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Additions to tribe Chromosereae (Basidiomycota, Hygrophoraceae) from China, including Sinohygrocybe gen. nov. and a first report of Gloioxanthomyces nitidus
expand article infoChao-Qun Wang, Ming Zhang, Tai-Hui Li, Xi-Shen Liang, Ya-Heng Shen
‡ Guangdong Institute of Microbiology, Guangzhou, China
Open Access

Abstract

Sinohygrocybe gen. nov., typified by S. tomentosipes sp. nov., is described upon morphological and molecular evidence. The new genus is characterised by its sinuate to subdecurrent or short deccurent, usually furcate and interveined and relatively distant lamellae, dry and whitish tomentose stipe, thin-walled ellipsoid to oviod, non-constricted basidiospores and particularly elongated basidia and a ratio of basidiospore to basidium length of >5 to 8; it is close to genera Chromosera and Gloioxanthomyces of the tribe Chromosereae, but morphologically differs from Chromosera in less umbilicate basidiomata, tomentose stipe and usually longer basidia and differs from Gloioxanthomyces in more robust basidioma and less glutinous pileus and/or stipe surface. Phylogenetic analyses, with ITS-LSU-RPB2 data, also indicate that Sinohygrocybe forms a very distinct and independent clade at the generic level. In addition, a Chinese new record G. nitidus is described here.

Keywords

East Asia, new record species, new taxa, phylogeny overview

Introduction

Hygrophoraceae Lotsy (Hymenomycetes, Basidiomycota) is a large family in Agaricales, including 26 genera and over 600 species (Lodge et al. 2014). In a six-gene phylogenetic tree of Agaricales, Hygrophoraceae, Pterulaceae Corner, Typhulaceae Jülich and some small groups formed a Hygrophoroid clade, which is one of the six largest clades in Agaricales (Matheny et al. 2006); and in a genome based mushroom tree of life, Hygrophoraceae and Clavariaceae Chevall. are representative families of the suborder Hygrophorineae Aime, Dentinger & Gaya, which is one of the seven suborders of the Agaricales (Dentinger et al. 2016). Traditionally, the family Hygrophoraceae referred to a group of agaricoid, waxy-gilled and white-spored mushrooms; and a majority of the members are classified in the type genus Hygrophorus Fr. and genus Hygrocybe (Fr.) P. Kumm. Morphological characters of the Hygrophoraceae taxa are relatively simple (usually without annulus or volva and a cystidiate) amongst the agaric fungi and their basidioma colours are often very susceptible to the environmental conditions and developmental stages, making their classification and identification difficult, so it is often challenging to make correct identification and taxonomy of them just according to morphological recognition (Young 2005). Modern molecular techniques have been revolutionising the taxonomy and phylogeny of Hygrophoraceae.

Lodge et al. (2014) had conducted the most comprehensive molecular phylogenetic study on the family until now, therefore their systematic viewpoint on Hygrophoraceae is adopted in this paper. According to their study, the family could be divided into four groups at subfamily level, i.e. subfamily Hygrophoroideae E. Larss., Lodge, Vizzini, Norvell & S.A. Redhead, Hygrocyboideae Padamsee & Lodge, Lichenomphalioideae Lücking & Redhead and Cuphophylloid grade. The subfamily Hygrocyboideae could be divided into three tribes, i.e. tribe Chromosereae, Humidicuteae and Hygrocybeae; and the tribe Chromosereae included two sister genera, Chromosera Redhead, Ammirati & Norvell and Gloioxanthomyces Lodge, Vizzini, Ercole & Boertm.

Chromosera, the type genus of the tribe Chromosereae, was erected to accommodate Omphalina cyanophylla (Fr.) Quél. which was originally described from Sweden and combined as C. cyanophylla (Fr.) Redhead, Ammirati & Norvell (Redhead et al. 1995, 2012). Now, another four species, formerly placed in Hygrocybe or Hygrophorus, are also classified into Chromosera, i.e. C. citrinopallida (A.H. Sm. & Hesler) Vizzini & Ercole originally described from USA, C. lilacina (P. Karst.) Vizzini & Ercole originally described from the northern Fennoscandia, C. viola (J. Geesink & Bas) Vizzini & Ercole originally described from Belgium and C. xanthochroa (P.D. Orton) Vizzini & Ercole originally described from Scotland (Lodge et al. 2014).

