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Research Article
Taxonomic study of Collybiopsis (Omphalotaceae, Agaricales) in the Republic of Korea with seven new species
expand article infoJi Seon Kim, Yoonhee Cho, Ki Hyeong Park, Ji Hyun Park§, Minkyeong Kim|, Chang Sun Kim, Young Woon Lim
‡ Seoul National University, Seoul, Republic of Korea
§ National Institute of Environmental Research, Incheon, Republic of Korea
| National Institute of Biological Resources, Incheon, Republic of Korea
¶ Korea National Arboretum, Pocheon-si, Republic of Korea
Open Access

Abstract

Collybiopsis is a genus of the gymnopoid/marasmioid complex of the family Omphalotaceae. The classification system of Collybiopsis has recently undergone large changes through molecular approaches. The new classification system has not been applied for Collybiopsis in the Republic of Korea, and general research on this genus was also lacking. In this study, we analyzed the Collybiopsis species in the Republic of Korea by assessing all gymnopoid/marasmioid specimens collected nationwide for ten years by combining morphological approaches and multilocus (ITS + nrLSU) phylogenetic analysis. We thus confirmed that 16 species of Collybiopsis are present in the Republic of Korea, including two previously unreported species (Co. nonnulla and Co. dichroa) and seven new species (Co. albicantipes sp. nov., Co. clavicystidiata sp. nov., Co. fulva sp. nov., Co. orientisubnuda sp. nov., Co. subumbilicata sp. nov., Co. undulata sp. nov., and Co. vellerea sp. nov.). A thorough examination of the Collybiopsis suggested that it is difficult to distinguish or identify the species based on morphological characteristics only; a combined molecular approach is needed for accurate identification. The Collybiopsis database of the Republic of Korea is updated, and information on the new species is provided. Five new combinations from Marasmiellus to Collybiopsis are also proposed (Co. istanbulensis comb. nov., Co. koreana comb. nov., Co. omphalodes comb. nov., Co. pseudomphalodes comb. nov., and Co. ramuliciola comb. nov.).

Keywords

Collybia, gymnopoid, Gymnopus, ITS, Marasmiellus, marasmioid, nrLSU

Introduction

Collybiopsis Earle (1909) is a genus of gymnopoid/marasmioid mushrooms belonging to the family Omphalotaceae Bresinsky (Earle 1909; Petersen and Hughes 2021). Species of Collybiopsis are characterized by collybioid, gymnopoid, marasmielloid, omphalioid, and pleurotoid basidiomata; free to decurrent lamellae; a central to eccentric, insititious to subinsititious stipe; ellipsoid to oblong, inamyloid, and hyaline basidiospores with white sporeprints; presence of caulocystidia; and coralloid or diverticulate terminal elements of pileipellis (Murrill 1915; Singer 1973; Antonín and Noordeloos 1993; Retnowati 2018; Oliveira et al. 2019). Owing to its relatively uncharacteristic basidiocarp and little variation in morphological characteristics, most gymnopoid/marasmioid species were previously placed within the genus Collybia Staude (1857) and Marasmius Fr. (1835) before molecular identification was introduced actively to taxonomy. However, recent molecular studies have clarified the phylogenetic relationship of gymnopoid/marasmioid species belonging to the family Omphalotaceae and family Marasmiaceae Roze ex Kühner (Wilson and Desjardin 2005; Oliveira et al. 2019).

