from type specimens were released in GenBank by Vu et al. [9] and thus made it possible to study the phylogeny of this group. In this paper, we studied the taxonomy and phylogeny of Peniophora s.l. by adding many sequence data of species from Asia, which was shown to be rich in the species diversity of this group [10,11,12,13,14,15,16]. We aim to resolve the phylogenetic relationships among Peniophora s.s., Dendrophora and Duportella, and explore the species diversity in China. This research is a part of the studies of species diversity, taxonomy and phylogeny of corticioid fungi in China.

2. Materials and Methods

2.1. Morphological Studies

Voucher specimens and strains are deposited at the herbaria of Beijing Forestry University, Beijing, China (BJFC) and Centre for Forest Mycology Research, U.S. Forest Service, Madison, Wisconsin, USA (CFMR). Freehand sections were made from dried basidiomes and mounted in 2% (w/v) potassium hydroxide (KOH) with 1% (w/v) phloxine, Melzer’s reagent (IKI) or cotton blue (CB). Microscopic examinations were carried out with a Nikon Eclipse 80i microscope (Nikon Corporation, Tokyo, Japan) at magnifications up to 1000×. Drawings were made with the aid of a drawing tube. The following abbreviations are used: L = mean spore length, W = mean spore width, Q = L/W ratio, n (a/b) = number of spores (a) measured from number of specimens (b). Color codes and terms follow Kornerup and Wanscher [17].

2.2. DNA Extraction and Sequencing

A CTAB plant genomic DNA extraction Kit DN14 (Aidlab Biotechnologies Co., Ltd., Beijing, China) was used to extract total genomic DNA from dried specimens which were then amplified by the polymerase chain reaction (PCR), according to the manufacturer’s instructions. The ITS1-5.8S-ITS2 region was amplified with the primer pair ITS5/ITS4 [18] using the following protocol: initial denaturation at 95 °C for 4 min, followed by 34 cycles at 94 °C for 40 s, 58 °C for 45 s and 72 °C for 1 min, and final extension at 72 °C for 10 min. The 28S D1-D2 region was amplified with the primer pair LR0R/LR7 [19] employing the following procedure: initial denaturation at 94 °C for 1 min, followed by 34 cycles at 94 °C for 30 s, 50 °C for 1 min and 72 °C for 1.5 min, and final extension at 72 °C for 10 min. DNA sequencing was performed at Beijing Genomics Institute, and the newly generated sequences were deposited in GenBank (Table 1). BioEdit v.7.0.5.3 [20] was used to review the chromatograms and for contig assembly.

2.3. Phylogenetic Analyses

The molecular phylogenetic analyses were inferred from two separate concatenated ITS-28S sequences datasets of species in the Peniophoraceae and Peniophora s.l., respectively. Amylostereum chailletii (Pers.) Boidin was elected as the outgroup for the Peniophoraceae dataset, whilst Confertobasidium olivaceoalbum (Bourdot & Galzin) Jülich and Metulodontia nivea (P. Karst.) Parmasto were used for the Peniophora s.l. dataset. The ITS and 28S sequences were aligned separately using MAFFT v.7 [21] with the G-INS-I iterative refinement algorithm and optimized manually in BioEdit v.7.0.5.3. The separate alignments were then concatenated using Mesquite v.3.5.1 [22].

Maximum parsimony (MP), maximum likelihood (ML) analyses and Bayesian inference (BI) were carried out by using PAUP* v.4.0b10 [23], RAxML v.8.2.10 [24] and MrBayes 3.2.6 [25], respectively. In MP analysis, trees were generated using 100 replicates of the random stepwise addition of sequence and tree-bisection reconnection (TBR) branch-swapping algorithm with all characters given equal weight. Branch supports for all parsimony analyses were estimated by performing 1000 bootstrap replicates with a heuristic search of 10 random-addition replicates for each bootstrap replicate. In ML analysis, statistical support values were obtained using rapid bootstrapping with 1000 replicates, with default settings used for other parameters. For BI, the best-fit substitution model was estimated with jModeltest v.2.17 [26]. Four Markov chains were run for 0.3 and 20 million generations for the Peniophoraceae and Peniophora s.l. datasets, respectively, until the split deviation frequency values were lower than 0.01. Trees were sampled every 100 generations. The first quarter of the trees, which represented the burn-in phase of the analyses, were discarded, and the remaining trees were used to calculate posterior probabilities (BPP) in the majority rule consensus tree.

3. Results

3.1. Phylogenetic Analyses

Thirty-nine ITS and 39 28S sequences were newly generated in this study (Table 1). The Peniophoraceae dataset contained 33 ITS and 34 28S sequences from 34 samples representing 13 genera and the outgroup, and it had an aligned length of 2313 characters, of which 544 were parsimony-informative. MP analysis yielded 5000 equally parsimonious trees (TL = 2605, CI = 0.528, RI = 0.568, RC = 0.300, HI = 0.472). The Peniophora s.l. dataset contained 113 ITS and 97 28S sequences from 114 samples representing 63 taxa and the outgroup, and it had an aligned length of 1993 characters, of which 350 were parsimony-informative. MP analysis yielded 5000 equally parsimonious trees (TL = 1973, CI = 0.372, RI = 0.698, RC = 0.260, HI = 0.628). The jModelTest suggested GTR+I+G as the best-fit model of nucleotide evolution for both Peniophoraceae and Peniophora s.l. datasets. The average standard deviation of split frequencies of BI was 0.004389 (for the Peniophoraceae dataset) and 0.004179 (for the Peniophora s.l. dataset) at the end of the run. ML and BI analyses resulted in almost identical tree topologies compared to the MP analysis. The MP trees of Penophoraceae and Peniophora s.l. are shown in Figure 1 and Figure 2, respectively, with the parsimony bootstrap values (≥50%, front), likelihood bootstrap values (≥50%, middle) and Bayesian posterior probabilities (≥0.95, back) labeled along the branches.

Figure 1.