Gloioxanthomyces is a small genus with only two known species, the type species G. vitellinus (Fr.) Lodge, Vizzini, Ercole & Boertm. originally described from Europe and G. nitidus (Berk. & M.A. Curtis) Lodge, Vizzini, Ercole & Boertm. from North America (Crous et al. 2004, Lodge et al. 2014). Before the recognition of Gloioxanthomyces, those two species were usually placed in the genus Hygrocybe as H. vitellina (Fr.) P. Karst and H. nitida (Berk. & M.A. Curtis) Murrill, respectively. Morphologically, the main differences between the two species were in their basidiospore sizes: G. nitidus had ellipsoid to oblong basidiospores, measuring 7–10 × 5–6 μm with Q = 1.3–1.8; while G. vitellinus had subglobose basidiospores, measuring 6.5–8.5 × 5–7 μm with Q=1.1–1.6 (Boertmann 1990). Since their differences were limited, the two taxa seemed to be conspecific (Boertmann 2011). However, according to the phylogenetic analyses with ITS data by Boertmann (2012), the European collections clearly clustered together as the G. vitellinus species clade, while the North American materials independently formed another group as the G. nitidus species clade, thus they could actually be sharply defined as two separated sister species.

During the studies on the Chinese Hygrophoraceae in recent years, some collections morphologically corresponding to tribe Chromosereae were collected. Comprehensive observation and analyses revealed some interesting findings, which can contribute to the taxonomic knowledge of the tribe. In this paper, we aim to: 1) formally describe a new genus of tribe Chromosereae from East Asia based upon morphological and molecular analyses and present a Chinese new record of Gloioxanthomyces nitidus; 2) reconstruct the phylogeny of the family Hygrophoraceae using 3 gene regions, i.e. the internal transcribed spacer region (ITS), the large subunit nuclear ribosomal RNA region (nrLSU) and the nuclear RPB2 6F to 7.1R region (RPB2). Detailed studies were therefore conducted and the results are presented as follows.

Materials and methods

Morphological studies

Specimens were photographed and annotated in the field and then dried in an electric drier. Macroscopic descriptions were gained from the original field notes and photographs. Colour descriptions followed Kornerup and Wanscher (1978). Tissue sections were immersed in 5% potassium hydroxide (KOH) and/or 1% Congo Red solution for microscopical examinations, but in distilled water for colour descriptions of basidia, pileipellis and stipitipellis. From a mature specimen, over 40 basidiospores and 20 basidia were randomly selected and measured under a light microscope in KOH. The notation (a)b–c(d) was used to describe dimensions where the range b–c representing 90% or more of the measured values and a, d were the extreme values. The length/width ratio of spores was presented as Q and the mean ratio was presented as Qm. The studied specimens were deposited in the Fungal Herbarium of Guangdong Institute of Microbiology (GDGM), Guangzhou, China.

Molecular studies

Genomic DNA was extracted from the herbarium specimens using the Sangon Fungus Genomic DNA Extraction kit (Sangon Biotech Co., Ltd., Shanghai, China) according to the manufacturer’s instructions. The ITS, LSU and RPB2 gene regions were amplified by Polymerase Chain Reaction, using universal primers ITS1F/ITS5 and ITS4 (White et al. 1990; Gardes and Bruns 1993), LR0R and LR5 (http://biology.duke.edu/fungi/mycolab/primers.htm) and RPB2-6F and RPB2-7.1R (Matheny 2005), respectively. Amplified products were sequenced by Beijing Genomic Institute (BGI) using the same primers. The abi format sequences were assembled by SeqMan version 7.1.0 (DNAStar, Inc.) and then the assembled sequences were submitted to GenBank.

In this study, two datasets were constructed. The first one is an ITS-LSU-RPB2 matrix of the family Hygrophorceaeae for making a comprehensive phylogenetic tree and analysing the positions of the new taxa; most known species of Hygrophoraceae with available sequences from reliable sources were included in the dataset, each of them having at least an LSU sequence and Typhula phacorrhiza (Reichard) Fr. was selected as the outgroup referred from Yang et al. (2013) and Lodge et al. (2014). The second dataset is an ITS matrix of the tribe Chromosereae and Hygrocybe conica (Schaeff.) P. Kumm. and H. conica var. conicoides (P.D. Orton) Boertm. were chosen as outgroups. Each gene was independently aligned on the online MAFFT service (Katoh et al. 2017), then combined by the Geneious software (Biomatters Ltd.) for the first dataset. Maximum likelihood phylogenetic trees were generated by the RAxML software (Stamatakis 2014) on the CIPRES service (Miller et al. 2010) with 1000 bootstrap replications using the default options.