Initial molecular studies have segregated Collybia and Marasmius and some species of both genera transferred into several genera such as Gymnopus Roussel, Marasmiellus Murril, Rhodocollybia Singer, etc. (Moncalvo et al. 2002; Mata et al. 2004b; Mata et al. 2004c; Wilson and Desjardin 2005; Hughes et al. 2010; Oliveira et al. 2019; Petersen and Hughes 2017, 2021). Five Collybia sections (Iocephalae Halling, Levipedes Quél, Striipedes Quél, Subfumosae Singer, and Vestipedes Quél) were subsumed into Gymnopus sensu lato (s.l.) (Mata et. al., 2004c). However, Gymnopus s. l. is polyphyletic, and there has been much debate on the delimitation of this genus (Mata et al, 2004c; Wilson and Desjardin 2005; Mata et al. 2006; Oliveira et al. 2019; Petersen and Hughes 2016). Prior to this debate, a monophyletic genus, Marasmiellus sensu stricto (s. str.), was proposed (Wilson and Desjardin 2005), with Marasmiellus juniperinus Murrill as the monotype species (Wilson and Desjardin 2005; Sandoval-Leiva et al. 2016; Oliveira et al. 2019). A recent study showed that if judged congeneric, Collybiopsis Earle (1909) has priority over Marasmiellus Murrill (1915) based on the nomenclature rule (Petersen and Hughes 2021). Hereupon, Collybiopsis has been redefined based on the type species, Collybiopsis ramealis Earle, with at least 44 closely related species (Petersen and Hughes 2021). All species of Collybiopsis and some species of Gymnopus sect. Vestipedes, as well as some species of Marasmiellus, are included in the genus Collybiopsis (Petersen and Hughes 2021).

Collybiopsis is morphologically similar and phylogenetically close to Gymnopus (Desjardin et al. 1999; Mata 2002; Dutta et al. 2015). Both genera are reported to be distinguishable through like types of the terminal element of pileipellis, attachment of lamellae, the character of stipe, basidiospores, and cheilocystidia. However, as the characteristics of each genus cannot be seen as absolute because exceptions exist, and some characteristics overlap, it is difficult to distinguish Collybiopsis from Gymnopus solely on morphology. Furthermore, the morphological characteristics of their basidiomata vary greatly depending on the environment and developmental stage. Therefore, molecular data play an important role in distinguishing these genera (Antonín and Herink 1999; Hughes et al. 2014; Hughes and Petersen 2015).

Although there have been many taxonomic changes for gymnopoid/marasmioid species, these changes have not been reflected in the gymnopoid/marasmioid species in the Republic of Korea. Since the first report of Collybiopsis confluens (Pers.) R.H. Petersen, as its previous name Collybia confluens Fr. (Kaburagi 1940), nine current Collybiopsis species have been reported until recently (National list of species of Korea 2020). However, they were identified and classified as Collybia, Gymnopus, and Marasmiellus based on their macroscopic morphological features. Owing to the uncertain placement of previous morphologically identified collybioid collections, it was necessary to re-examine Korean collections of collybioids and marasmioids based on molecular data. In this study, we investigated gymnopoid/marasmioid specimens collected over 10 years and deposited in three Korean herbaria based on their molecular analysis. As a result, we provide a list of Collybiopsis species in the Republic of Korea with seven new species.

Methods

Collections of specimens

A total of 372 specimens deposited in three Korean fungal herbarium – Seoul National University Fungus Collection (SFC), Korea National Arboretum (KA), and the National Institute of Biological Resources (NIBR) – were used in this study. The specimens were collected from 2012 to 2021 and stored in dried condition. All specimens were identified based on their morphological characteristics by each herbarium. The collection information (e.g. collection date, collection site, collector, etc.) and the notes of fresh basidiomata of each specimen were provided from each herbarium.

Molecular analysis

Genomic DNA was extracted from each specimen using a modified CTAB DNA extraction protocol (Rogers and Bendich 1994). The primer set ITS1F/ITS4B (Gardes and Bruns 1993) was used to amplify the internal transcribed spacer (ITS) region for all specimens, and the primer set LR0R/LR5 (Vilgalys and Hester 1990; Rehner and Samuels 1994) was used to amplify the nuclear large subunit ribosomal RNA (nrLSU) region. PCR was conducted by a C1000 thermal cycler (Bio-Rad, Richmond, CA, USA) using AccuPower PCR master premix (Bioneer Co., Daejeon, the Republic of Korea). PCR conditions for ITS and nrLSU region were: 5 min initial denaturation at 95 ˚C followed by 35 cycles of 40 s at 95 ˚C, 40 s at 55 ˚C and 60 s at 72 ˚C with a final extension step for 7 min at 72 ˚C. The amplifications of the PCR products were verified by visualization using 1% agarose gels with EcoDye DNA staining solution (SolGent Co., Daejeon, the Republic of Korea). The PCR products were purified using the ExpinTM PCR Purification Kit (GeneAll Biotechnology, Seoul, the Republic of Korea) following the manufacturer’s instructions. The purified PCR amplicons were sequenced using an ABI Prism 3700 Genetic Analyzer (Life Technologies, Gaithersburg, MD, USA) at Macrogen (Seoul, the Republic of Korea).