Phylogenetic tree obtained from maximum parsimony analysis of ITS-28S sequence data of Peniophoraceae. Branches are labeled with parsimony bootstrap values (≥50%, front), likelihood bootstrap values (≥50%, middle) and Bayesian posterior probabilities (≥0.95, back). New species and new combinations are set in bold.

Figure 2.

Phylogenetic tree obtained from maximum parsimony analysis of ITS-28S sequence data of Peniophora s.l. Branches are labeled with parsimony bootstrap values (≥50%, front), likelihood bootstrap values (≥50%, middle) and Bayesian posterior probabilities (≥0.95, back). New species (purple) and new combinations (blue) are set in bold.

Table 1.

Species and sequences used in the phylogenetic analyses. New species are set in bold with type specimens indicated with an asterisk (*).

Taxa	Voucher	Locality	ITS	28S	Reference
Amylostereum chailletii	NH8031/1035	Romania	AF506406	AF506406	[6]
Asterostroma laxum	EL33-99	Estonia	AF506410	AF506410	[6]
A. muscicola	KHL9537	Puerto Rico	AF506409	AF506409	[6]
Baltazaria eurasiaticogalactina	CBS666.84	France	—	AY293211	[27]
B. octopodites	FLOR 56449	Brazil	MH260025	MH260047	[28]
Confertobasidium olivaceoalbum	FP90196	USA	AF511648	AF511648	[6]
Dichostereum effuscatum	GG930915	France	AF506390	AF506390	[6]
D. pallescens	NH7046/673	Canada	AF506392	AF506392	[6]
Gloiothele lactescens	EL8-98	Sweden	AF506453	AF506453	[6]
G. lamellosa	KHL11031	Venezuela	AF506454	AF506454	[6]
Lachnocladium schweinfurthianum	KM 49740	Cameroon	MH260033	MH260051	[28]
L. sp.	KHL10556	Jamaica	AF506461	AF506461	[6]
Metulodontia nivea	NH13108/2712	Russia	AF506423	AF506423	[6]
Peniophora albobadia	CBS329.66	France	MH858809	MH870448	[9]
P. albobadia	He2159	USA	MK588755	MK588795	Present study
P. aurantiaca	UBCF:19732	—	HQ604854	HQ604854	—
P. aurantiaca	CBS396.50	France	MH856678	MH868195	[9]
P. bicornis	He3609	China	MK588763	MK588803	Present study
P. bicornis	He4767	China	MK588764	MK588804	Present study
P. borbonica	He4606	China	MK588765	MK588805	Present study
P. borbonica	He4597	China	MK588766	MK588806	Present study
P. cinerea	NH9808/1788	Spain	AF506424	AF506424	[6]
P. cinerea	CBS261.37	Belgium	MH855905	MH867412	[9]
P. cinerea	He3725	China	MK588769	MK588809	Present study
P. crassitunicata	CBS663.91	Reunion	MH862292	MH873972	[9]
P. crassitunicata	He3814	China	MK588770	MK588810	Present study
P. cremicolor	He5380 *	China	MK588791	MK588831	Present study
P. duplex	TPDuB1022	—	AF119519	—	[29]
P. duplex	CBS286.58	Canada	MH857787	MH869321	[9]
P. erikssonii	CBS287.58	France	MH857788	MH869322	[9]
P. erikssonii	Cui11871	China	MK588771	MK588811	Present study
P. exima	T-523	USA	MK588772	MK588812	Present study
P. fasticata	CBS942.96	Ethiopia	MH862624	—	[9]
P. fissilis	CBS681.91	Reunion	MH862298	MH873975	[9]
P. fissilis	CBS684.91	Mascarene Islands	MH862299	MH873976	[9]
P. gilbertsonii	CBS357.95	USA	MH862528	MH874164	[9]
P. gilbertsonii	CBS360.95	USA	MH862530	MH874165	[9]
P. guadelupensis	CBS715.91	Guadeloupe	MH862304	MH873977	[9]
P. halimi	CBS863.84	France	MH861844	MH873532	[9]
P. halimi	CBS864.84	France	MH861845	MH873533	[9]
P. incarnata	NH10271/1909	Danmark	AF506425	AF506425	[6]
P. incarnata	CBS399.50	France	MH856681	MH868198	[9]
P. junipericola	CBS349.54	Sweden	MH857354	—	[9]
P. junipericola	He2462	China	MK588773	MK588813	Present study
P. kuehneri	CBS719.91	Mascarene Islands	MH862307	MH873980	[9]
P. kuehneri	He4745	China	MK588757	MK588797	Present study
P. kuehneroides	CBS731.91	Mascarene Islands	MH862317	MH873989	[9]
P. kuehneroides	CBS732.91	Mascarene Islands	MH862318	MH873990	[9]
P. laete	CBS256.56	France	MH857617	MH869165	[9]
P. laete	FCUG 2681	Russia	GU322869	—	[30]
P. lassa	SP6129	Russia	KJ509191	—	[31]
P. lassa	He3052	China	MK588758	MK588798	Present study
P. lassa	Dai17081A	China	MK588759	MK588799	Present study
P. laurentii	CBS325.73	Norway	—	MH872397	[9]
P. laxitexta	BAFC 3309	Argentina	FJ882040	—	[32]
P. laxitexta	LGMF1159	Brazil	JX559580	—	[33]
P. lilacea	CBS337.66	Armenia	MH858813	MH870452	[9]
P. limitata	olrim963	Lithuania	AY787678	—	[34]
P. lycii	CBS264.56	France	MH857624	MH869169	[9]
P. lycii	Boid-437	France	MK588774	MK588814	Present study
P. major	He5528 *	China	MK588792	MK588832	Present study
P. malaiensis	CBS679.91	Singapore	MH862297	MH873974	[9]