Results

Molecular phylogenetic results

The combined 3-gene dataset composed of 120 samples (Table 1), including 5 newly sequenced samples and 115 published ones. In the final matrix, the ITS, LSU and RPB2 regions comprised positions 1 to 1751, 1752 to 2873, 2874 to 3759, respectively. In the 3-gene Maximum Likelihood tree (Fig. 1), the four Chinese collections (GDGM43351 and GDGM43347 from Sichuan province, GDGM50075 and GDGM50149 from Hunan province) formed a strong monophyletic clade with 100% bootstrap support, which was near the Chromosera-Gloioxanthomyces clade composed of members of Chromosera and Gloioxanthomyces with 76% bootstrap support.

Figure 1. 

Phylogenetic overview of the family Hygrophoraceae inferred from ITS-LSU-RPB2 data using Maximum Likelihood (ML) method. Typhula phacorrhiza was selected as outgroup. Bootstrap values (≥50%) were presented around the branches. The newly generated sequences are shown in bold.

Sequences information of samples used for the ITS-LSU-RPB2 combined tree. Newly generated sequences were bold.

Species name Isolate/voucher ID ITS LSU RPB2
Acantholichen albomarginatus MDF543 KT429797 KT429809
Acantholichen campestris DIC595b KT429798 KT429810 KT429818
Acantholichen galapagoensis MDF057 KT429784 KT429799 KT429811
Acantholichen galapagoensis MDF058 KT429785 KT429800 KT429812
Acantholichen galapagoensis MDF089 KT429786 KT429801
Acantholichen galapagoensis MDF090 KT429787 KT429802 KT429813
Acantholichen galapagoensis MDF093 KT429790 KT429803 KT429814
Acantholichen galapagoensis MDF094 KT429791 KT429804 KT429815
Acantholichen galapagoensis MDF100 KT429792 KT429805 KT429816
Acantholichen pannarioides MDF352 KT429795 KT429807 KT429817
Acantholichen pannarioides Bungartz 5593 EU825953 EU825953
Acantholichen sorediatus DIC335 KT429794 KT429806
Acantholichen variabilis MDF679 KT429796 KT429808
Ampulloclitocybe clavipes DJL06TN40 KF381542 KF407938
Ampulloclitocybe clavipes AFTOL-ID 542 AY789080 AY639881 AY780937
Arrhenia auriscalpium Lutzoni Lamoure 910824-3 U66428 U66428
Arrhenia lobata Lutzoni Lamoure 910824-1 U66429 U66429
Cantharellula umbonata RDY-1366 (SFSU) KF381519 AF261443
Cantharocybe brunneovelutina DJL-BZ-1883 (holotype) KX452404 HM588721
Cantharocybe gruberi AFTOL-ID 1017 DQ200927 DQ234540 DQ385879
Cantharocybe gruberi AH24539 JN006422 JN006420
Cantharocybe virosa TENN 63483(holotype) KX452405 JX101471
Chromosera citrinopallida DUKE8895 U66435 U66435
Chromosera citrinopallida D. Boertmann 2006/2 KF291072 KF291073
Chrysomphalina chrysophylla AFTOL-ID 1523 DQ457656 DQ192180
Chrysomphalina chrysophylla S.A. Redhead 7700 U66430 U66430
Chrysomphalina grossula OSC 113667 EU652372 EU644703
Chrysomphalina grossula OSC 113683 EU652373 EU644704
Cora minor Luecking 15243 EU825968 EU825968
Cuphophyllus acutoides var. pallidus CFMR TN-257 KF291097
Cuphophyllus adonis MES-152 KF291036 KF291037
Cuphophyllus aff. pratensis PBM-752 DQ457650 KF442252
Cuphophyllus aurantius CFMR PR-6601 KF291100 KF291102
Cuphophyllus bicolor DJL-PR-2 KF291056
Cuphophyllus flavipes Hattori-JP-6 KF291045 KF291047
Cuphophyllus fornicatus D. Boertmann 2009/94 KF291124
Cuphophyllus pratensis DJL-Scot-8 KF291058
Cuphophyllus sp. AM01 HM026542
Dictyonema glabratum AFTOL-ID 1995 DQ917656 DQ917661
Dictyonema glabratum Luecking 15581 EU825958 EU825958
Dictyonema glabratum Luecking 16563 EU825956 EU825956
Dictyonema glabratum R06 EU825959 EU825959
Dictyonema glabratum R11 EU825960 EU825960
Dictyonema glabratum R18 EU825961 EU825961
Dictyonema glabratum R20 EU825963 EU825963
Gliophorus aff. psittacinus CFMR JP-4 KF291079 KF291080
Gliophorus graminicolor TJB-10048 KF381520 KF381545 KF407936
Gliophorus psittacinus D. Boertmann 2002/10 KF291075 KF291076 KF291078
Gloioxanthomyces nitidus GDGM41710 MG712283-4 MG712282 MG711911
Haasiella splendidissima Herbarium Roux n. 3666 JN944398 JN944399