All sequences generated in this study were proofread using MEGA version 7 (Kumar et al. 2016). The sequences used for analyses were deposited in GenBank (Table 1). We then selected the closely related sequences from NCBI databases mainly referred to Oliveira et al. (2019) and Petersen and Hughes (2021). After retrieving all published ITS and nrLSU sequences of all Collybiopsis species in GenBank, phylogenetic analyses were performed together with new sequences generated from specimens. The sequences were respectively aligned for each loci using Multiple Alignment Fast Fourier Transform (MAFFT ver. 7) with the L-NSI-I option algorithm (Katoh and Standley 2013). The aligned sequence data were manually checked and edited. The final sequence of each specimen was created as a concatemer by manually attaching the aligned sequences of the two loci. Maximum likelihood (ML) phylogenetic tree was constructed on the CIPRES Science Gateway (Miller et al. 2012) using the GTR+GAMMA model with 1000 bootstrap replicates. Rhodocollybia butyraceae Lennox (TFB14382), Rhodocollybia dotae JL Mata and Halling (REH7007), and Rhodocollybia maculate Singer (TFB13989) were used as outgroups (Oliveira et al. 2019). Bootstraps higher than 70% were considered to support a clade and are shown in the tree (Figure 1).

Table 1.

Information about the Collybiopsis specimens and published Collybiopsis sequences used in phylogenetic analysis. Species with an asterisk are those proposed as new species. Sequences newly produced in this study are presented in bold.