P. manshurica	He2956	China	MK588776	MK588816	Present study
P. manshurica	He3729	China	MK588777	MK588817	Present study
P. meridionalis	CBS289.58	France	MH857789	MH869323	[9]
P. molesta	CBS677.91	Gabon	MH862295	—	[9]
P. molesta	CBS676.91	Gabon	MH862294	MH873973	[9]
P. monticola	CBS649.91	Reunion	MH862289	MH873970	[9]
P. nuda	He5280	China	MK588778	MK588818	Present study
P. nuda	HHB-4916-Sp	USA	MK588779	MK588819	Present study
P. ovalispora	CBS653.91	Mascarene Islands	MH862290	MH873971	[9]
P. parvocystidiata	CBS716.91	Guadeloupe	MH862305	MH873978	[9]
P. piceae	olrim10	Sweden	AY781264	—	[35]
P. piceae	209	Russia	JX507718	—	[36]
P. pilatiana	CBS265.56	France	MH857625	MH869170	[9]
P. pilatiana	CBS-A1/A2	—	MK588780	MK588820	Present study
P. pini	Hjm 18143	Sweden	EU118651	EU118651	[7]
P. pini	CBS274.56	France	MH857632	MH869177	[9]
P. pithya	CBS277.56	France	MH857635	MH869180	[9]
P. pithya	He3107	China	MK588781	MK588821	Present study
P. polygonia	CBS404.50	France	MH856684	MH868201	[9]
P. polygonia	He4651	China	MK588782	MK588822	Present study
P. proxima	CBS405.50	France	MH856685	MH868202	[9]
P. proxima	He5498	China	MK588783	MK588823	Present study
P. pseudopini	TPPpB1007	—	AF119514	—	[29]
P. pseudopini	DAOM-30124-Sp	Canada	MK588784	MK588824	Present study
P. pseudoversicolor	CBS338.66	France	MH858814	MH870453	[9]
P. pseudoversicolor	He5132	China	MK588785	MK588825	Present study
P. quercina	CBS407.50	France	MH856687	MH868204	[9]
P. quercina	CBS408.50	France	MH856688	MH868205	[9]
P. reidii	CBS397.83	France	MH861616	MH873334	[9]
P. rhoica	CBS943.96	Ethiopia	MH862625	MH874246	[9]
P. roseoalba	CLZhao3513	China	ON786559	OP380690	[16]
P. roseoalba	CLZhao9401	China	ON786560	—	[16]
P. roseoalba	He5031	China	OP872571	OP872575	Present study
P. rufa	CBS351.59	Canada	MH857891	MH869432	[9]
P. rufa	He2788	China	MK588786	MK588826	Present study
P. rufomarginata	CBS281.56	France	MH857639	MH869183	[9]
P. rufomarginata	CBS282.56	France	MH857640	MH869184	[9]
P. septentrionalis	CBS294.58	Canada	MH857791	MH869325	[9]
P. shenghuae	He3507 *	China	MK588788	MK588828	Present study
P. shenghuae	He3535	China	MK588789	MK588829	Present study
P. shenghuae	He5447	China	MK588790	MK588830	Present study
P. simulans	CBS874.84	France	MH861849	MH873537	[9]
P. simulans	CBS875.84	France	MH861850	MH873538	[9]
P. sphaerocystidiata	HHB-8827-Sp	USA	MK588787	MK588827	Present study
P. subsalmonea	CBS696.91	Mascarene Islands	MH862302	—	[9]
P. subsalmonea	CBS697.91	Mascarene Islands	MH862303	—	[9]
P. taiwanensis	He4870	China	MK588775	MK588815	Present study
P. taiwanensis	Wu 9206-28	China	MK588793	MK588833	Present study
P. taiwanensis	Wu 9209-14	China	MK588794	MK588834	Present study
P. tamaricicola	CBS438.62	Morocco	MH858203	MH869802	[9]
P. tamaricicola	CBS439.62	Morocco	MH858204	MH869803	[9]
P. trigonosperma	CBS402.83	France	MH861618	MH873335	[9]
P. trigonosperma	He3602	China	MK588762	MK588802	Present study
P. tristicula	CBS210.63	Pakistan	MH858266	—	[9]
P. tristicula	He4775	China	MH669235	MH669239	[37]
P. versicolor	CBS358.61	Morocco	MH858082	MH869651	[9]
P. versiformis	CBS358.54	France	MH857360	MH868902	[9]
P. versiformis	He3029	China	MK588756	MK588796	Present study
P. vietnamensis	He5242	Vietnam	MK588760	MK588800	Present study
P. vietnamensis	He5252 *	Vietnam	MK588761	MK588801	Present study
P. violaceolivida	CBS348.52	France	MH857077	MH868613	[9]
P. yunnanensi	CLZhao3978	China	OP380617	OP380689	[16]
P. yunnanensi	CLZhao7347	China	OP380616	—	[16]
Scytinostroma jacksonii	NH6626/635	Canada	AF506467	AF506467	[6]
S. portentosum	EL11-99	Sweden	AF506470	AF506470	[6]
S. renisporum	CBS770.86	Indonesia	MH862050	MH873737	[9]
Vararia investiens	TAA164122	Norway	AF506484	AF506484	[6]
V. ochroleuca	JS24400	Norway	AF506485	AF506485	[6]
Vesiculomyces citrinus	EL53-97	Sweden	AF506486	AF506486	[6]

In the trees, species of Peniophora s.l. including the type species of Peniophora s.s., Dendrophora and Duportella formed a strongly supported clade (95/95/1 in Figure 1, 100/100/1 in Figure 2). Four distinct lineages corresponding to Peniophora cremicolor, P. major, P. shenghuae and P. vietnamensis spp. nov. were recovered. For other sequences generated in this study, they formed distinct lineages alone or together with sequences from GenBank and represented known species.