Haasiella splendidissima Herbarium Roux n. 4044 JN944400 JN944401
Haasiella splendidissima JVG1071013-1 JN944395 JN944396
Haasiella venustissima A. Gminder 971488 KF291092 KF291093
Haasiella venustissima E.C. 08191 JN944393 JN944394
Humidicutis sp. 2 CFMR PR4047 KF291151 KF291149
Humidicutis sp. 2 DJL-2103 CFMR PR-6524 KF291150 KF291151
Humidicutis sp. 3 D.J. Lodge DJL-BZ-3 KF291110 KF291111
Hygroaster albellus AFTOL ID 1997 KF381521 EF551314 KF381510
Hygroaster nodulisporus AFTOL-ID 2020 EF561625 KF381511
Hygrocybe acutoconica f. japonica CFMR JP-2 KF291161 KF291162
Hygrocybe aff. citrinovirens DJL05TN10 KF291090 KF291091
Hygrocybe aff. conica PBM 918 AY854074 DQ071739 AY803747
Hygrocybe aff. prieta DJL-BZ-65 KF291168 KF291169
Hygrocybe caespitosa DMWV-03-737 KF291104 KF291105 KF291107
Hygrocybe cantharellus AFTOL-ID 1714 DQ490628 DQ457675
Hygrocybe ceracea D. Boertmann 2002/7 KF291108 KF291109
Hygrocybe cf. acutoconica DJL04NC2 KF291117 KF291118 KF291120
Hygrocybe chloochlora DJL-BZ-32 EU435147 EU435147
Hygrocybe chlorophana Boertmann 2002/9 EU435148 EU435148 KF381513
Hygrocybe coccinea AFTOL-ID 1715 DQ490629 DQ457676 DQ472723
Hygrocybe coccinea Boertmann02/8 EU435146 EU435146 KF291114
Hygrocybe constrictospora D. Boertmann 2007/38 KF291115 KF291116
Hygrocybe glutinipes var. rubra DJL05NC9 EU435149 EU435149
Hygrocybe helobia AK-124 KF291182 KF291183
Hygrocybe hypohaemacta DJL-BZ-105 EU435150 EU435150 KF291165
Hygrocybe konradii var. konradii Boertmann 2004/6 KF306329 KF306330
Hygrocybe lepida Boertmann 2002/2 KF306333 KF306334
Hygrocybe melleofusca DJL-PR-EV KF291154 KF291155
Hygrocybe miniata AK-110 KF291179 KF291180
Hygrocybe miniata f. longipes AFTOL-ID 1891 DQ490630 DQ457677 DQ472724
Hygrocybe noninquinans DJL-PR-1 KF291127 KF291129 KF291128
Hygrocybe occidentalis var. occidentalis Cancerel PR 02 EU435151 EU435151
Hygrocybe punicea DJL-SCOT-B2 KF291133 KF291134
Hygrocybe purpureofolia DJL04NC1 KF291192 KF291193
Hygrocybe reidii DJL-ENG-15-2006 KF291158 KF291159
Hygrocybe rosea DJL-PR-4 KF291197 KF291198
Hygrophorus agathosmus EL2-00 AY586660
Hygrophorus cossus SJ94064 AY548963 AY548963
Hygrophorus hyacinthinus SJ950830 HM143012
Hygrophorus olivaceoalbus SJ91060 AY586662
Hygrophorus russula JP-3 KF291216 KF291217 KF291219
Hygrophorus sordidus AFTOL-1338 DQ490632 AF042562
Lichenomphalia umbellifera J. Geml-2 U66445 U66445 KF381515
Neohygrocybe ingrata GWG H. ingrata 23-10-06 (ABS) KF291225 KF291226
Neohygrocybe ingrata TN-62 voucher DJL05TN62 KF381525 KF381558 KF381516
Neohygrocybe ingrata CFMR NY-43 KF291223 KF291224
Neohygrocybe ovina K(M) 187568 KF291228 KF291229
Neohygrocybe ovina GWG H. ovina Rhosisaf (ABS) KF291233 KF291234 KF291236
Neohygrocybe subovina WRWV04-752 (DEWV 5366) KF291142 KF291138
Neohygrocybe subovina CFMR NC-61 KF291136 KF291137
Neohygrocybe subovina DJL04TN16 (GRSM 77065) KF291140 KF291141
Omphalina epichysium Redhead3140 U66442 U66442
Omphalina grossula Gulden 417/75 U66444 U66444
Omphalina hudsoniana LUTZ-920728.4a U66446 U66446
Omphalina obscurata Lam L73-101 U66448 U66448
Omphalina philonotis LUTZ930804-5 U66449 U66449
Omphalina sphagnicola LUTZ930810 U66453 U66453
Omphalina velutina LUTZ-930812.1 U66454 U66454
Omphalina velutipes Lamoure L77 U66455 U66455
Omphalina wynniae A. H. Smith 82899 U66457 U66457
Porpolomopsis aff. calyptriformis DJL05TN80 KF291246 KF291247 KF291249
Porpolomopsis calyptriformis EB-ENG-3 KF291242 KF291243 KF291245
Porpolomopsis lewelliniae TJB-10034 KF291238 KF291239 KF291241
Pseudoarmillariella bacillaris HKAS76377 KC222315 KC222316
Pseudoarmillariella ectypoides AFTOL-ID 1557 DQ192175 DQ154111 DQ474127
Sinohygrocybe tomentosipes GDGM43351 MG685872 MG696901 MG696905
Sinohygrocybe tomentosipes GDGM43347 MG696900 MG696904
Sinohygrocybe tomentosipes GDGM50075 MG685873 MG696902 MG696906
Sinohygrocybe tomentosipes GDGM50149 MG685874 MG696903 MG675232
Typhula phacorrhiza TP21 AF134710 AF393079 AY218525

The ITS dataset included 30 samples of all known taxa of tribe Chromosereae and 2 Hygrocybe sequences chosen as the outgroups, the matrix length is 679 bp. In the ITS Maximum Likelihood tree (Fig. 2), collections of the species G. nitidus and G. vitellinus were clustered together with 93% and 100% support values, respectively and the North American and the East Asian G. nitidus were clustered as sister groups with 93% support value; all the members of Chromosera (except C. viola), Gloioxanthomyces and Sinohygrocybe were clustered together with 95%, 93% and 100% support values, respectively; and the Chromosera-Gloioxanthomyces clade was presented as the sister clade of the Sinohygrocybe clade with strong support value (100%).

Figure 2. 

Phylogenetic overview of the tribe Chromosereae inferred from ITS data using ML method. Two Hygrocybe conica sequences were rooted as outgroups. Bootstrap values (≥50%) are shown around the branches. GenBank accession numbers of downloaded sequences were added after the species name and the collection locations were added at the ends. NA, EA and EU referred to North America, East Asia and Europe, respectively. The newly generated sequences are shown in bold.

Taxonomy

Sinohygrocybe C.Q. Wang, Ming Zhang & T.H. Li, gen. nov.

MycoBank No: MB824821

Diagnosis

Differs from Chromosera and Gloioxanthomyces by its less omphalioid, more robust basidiomata, dry to subviscid pileus, dry and white tomentose stipe, more elongated basidia, higher length ratio (up to 8 times) of basidia to basidospores.

Etymology

Sino- refers China, the holotype’s location of the genus; -hygrocybe indicates that it is a Hygrocybe-like genus.