3.2. Taxonomy

Peniophora Cooke, Grevillea 8 (no. 45): 20, 1879, emended

Basidiomes annual or perennial, resupinate, effused or effused-reflexed, adnate or sometimes loosening with age, membranaceous, ceraceous or coriaceous, usually stratified in section. Reflexed parts narrow, velutinous, felty to tomentose. Hymenophore smooth or tuberculate, rarely raduloid or merulioid, reddish, orange, pink, violaceous, gray, cream-colored, ochraceous, brown to dark brown; margin indistinct to fibrillose, adnate or slightly elevated, usually curved inside in reflexed parts when dry and old, concolorous or darker than hymenophore surface. Hyphal system monomitic or dimitic. Skeletal hyphae thick-walled, yellowish brown, dominated in the subiculum. Generative hyphae colorless to yellowish brown, thin- to thick-walled, with or without clamps. Dendrohyphidia present in some species, colorless or brown, thin- or thick-walled. Lamprocystidia present in most species, subulate or subcylindrical, colorless to brown, mostly thick-walled, encrusted with crystals. Gloeocystidia present or not, fusiform, subclavate to subcylindrical, colorless, thin- to thick-walled, empty or with contents. Basidia clavate to subcylindrical, sometimes flexuous, thin- to slightly thick-walled, with (2–) 4 sterigmata. Basidiospores colorless, usually cylindrical, allantoid or ellipsoid, rarely ovoid, subglobose, lacrimoid, pyriform or triangular, thin-walled, smooth, inamyloid, acyanophilous, spore print mostly pink.

Notes—According to the phylogenetic analyses, the morphological characters used to delimit the three genera, Peniophora s.s., Dendrophora and Duportella, are not reliable. Thus, we propose to use a broad concept for Peniophora, which includes taxa possessing resupinate to effused-reflexed basidiomes with a bright or dull hymenophore surface, a monomitic or dimitic hyphal system with simple-septate or clamped generative hyphae, colorless or brown lamprocystidia and differently shaped basidiospores. However, we believe that the simultaneous presences of lamprocystidia and gloeocystidia, and the inamyloid basidiospores can be regarded as the synapomorphic traits for Peniophora in Russulales.

Peniophora cremicolor Y.L. Xu, Y. Tian & S.H. He, sp. nov. Figure 3

Figure 3.

Peniophora cremicolor ((a) from paratype BJFC 026446; (b–f) from the holotype BJFC 026441). Scale bars: (a) = 1 cm; (b–f) = 10 µm. (a). Basidiomes; (b). Basidiospores; (c). Basidia and a basidiole; (d). Gloeocystidia; (e). Lamprocystidia; (f). Hyphae from subiculum.

MycoBank: MB846853

Type—CHINA, Fujian Province, Wuyishan County, Wuyishan Nature Reserve, on dead but still attached branch of angiosperm tree, 6 April 2018, He 5380 (BJFC 026441, holotype).

Etymology—refers to the species having the cream color of the dried basidiomes.

Fruiting body—Basidiomes annual, resupinate, effused, adnate or slightly detached from substrate with age, membranaceous to coriaceous, first as small colonies, later confluent up to 20 cm long, 2 cm wide, 200 µm thick in section. Hymenophore smooth, orange yellow [4B(7–8)] when fresh, cream [4A3] to grayish yellow [4B3] after dry, not cracked, unchanged in KOH; margin thinning out, fimbriate and white when juvenile, becoming indistinct and concolorous with hymenophore surface when mature.

Microscopic structures—Hyphal system monomitic; generative hyphae simple-septate. Subiculum well-developed, colorless, with a compact texture; hyphae colorless, thin- to slightly thick-walled, smooth, rarely branched, moderately septate, agglutinated, more or less parallel to substrate, 2–4 µm in diam. Subhymenium thickening with age, composed of lamprocystidia, hyphae and collapsed hymenial elements; hyphae colorless, thin- to slightly thick-walled, smooth, agglutinated, interwoven, 2–3.5 µm in diam. Lamprocystidia numerous, metuloid, subulate, colorless, thick-walled, heavily encrusted with crystals in the middle and upper parts, embedded, with a basal simple septum, 32–70 × 6–12 μm (with encrustations). Gloeocystidia subcylindrical to subclavate, usually with one or two contractions, empty or sometimes with contents, colorless, slightly thick-walled in most parts, slightly thickening toward the base, with a basal simple septum, smooth, 50–80 × 7–12 μm. Basidia clavate, colorless, slightly thick-walled, with a basal simple septum and four sterigmata, usually projecting beyond the hymenium, 45–65 × 8–12 μm; basidioles numerous, in shape similar to basidia but slightly smaller. Basidiospores ellipsoid to broadly ellipsoid, colorless, thin-walled, smooth, bearing a distinct apiculus, inamyloid, acyanophilous, 9–13 × 6–7 µm, L = 11.3 µm, W = 6.3 µm, Q = 1.8 (n = 60/2).

Additional specimen examined—CHINA, Fujian Province, Wuyishan County, Wuyishan Nature Reserve, on dead but still attached branch of angiosperm tree, 6 April 2018, He 5385 (BJFC 026446).

Notes—Peniophora cremicolor is characterized by the cream-colored basidiomes, simple-septate generative hyphae, numerous lamprocystidia and gloeocystidia, large ellipsoid to broadly ellipsoid basidiospores. In the phylogenetic tree (Figure 2), P. cremicolor formed a distinct lineage sister to P. fasticata Boidin & Lanq., P. subsalmonea Boidin, Lanq. & Gilles and P. rhoica, all of which have cylindrical to allantoid basidiospores [5]. Morphologically, P. erikssonii Boidin is similar to P. cremicolor by having orange yellow basidiomes, simple-septate generative hyphae and ellipsoid basidiospores, but differs in having larger lamprocystidia (50–110 × 8–15 µm), gloeocystidia (70–140 × 10–15 µm) and basidiospores (13–20 × 8–13 µm) [5]. Peniophora proxima Bres. is similar to P. cremicolor by sharing same size of basidiospores but differs in having clamped generative hyphae and smaller lamprocystidia (15–40 × 5–7 µm) [38].

Peniophora major Y.L. Xu, Y. Tian & S.H. He, sp. nov. Figure 4

Figure 4.