Type species

Sinohygrocybe tomentosipes C.Q. Wang, Ming Zhang & T.H. Li

Description

Basidiomata medium-sized, subcaespiotose. Pileus convex to applanate, slightly depressed in the centre, yellow, orangish-yellow to orange, dry to subviscid, slightly when wet, never strongly gelatinised or glutinous. Lamellae adnate to decurrent, concolorous with pileus, with usually furcate and interveined lamellulae. Stipe yellow to whitish or almost concolorous with pileus, yellow or covered by white to yellowish-white tomentum. Basidiospores ellipsoid to oblong, ovoid, Qm = 1.6-1.7, not constricted, thin-walled, inamyloid, hyaline, smooth; basidia usually 4-sterigmate, 41–80 μm long, ratio of basidia to basidiospore length over 5 (up to 8), with basal clamp connection. Pileipellis and stipitipellis a cutis. Lamellar trama subregular. Clamp connections present throughout.

Sinohygrocybe tomentosipes C.Q. Wang, Ming Zhang & T.H. Li, sp. nov.

MycoBank No: MB824824
Figs 3, 4

Diagnosis

Differs from the other members of the tribe Chromosereae by its larger and more robust basidiomata, concolorous yellow pileus, lamellae and the subsurface of stipe, usually furcate and interveined lamellae and lamellulae, white fibrillose stipe surface, long basidia (up to 80 μm), ratio of basidia to basidiospore length over 5 and even up to 8.

Etymology

The species epithet tomentosipes refers to the tomentose stipe.

Type

China. Sichuan Province, Panzhihua City, Yanbian County, Gesala Eco-tourism Area, at 27°16'N, 101°26'E, alt. 3100 m, 24 Aug 2013, Ming Zhang (GDGM43351, holotype).

Description

Basidiomata small to medium-sized. Pileus 2.5–6 cm diam., convex to applanate, usually slightly depressed in the centre, smooth, dry but subviscid when wet, light yellow to vivid yellow (3A5–8) or to deep yellow (4A5–8), or light orange to dark orange (5A5–8), becoming paler when dry; margin even, straight or upturned and occasionally split when mature. Lamellae up to 7 mm wide, adnate to sinuate or decurrent, distant, 17–22 lamellae per pileus, with 1–3 lamellulae between two complete lamellae, usually furcate, often interveined or anastomosing at lamella base, thick, concolorous with the pileus; lamellar base and lamellulae irregular and occasionally the whole hymenophore irregular; lamellar edge even and concolorous. Context concolorous with lamellae and pileus, unchanged when cut. Stipe 4–6.5 × 0.6–1.2 cm, central or occasionally eccentric, subcylindrical, moderately to densely covered with white tiny adpressed fibres. Odour indistinct.

Basidiospores 8–10(–10.5) × (4.5–)5–7(–7.5) μm, Q = (1.3–)1.5–1.8, Qm = 1.6–1.7, ellipsoid to ellipsoid-oblong, ovoid, not constricted, thin-walled, hyaline, smooth. Basidia 41–80 × 4–10 μm, strongly elongated, narrow clavate, 4-spored, thin-walled; sterigmata up to 10 μm long; ratio of basidia to basidiospore length over 5 and up to 8. Hymenophoral trama subregular, yellow, made up of thin-walled hyphae 3–15 µm wide and usually less than 100 μm long and some conducting elements. Pileipellis a cutis, made up of repent hyphae 3–9 µm wide with the terminal elements 30–80 µm long. Stipitipellis a cutis, with thin-walled hyphae (5–7 μm wide). Clamp-connections present in all tissues.

Habitat and known distribution

Gregarious, caespitose, or scattered in broad-leaf forest in subtropical temperate transition zone, so far known only from Sichuan and Hunan Provinces in China.

Additional specimens examined

CHINA, Sichuan Province, Panzhihua City, Yanbian County, Gesala Eco-Tourism Area, at 27°16'N, 101°26'E, alt. 3100 m, 24 Aug 2013, Ming Zhang (GDGM43347), Chao-Qun Wang (GDGM43352); Hunan Province, Zhuzhou City, Yanling County, Taoyuandong National Nature Reserve, at 26°19'N, 114°00'E, alt. 1534 m, 23 Nov 2013, Chao-Qun Wang (GDGM50075 and GDGM50149).

Figure 3. 

Basidiomata of Sinohygrocybe tomentosipes (a–b GDGM43351 c–d GDGM43352 e GDGM43347 f GDGM50075 g–h GDGM50149). Scale bars: 2 cm.

Figure 4. 