Peniophora major (from the holotype BJFC 026589). Scale bars: (a) = 1 cm; (b–e) = 10 µm. (a). Basidiomes; (b). Basidiospores; (c). Basidia and a basidiole; (d). Gloeocystidia; (e). Lamprocystidia.

MycoBank: MB846854

Type—CHINA, Guizhou Province, Jiangkou County, Fanjingshan Nature Reserve, on dead angiosperm branch, 11 July 2018, He 5528 (BJFC 026589, holotype).

Etymology—refers to the species having large lamprocystidia, gloeocystidia and basidiospores.

Fruiting body—Basidiomes annual, resupinate, effused, closely adnate, inseparable from substrate, coriaceous, up to 35 cm long, 3 cm wide, 350 µm thick in section. Hymenophore smooth, pale orange [6A3], orange grey [6B2] to grayish orange [6B(3–4)], not cracked, unchanged in KOH; margin thinning out, indistinct, concolorous with hymenophore surface.

Microscopic structures—Hyphal system monomitic; generative hyphae simple-septate. Subiculum thin, yellowish brown, with a compact texture; hyphae colorless to pale yellow, thick-walled, smooth, moderately septate, rarely branched, densely agglutinated, more or less parallel to substrate, 3–5 µm in diam. Subhymenium thickening, composed of lamprocystidia, hyphae and collapsed hymenial elements; hyphae colorless, thin- to slightly thick-walled, smooth, agglutinated, interwoven, 2–4 µm in diam. Lamprocystidia numerous, metuloid, subulate, colorless or pale yellow at base with age, thick-walled, heavily encrusted with crystals in the middle and upper parts, embedded or projecting beyond the hymenium, with a basal simple septum, 40–105 × 11–16 μm (with encrustations). Gloeocystidia subclavate to subcylindrical, colorless, slightly thick-walled, smooth, often with contents, with a basal simple septum, 40–85 × 7–10 μm. Basidia subclavate, usually with a contraction in the upper part, colorless, slightly thick-walled, with a basal simple septum and four sterigmata, 35–50 × 8–9 μm; basidioles numerous, in shape similar to basidia but slightly smaller. Basidiospores cylindrical, usually slightly concaved in one side, bearing a distinct apiculus, colorless, thin-walled, smooth, inamyloid, acyanophilous, 10–14 × 4.8–6 µm, L = 12.2 µm, W = 5.1 µm, Q = 2.4 (n = 30/1).

Notes—Peniophora major is characterized by the grayish basidiomes, simple-septate generative hyphae, and large lamprocystidia, gloeocystidia and basidiospores. In the phylogenetic tree (Figure 2), P. major formed a sister lineage to P. limitata (Chaillet ex Fr.) Cooke, but their relationship was not well-supported. Morphologically, P. limitata differs from P. major by clamped generative hyphae, the absence of gloeocystidia, and smaller lamprocystidia (25–60 × 8–12 µm) and basidiospores (7.5–12 × 2.5–3.5 µm) [5]. Peniophora coprosmae G. Cunn. from Australia and New Zealand is similar to P. major by sharing distinct gloeocystidia and large cylindrical basidiospores, but it differs in having clamped generative hyphae, slightly shorter lamprocystidia (35–80 µm long) and slightly smaller basidiospores (9–11.5 × 4–5 µm) [5].

Peniophora shenghuae Y.L. Xu, Y. Tian & S.H. He, sp. nov. Figure 5

Figure 5.

Peniophora shenghuae (from the holotype BJFC 021904). Scale bars: (a) = 1 cm; (b–f) = 10 µm. (a). Basidiomes; (b). Basidiospores; (c). Basidia and a basidiole; (d). Gloeocystidia; (e). Lamprocystidia; (f). Hyphae from subiculum.

MycoBank: MB846855

Type—CHINA, Yunnan Province, Luquan County, Zhuanlong Town, on dead angiosperm branch, 4 December 2015, He 3507 (BJFC 021904, holotype).

Etymology—Named to honor Dr. Sheng-Hua Wu (National Museum of Natural Science, Taiwan) who contributed to the taxonomy of Peniophora s.l. and other corticioid fungi in Taiwan.

Fruiting body—Basidiomes annual, resupinate, effused, closely adnate, coriaceous, first as small colonies, later confluent up to 9 cm long, 3 cm wide, 200 µm thick in section. Hymenophore smooth, pale orange [5A3], orange gray [5B2] to brownish orange [5C (3–6)], not cracked or with scattered crevices when dry, slightly darkening in KOH; margin thinning out, indistinct, usually darker than hymenophore surface, brown.

Microscopic structures—Hyphal system monomitic; generative hyphae simple-septate. Subiculum yellowish brown, with a compact texture, up to 60 µm thick; hyphae colorless to pale yellow, thin- to slightly thick-walled, smooth, rarely branched, moderately septate, interwoven, densely agglutinated, 2–4 µm in diam. Subhymenium thickening, composed of lamprocystidia, hyphae and collapsed hymenial elements; hyphae colorless, thin- to slightly thick-walled, smooth, tightly interwoven, 2–3 µm in diam. Lamprocystidia abundant, subulate, colorless, thick-walled, heavily encrusted with crystals in most parts, mostly embedded or slightly projecting beyond the hymenium, with a basal simple septum, 20–60 × 8–16 μm (with encrustations). Gloeocystidia fusiform, usually with a small apical papilla, flexuous, colorless, slightly thick-walled, smooth, empty or with content, 28–50 × 5–8 μm. Basidia subclavate to subcylindrical, usually with several contractions, flexuous, colorless, thin-walled, smooth, with a basal simple septum and four sterigmata, 24–45 × 5–7 μm; basidioles numerous, in shape similar to basidia but slightly smaller. Basidiospores cylindrical, bearing a distinct apiculus, colorless, thin-walled, smooth, inamyloid, acyanophilous, 7.5–10 (–10.5) × 3–4 µm, L = 9.1 µm, W = 3.3 µm, Q = 2.8 (n = 30/1).

Additional specimens examined—CHINA, Yunnan Province, Luquan County, Zhuanlong Town, on dead angiosperm branch, 4 December 2015, He 3506 (BJFC 021903) & He 3535 (BJFC 021933); Guizhou Province, Chishui County, Suoluo Nature Reserve, on dead liana, 7 July 2018, He 5447 (BJFC 026508).

Notes—Peniophora shenghuae is characterized by the grayish orange basidiomes, simple-septate generative hyphae, numerous strongly encrusted lamprocystidia, papillated gloeocystidia and cylindrical basidiospores. In the phylogenetic tree (Figure 2), P. shenghuae formed a strongly supported lineage with P. reidii Boidin & Lanq. Meanwhile, morphologically, P. reidii is similar to P. shenghuae by sharing simple-septate generative hyphae, papillated gloeocystidia and same size, cylindrical basidiospores. However, P. reidii has thicker basidiomes (up to 0.6 mm) and wider, sometimes bifurcate lamprocystidia (12–20 μm wide) [5]. The occurrence of P. reidii in Taiwan needs to be confirmed [11]. Peniophora borbonica Boidin & Gilles is similar to P. shenghuae by sharing simple-septate generative hyphae, fusiform gloeocystidia and cylindrical basidiospores, but it differs in having thicker basidiomes (up to 1.2 mm thick), slightly thick-walled basidia and slightly slender basidiospores (2.7–3.5 μm wide) [5]. Two specimens collected from Taiwan were identified as P. borbonica by us, which formed a distinct lineage distantly related to the lineage of P. shenghuae and P. reidii (Figure 2).

Peniophora vietnamensis Y.L. Xu, Y. Tian & S.H. He, sp. nov. Figure 6

Figure 6.

Peniophora vietnamensis ((a,c–g) from the holotype BJFC 024770; (b) from the paratype BJFC 024760). Scale bars: (b,c) = 1 cm; (d–g) = 10 µm. (a–c). Basidiomes; (d). Basidiospores; (e). Basidia and basidioles; (f). Gloeocystidia; (g). Lamprocystidia.

MycoBank: MB846856

Type—VIETNAM, Lam Dong Province, Bi Doup Nui Ba National Park, on dead Araceae plant, 15 October 2017, He 5252 (BJFC 024770, holotype).

Etymology—refers to the species being found in Vietnam.

Fruiting body—Basidiomes annual, resupinate, effused, closely adnate, first as small colonies, later confluent up to 9 cm long, 1 cm wide, 260 µm thick in section. Hymenophore smooth, brownish orange [6C(5–7)] to light brown [6D(6–8)], not cracked or finely cracked with age, turning reddish brown in KOH; margin thinning out, indistinct, concolorous or darker than hymenophore surface.

Microscopic structures—Hyphal system monomitic; generative hyphae simple-septate. Subiculum indistinct or absent; hyphae colorless, thin- to slightly thick-walled, smooth, rarely branched, moderately septate, interwoven, 2–3 µm in diam. Subhymenium thickening, with numerous lamprocystidia; hyphae colorless, thin- to slightly thick-walled, smooth, interwoven, 1.5–2.5 µm in diam. Lamprocystidia numerous, subulate, usually bifurcate, with one or two secondary septa, yellowish brown, distinctly thick-walled, slightly encrusted with fine crystals in the apex, embedded or slightly projecting beyond the hymenium, 25–40 × 5–10 μm. Gloeocystidia subulate, colorless, thin-walled, smooth, usually with one secondary septum, usually empty in the apical part, with contents in the basal part, 28–50 × 5–8 μm. Basidia subclavate, with a contraction in the middle part, colorless, thin-walled, with a basal simple septum and four sterigmata, 23–32 × 6–10 μm; basidioles numerous, in shape similar to basidia but slightly smaller. Basidiospores oblong cylindrical, colorless, thin- to slightly thick-walled, smooth, inamyloid, cyanophilous when thick-walled, 12–16.5 (–17) × 4–6 µm, L = 14.5 µm, W = 4.5 µm, Q = 3.2–3.3 (n = 60/2).

Additional specimen examined—VIETNAM, Lam Dong Province, Bi Doup Nui Ba National Park, on dead Araceae plant, 15 October 2017, He 5242 (BJFC 024760).

Notes—Peniophora vietnamensis is characterized by its brownish orange basidiomes on Araceae plant, simple-septate generative hyphae, brown lamprocystidia, subulate gloeocystidia and oblong cylindrical basidiospores. In the phylogenetic trees (Figure 1 and Figure 2), P. vietnamensis and P. trigonosperma Boidin, Lanq. & Gilles formed a strongly supported lineage. Both species grow on palm trees and have similar brown lamprocystidia, however, P. trigonosperma differs in having clamped hyphae, cylindrical to fusiform gloeocystidia and triangular basidiospores [5]. Duportella rhoica Boidin & Lanq. is similar to P. vietnamensis by sharing oblong cylindrical basidiospores (10–14.5 × 4–6 µm) but differs in having a dimitic hyphal system with skeletoid hyphae and clamped generative hyphae and larger fusiform gloeocystidia (60–90 × 5–12 µm) [5].

Peniophora globispora Y.L. Xu & S.H. He, nom. & comb. nov.

MycoBank: MB846863

Duportella sphaerospora G. Cunn., Transactions and Proceedings of the Royal Society of New Zealand 85: 96 (1957).

Notes—Duportella sphaerospora is characterized by the large globose to subglobose basidiospores (10–12 × 9–12 µm) [5]. Since the epithet ‘sphaerospora’ was used in Peniophora for another species (P. sphaerospora Höhn. & Litsch. = Hypochnicium sphaerosporum (Höhn. & Litsch.) J. Erikss.), we propose the new name and new combination, Peniophora globispora, for this species.

Peniophora jordaoensis (Hjortstam & Ryvarden) Y.L. Xu & S.H. He, comb. nov.