Line drawings of Sinohygrocybe tomentosipes. a Basidiomata b Basidiospores c Basidia d Elements of pileipellis cells e Elements of gill trama.

Gloioxanthomyces nitidus (Berk. & M.A. Curtis) Lodge, Vizzini, Ercole & Boertm., Fungal Diversity 64: 50 (2014)

Figs 5, 6

= Hygrophorus nitidus Berk. & M.A. Curtis, Ann. Mag. nat. Hist., Ser. 2 12: 424 (1853).

Description

Pileus 1.5–3.5 cm wide, convex to nearly plane with a slightly depressed disc, strongly glutinous, yellow, light orange yellow to apricot yellow, even whitish-yellow when mature, clearly striate at margin; pileus margin usually slightly undulating, slightly incurved when young, expanded to flat or partially uplifted when mature. Context thin, yellow to nearly concolorous with pileus, hygrophanous and translucent. Lamellae arcuate-decurrent, narrow at both ends, bright yellow or slightly orange yellow, waxy and fragile, subdistant, usually having 1–3 unequal lamellulae between two lamellae; lamellar edge even, usually gelatinised and sometimes translucent. Stipe 2.5–6 × 0.2–0.5 cm, cylindrical, hollow, yellow to slightly greenish-yellow, smooth, sticky or glutinous with a layer of viscid and translucent material when wet, nearly equal mostly but usually tapering at base.

Basidiospores 7–9(11) × 5–6.5(7.5) μm, Q=1.25–1.7, Qm=1.48, ellipsoid, not constricted, smooth, hyaline, thin-walled. Basidia 29–39 × 7.5–10 μm, clavate, 4-spored; sterigmata up to 5 μm. Lamellar trama subregular, with hyphal elements 10–20 μm wide. Pileipellis an ixotrichoderm. Clamp connections present.

Habitat and known distribution

Solitary or scattered, on moist ground in a mixed forest with mosses in North-eastern China, so far known in North America and East Asia.

Material examined

CHINA. Jilin Province, Antu County, Changbaishan Mountains, 20 August 2012, Ming Zhang, Jiang Xu, Chao-Qun Wang (GDGM41710, GDGM42150 and GDGM42151).

Figure 5. 

Basidiomata of Gloioxanthomyces nitidus (a–b GDGM41710 c–d GDGM42150 e–f GDGM42151).

Figure 6. 

Line drawings of Gloioxanthomyces nitidus (GDGM41710). a basidiomata b basidiospores c basidia.

Discussion

Phylogenetically, the distinction of the three subfamilies (Lodge et al. 2014) within Hygrophoraceae has very convincing support in the multi-locus tree of this study (Fig. 1). In addition, the establishment of the three well-defined monophyletic tribes in subfamily Hygrocyboideae is supported in this phylogenetic frame where the tribe Hygrocybeae with 73% support values and the tribe Humidicuteae with low support value are sister clades, while the tribe Chromosereae with 76% support values is located at their base. However, the cuphophylloid grade appears not to be monophyletic, thus more studies are still needed to understand the phylogenetic positions of Ampulloclitocybe, Cantharocybe H.E. Bigelow & A.H. Sm. and Cuphophyllus (Donk) Bon.

In the multi-gene analyses, Sinohygrocybe is placed together with two other genera in Chromoserae. Chromosera and Gloioxanthomyces are sister genera under the monophyletic tribe Chromosereae, while Sinohygrocybe is an independent generic lineage; and the distances between Sinohygrocybe and Chromosera or Gloioxanthomyces are further than the distance between Chromosera and Gloioxanthomyces. Such results are confirmed in the ITS phylogenetic tree (Fig. 2). According to the Blastn results, the ITS and LSU sequence identities of the new species to the known taxa are not more than 76% and 96%, respectively, with the Chromosera and Gloioxanthomyces sequences in GenBank. Thus, it is clear the new genus is independent of those two existed genera.