MycoBank: MB846857

Duportella jordaoensis Hjortstam & Ryvarden, Synopsis Fungorum 18: 20 (2004).

Notes—The species was originally described from Sao Paulo, Brazil, and it is known only from the type locality so far. Although sequences of the species are unavailable at present, morphologically, it has typical characteristics of Peniophora, such as the presence of both gloeocystidia and lamprocystidia, and suballantoid to allantoid basidiospores [39]. Meanwhile, the felted subiculum and brownish metuloid cystidia of the species can be seen in other species of Peniophora.

Peniophora kuehneroides (Boidin, Lanq. & Gilles) Y.L. Xu & S.H. He, comb. nov.

MycoBank: MB846858

Duportella kuehneroides Boidin, Lanq. & Gilles, Bulletin de la Société Mycologique de France 107 (3): 98 (1991).

Notes—Two strains (CBS 731.91 and CBS 732.91) of Duportella kuehneroides from Mascarene Islands isolated and identified by Paule Lanquetin formed a distinct lineage in the large clade of Peniophora (Figure 1 and Figure 2). We propose the new combination based on both morphological and molecular evidence [5].

Peniophoralassa (Spirin & Kout) Y.L. Xu & S.H. He, comb. nov.

MycoBank: MB846859

Duportella lassa Spirin & Kout, Mycotaxon 130 (2): 484 (2015).

Notes—The species was recently described from northeast Russia [31]. A specimen from northeast China (He 3052) and the holotype of the species (Spirin 6129) formed a strongly supported lineage sister to other species of Peniophora. The close relationship between Duportella lassa and Peniophora was also noticed by Spirin and Kout [31]. Peniophora lassa is a common species in the Beijing area according to the authors’ investigations carried out recently.

Specimens examined—CHINA, Inner Mongolia Autonomous Region, Genhe County, Greater Khingan Mountains Nature Reserve, on trunk of Salix, 17 October 2015, He 3052 (BJFC 021442); Beijing, Mentougou District, Tanzhe Temple Park, on dead branch of Syringa, 17 July 2020, He 6511 (BJFC 033459); Jietai Temple Park, on dead branch of Lonicera, 7 August 2020, He 6735 (BJFC 033683); Pinggu District, Jinhai Lake Park, on trunk of Cotinus, 11 August 2020, He 6766 (BJFC 033714); Yanqing District, Songshan Nature Reserve, on dead branch of Syringa, 3 September 2020, He 6943 (BJFC 033892).

Peniophora miranda (Boidin, Lanq. & Gilles) Y.L. Xu & S.H. He, comb. nov.

MycoBank: MB846860

Duportella miranda Boidin, Lanq. & Gilles, Bulletin de la Société Mycologique de France 107 (3): 100 (1991).

Notes—The species is characterized by the numerous brown lamprocystidia and subovoid basidiospores [3]. Boidin et al. (1998) showed that P. miranda was closely related to other Peniophora species, although the sequence is unavailable for us.

Peniophora pirispora (Boidin, Lanq. & Gilles) Y.L. Xu & S.H. He, comb. nov.

MycoBank: MB846861

Duportella pirispora Boidin, Lanq. & Gilles, Bulletin de la Société Mycologique de France 107 (3): 104 (1991).

Notes—The species is characterized by the brown lamprocystidia and lacrimoid to pyriform or subreniform basidiospores. Although the sequences of the species are unavailable, present molecular evidence indicated that Peniophora includes species with differently shaped basidiospores (Figure 1 and Figure 2).

Peniophora rhoica (Boidin & Lanq.) Y.L. Xu & S.H. He, comb. nov.

MycoBank: MB846862

Duportella rhoica Boidin & Lanq., Cryptogamie Mycologie 16 (2): 89 (1995).

Notes—In our phylogenetic trees (Figure 1 and Figure 2), one strain (CBS 943.96) isolated from the holotype of Duportella rhoica (LY 14759) was nested within the Peniophora clade. Thus, we propose the new combination based on molecular evidence and morphological descriptions and illustrations [40].

Peniophora tristiculoides (Sheng H. Wu & Z.C. Chen) Y.L. Xu & S.H. He, comb. nov.

MycoBank: MB846864

Duportella tristiculoides Sheng H. Wu & Z.C. Chen, Bulletin of the National Museum of Natural Science 4: 108 (1993).

Notes—Morphologically, Duportella tristiculoides is close to D. tristicula (Berk. & Broome) Reinking, which was the type species of Duportella and nested within the Peniophora clade (Figure 1 and Figure 2). Duportella tristiculoides has been only reported from the type locality in Taiwan and not been sequenced so far.

Peniophora malaiensis Boidin, Lanq. & Gilles, Bulletin de la Société Mycologique de France 107 (3): 137 (1991)

Peniophora taiwanensis Sheng H. Wu, Mycotaxon 85: 197 (2003)

Notes—Our phylogenetic analyses indicated that the holotype of P. malaiensis, LY 8292 from Singapore (CBS679.91), formed a strongly supported lineage with three specimens collected from Guangxi Autonomous Region and Taiwan, China, including the paratype of P. taiwanensis, Wu 9206-28 (Figure 2). The ITS sequence similarity between LY 8292 and Wu 9206-28 is 99.16% (5 base pair differences). Morphologically, the two species are very similar except that P. taiwanensis has narrower basidiospores (1.8–2.2 μm) than P. malaiensis (2–2.7 μm) [3,11]. However, our measurements of the basidiospore width of the specimen He 4870 match that of P. malaiensis (2–3 μm). Therefore, we believe that the difference in the basidiospore width is within the specific range and treat P. taiwanensis as a later synonym of P. malaiensis.

Specimen examined—CHINA, Guangxi Autonomous Region, Jinxiu County, Dayaoshan Nature Reserve, Shengtangshan, on fallen angiosperm trunk, 15 July 2015, He 4870 (BJFC 024389).