Beside the molecular analyses, morphological data also support its recognition within tribe Chromosereae. Sinohygrocybe shares a bright pileus colour and decurrent lamellae with the other genera Chromosera and Gloioxanthomyces (Table 2). However, the genus Chromosera, typified by C. cyanophylla (Fr.) Redhead, Ammirati & Norvell, differs from Sinohygrocybe in having omphaloid basidiomata, ephemeral dextrinoid reactions in the context, ratio of basidiospore to basidium length <5, ephemeral pigment bodies in the pileipellis and lilac pigments sometimes present (Redhead et al. 1995, Candusso 1997, Lodge et al. 2014); while Gloioxanthomyces differs from Sinohygrocybe by having weaker/delicate basidiomata, viscid pileus and stipe surface, gelatinised lamellar edge and cheilocystidia, shorter basidia (Boertmann 1990, 2012) with a length ratio of basidium to basidiospore 4–5. Sinohygrocybe shares some macroscopic characters with Hygrocybe, typified by H. conica, including bright colour of basidiomata and the distant lamellae, but Hygrocybe differs from Sinohygrocybe by having more fragile lamellae, more glabrous stipe (at least at the upper portion), often constricted spores and shorter basidia.

Sinohygrocybe samples were collected in both late summer (August) and winter (November), showing that they likely have a quite long fruiting season. It should be noted, however, that they are more abundant at times with lower temperature and higher humidity. Therefore, their fruiting in summer may occur only at higher altitude (with the elevation above 1500 m).

As to the Chinese new Gloioxanthomyces nitidus record: 1) phylogenetically, the Chinese samples are nested in the Gloioxanthomyces clade as a sister branch to the North American branch (Fig. 2); 2) morphologically, it shares these characters with the North American G. nitidus: deep yellow basidiomata fading to whitish with age, viscid, hygrophanous surface, central concave pileus and decurrent lamellae (Bessette et al. 2012); 3) geographically, G. nitidus and G. vitellinus are distributed in North America and Asia and Europe, respectively, indicating that Gloioxanthomyces is a Holarctic genus. It is assumed that both North American and East Asian G. nitidus were separated from the same ancestor because of geographical isolation, thus they are very similar at present; however, they may continue to diverge, eventually becoming separate species in the future since they live on detached continents.

Type location, basidiospores and basidia dimensions of species of the tribe Chromosereae.

Species name Type location Basidiospores (μm) Basidia (μm) Reference
Gloioxanthomyces nitidus USA, South Carolina 6.5–9(11) × 4–6.5(7.5) 29–39 × 7.5–10 Bessette et al. 2010, this study
Gloioxanthomyces vitellinus Sweden (6.5)7–9(9) × (5)5.5–7(7.5) 30–45 × 7–10 Boertmann 2010
Chromosera citrinopallida USA, Washington 7–9(10) × 4.5–5 10–45 × 6–8 Smith and Hesler 1954
Chromosera cyanophylla Sweden (6.8)7.2–8.0(8.8) × (3.2)3.6–4.4 24–28 × 5.5–6.5 Holec et al. 2015
Chromosera lilacina northern Fennoscandia 7–8.5(10) × (4)5–6(6.5) 30–45 × 7–9 Candusso 1997
Chromosera viola Belgium, Namur Province 6.5–10.5(11) × 5–7(7.5) 36–61 × 8–11 Candusso 1997
Chromosera xanthochroa Scotland (5.5)6–8.5(10) × (3.8)4–5.2(5.5) 25–32 × 6.5–7.5(8.5) Candusso 1997
Sinohygrocybe tomentosipes China, Sichuan & Hunan Province 8–10(10.5) × (4.5)5–7(7.5) 41–80 × 4–10 This study

Acknowledgments

Sincere acknowledgements are expressed to Dr. Xiao-Lan He and Dr. Egon Horak, Mr. Ye-Wei Xia and members of Dr. Wen-Bo Liao’s laboratory, Dr. Jiang Xu and Mrs. Xin Zhang for their help during the field trips in Gesala, Taoyuandong and Changbai Mountains, respectively; to Dr. Tolger Bau for trying to find some additional samples in HMJAU; to Dr. David Boertmann, Dr. Md. Iqbal Hosen and Dr. Wang-Qiu Deng for their improvements and constructive comments on an earlier version of this paper; to Dr. David Hibbett and the International Exchange Scholarship of the University of Chinese Academy of Sciences for providing an opportunity to the first author to learn molecular data analyses. This study was financed by the Ministry of Science and Technology of China (Nos. 2013FY111500, 2013FY111200), the Science and Technology Program of Guangzhou, China (No. 201607020017), the GDAS’ Special Project of Science and Technology Development (2018GDASCX-0907) and the Science and Technology Project of Guangdong Province (2017A030303050).

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