Duportella renispora Boidin, Lanq. & Gilles, Bulletin de la Société Mycologique de France 107 (3): 104 (1991).

Notes—The strain (CBS 733.91) isolated from the holotype of the D. renispora (LY 12699) was sequenced by Vu et al. [9]. The blast results of the ITS (MH862319) and 28S (MH873991) sequences showed that the species does not belong to Peniophora s.l. but is close to Amylostereum Boidin. Morphologically, the thinly encrusted brown cystidia and absence of subiculum of the species do match the characteristics of Amylostereum, which, however, has amyloid basidiospores. In order to confirm the identity of the species, the type specimen should be checked in the future.

A key to Peniophora species in China
1. Dendrohyphidia well-developed, brown	P. versiformis
1. Dendrohyphidia absent, or colorless when present	2
2. Lamprocystidia brown over the entire length	3
2. Lamprocystidia colorless or only brown at the basal part	6
3. Skeletocystidia present	4
3. Skeletocystidia absent	5
4. Basidiospores 10–12.5 × 3.7–4.2 µm	P. tristicula
4. Basidiospores 5.2–7.5 × 2–3.5 µm	P. kuehneri
5. Basidiospores triangular, on palms	P. trignosperma
5. Basidiospores cylindrical to narrowly ellipsoid or ovoid, on angiosperms	P. lassa
6. Dendrohyphidia present, often colorless and may be difficult to see	7
6. Dendrohyphidia absent	8
7. Lamprocystidia absent; basidiospores > 7.5 µm long	P. polygonia
7. Lamprocystidia present; basidiospores < 7.5 µm long	P. meridionalis
8. Basidiospores ellipsoid or ovoid	9
8. Basidiospores cylindrical or allantoid	12
9. Basidiospores ovoid	P. roseoalba
9. Basidiospores ellipsoid	10
10. Generative hyphae with clamps	P. proxima
10. Generative hyphae without clamps	11
11. Basidiospores 9–13 × 6–7 µm	P. cremicolor
11. Basidiospores 11–20 × 8–14 µm	P. erikssonii
12. Basidiomes red	13
12. Basidiomes grey, cream, pale orange, pinkish, yellowish or purplish	14
13. Basidiomes pulvinate, only found on Populus	P. rufa
13. Basidiomes effused, found on other hosts	P. pseudoversicolor
14. Generative hyphae without clamps	15
14. Generative hyphae with clamps	19
15. Basidia with two sterigmata	P. bicornis
15. Basidia with four sterigmata	16
16. Basidiospores > 10 µm long	P. major
16. Basidiospores < 10 µm long	17
17. Basidiospores < 7 µm long	P. malaiensis
17. Basidiospores > 7 µm long	18
18. Basidiomes up to 1.2 mm thick; basidia thick-walled	P. borbonica
18. Basidiomes up to 200 µm thick; basidia thin-walled	P. shenghuae
19. Gloeocystidia indistinct or absent	20
19. Gloeocystidia present	22
20. Basidiomes pinkish, effused-reflexed, usually on Quercus.	P. manshurica
20. Basidiomes greyish, resupinate, on gymnosperms or angiosperms	21
21. Lamprocystidia 40–80 × 6–14 µm; on Juniperus	P. junipericola
21. Lamprocystidia 15–25 × 5–10 µm; on gymnosperms or angiosperms	P. cinerea
22. Gloeocystidia distinctly thick-walled, with walls up to 2–3 µm thick	P. crassitunicata
22. Gloeocystidia thin- to slightly thick-walled, with walls < 1 µm thick	23
23. Lamprocystidia up to 20 µm wide; basidiospores up to 7 µm long	P. pithya
23. Lamprocystidia up to 12 µm wide; basidiospores up to 10 µm long	24
24. Gloeocystidia 30–80 × 8–20 µm; basidiospores 2.5–3.5 µm wide	P. nuda
24. Gloeocystidia 12.5–58 × 5.5–15.5 µm; basidiospores 3–5.5 µm wide	P. yunnanensis

4. Discussion

The modern molecular phylogenetics have significantly changed the taxonomic systems of wood-inhabiting fungi in recent years. On the one hand, many new lineages and taxa were found and described, and on another hand, some morphologically dissimilar taxa were proved to be closely related in phylogeny [41,42,43,44,45]. Our results indicated that in the Peniophora s.l. group, the morphological characters, such as the color of lamprocystidia and dendrohyphidia used for generic delimitation are not reliable. As already shown in other studies [46,47,48,49,50], the identities of some genera erected based merely on morphology or together with phylogenetic analyses of not well-sampled datasets need to be confirmed.

The Peniophoraceae is a well-supported large family in Russulales, most species of which have resupinate basidiomes and non-poroid hymenophores growing on twigs, branches or trunks of woody plants or bamboos [5,51]. The species diversity, taxonomy and phylogeny of Peniophoraceae in China have been investigated and studied [16,37,52,53,54,55], and this study is a part of this consecutive research. However, the two large genera in Peniophoraceae, Scytinostroma Donk and Vararia P. Karst., that are closely related and were shown to be polyphyletic [6,7,28], have not been sufficiently studied worldwide. We are going to carry out a complete morphological and phylogenetic analyses of the Peniophoraceae by adding a lot of Scytinostroma-Vararia samples from Asia accumulated by the authors in recent years.

Author Contributions

Conceptualization, S.-H.H.; methodology, Y.-L.X. and Y.T.; performing the experiment, Y.-L.X. and Y.T.; formal analysis, Y.-L.X. and Y.T.; validation, Y.-L.X., Y.T. and S.-H.H.; resources, S.-H.H.; writing—original draft preparation, Y.-L.X.; writing—review and editing, S.-H.H.; visualization, Y.-L.X. and Y.T.; supervision, S.-H.H.; project administration, S.-H.H.; funding acquisition, S.-H.H. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

Funding Statement

The research is supported by the National Natural Science Foundation of China (Project Nos. 31750001; 31670013).