Organisms Specimen Collection Date Location GenBank Accession Number
ITS nrLSU
Collybiopsis albicantipes * SFC20170725-35 25.7.2017 Yeosu-si, Jeollanam-do, the Republic of Korea OL467272 OL462811
SFC20180704-86 4.7.2018 Jindo-gun, Jeollanam-do, the Republic of Korea OL467273 OL462812
Co. biformis TFB14251 USA: Tennessee, GSMNP KJ416245 KJ189567
TFB13890 USA: North Carolina KJ416248 KJ189570
TFB13814 USA: Tennessee KJ416249 KJ189569
KA14-0526 15.7.2014 Suncheon, Jeollanam-do, the Republic of Korea OL467227 OL462784
KA16-0526 13.7.2016 Sinan-gun, Jeollanam-do, the Republic of Korea OL467228 OL462785
SFC20180704-36 4.7.2018 Wando-gun, Jeollanam-do, the Republic of Korea OL467229 OL462789
SFC20180831-16 31.8.2018 Jindo-gun, Jeollanam-do, the Republic of Korea OL467230 OL462790
Co. brunneigracilis AWW01 Java/Bali AY263434 AY639412
Co. californica TFB5787 Canada: British Columbia MN413338
Co. clavicystidiata * SFC20180705-26 5.7.2018 Haenam-gun, Jeollanam-do, the Republic of Korea OL467250 OL462816
SFC20180705-84 5.7.2018 Jindo-gun, Jeollanam-do, the Republic of Korea OL467252 OL462817
SFC20180705-92 5.7.2018 Jindo-gun, Jeollanam-do, the Republic of Korea OL467253 OL462818
SFC20180713-09 13.7.2018 Gwanak-gu, Seoul, the Republic of Korea OL467251 OL462819
Co. confluens SFC20190731-06 31.7.2019 Taebaek-si, Gangwon-do, the Republic of Korea OL467237 OL462797
SFC20190731-48 31.7.2019 Taebaek-si, Gangwon-do, the Republic of Korea OL467238 OL462798
TFB14115 Germany, Thuringia KP710292 KJ189578
110116MFBPL0425 China MW554401
HMAS 290186 China MK966541
Co. confluens ssp. americana TFB14409 Canada: New Brunswick KP710278 KJ189585
TFB14075 USA: North Carolina KP710281 KJ189581
Co. dichroa KA14-0969 19.8.2014 Hwasun-gun, Jeollanam-do, the Republic of Korea OL467254 OL462799
KA18-0389 10.7.2018 Cheongdo-gun, Gyeongsangbuk-do, the Republic of Korea OL467255 OL546541
SFC20180712-16 12.7.2018 Gwangju, Gyeonggi-do, the Republic of Korea OL467256 OL462800
TFB9623 USA: North Carolina MW396865 MW396865
TENN60014c2 USA: Tennessee, GSMNP JF313671
TFB7920 USA DQ450007
TENN61624c1a USA: Tennessee, GSMNP JF313678
TFB2028 USA DQ450008
TENN61624c9 USA: Tennessee, GSMNP JF313692
Co. disjuncta TFB14339 USA: Connecticut NR_137865
TFB14281 USA: Mississippi KJ416253 KY019643
Co. eneficola 09-09-26AV13 Canada: Newfoundland NR_137613 NG_059502
MICH:PK6975 Alaska KP710270 KP710304
Co. fibrosipes FB9699 Costa Rica AF505763
Co. filamentipes TFB13962 USA: Tennessee MN897832 MN897832
Co. foliiphila CUH AM090 India NR_154176 NG_060320
CUM AM101 India KP317638 KP317636
Co. fulva * KA13-0216 19.6.2013 Geochang-gun, Gyeongsangnam-do, the Republic of Korea OL467257 OL462793
KA13-0333 10.7.2013 Pocheon-si, Gyeonggi-do, the Republic of Korea OL467258 OL462794
KA15-0210 21.7.2015 Pocheon-si, Gyeonggi-do, the Republic of Korea OL467259 OL462795
Co. furtiva TFB4796 USA: Georgia MN413343 MW396879
Co. gibbosa MEL:2382838 Australia KP012713 KP012713
URM 90012 Brazil KY061202 KY061202
Co. hasanskyensis TFB11846 Russia: Kedrovaya MN897829
TFB11847 Russia MN897830
Co. indoctus AWW04 Unknown AY263439
Co. istanbulensis KATO Fungi 3596 Turkey KX184795 KX184796
BRNM 781163 Turkey KY250435
Co. juniperina TFB9889 USA: Louisiana AY256708 KY019637
TFB10782 Argentina: Missiones KY026661 KY026661
Co. koreana SFC20120821-84 21.8.2012 Boryeong-si, Chungcheongnam-do, the Republic of Korea OL467269 OL546545
SFC20130711-05 11.7.2013 Pyeongchang-gun, Gangwon-do, the Republic of Korea OL467270 OL462801
SFC20150721-10 21.7.2015 Inje-gun, Gangwon-do, the Republic of Korea OL467271 OL462802
BRNM 714972 Korea GU319113 GU319117
BRNM 718782 Korea GU319114 GU319118
Co. luxurians NIBRFG0000502888 4.9.2018 Ongjin-gun, Incheon, the Republic of Korea OL467248 OL462803
SFC20190731-18 31.7.2019 Taebaek-si, Gangwon-do, the Republic of Korea OL467249 OL462804
TFB10350 USA: North Carolina AY256709 AY256709
ZD16102301 China MN523270
TFB9121 USA: Louisiana KY026649 KY026649
Co. melanopus AWW54 Java/Bali NR_137539 NG_060624
CUH AM093 India KM896875 KP100305
Co. menehune SFC20150811-29 11.8.2015 Guri-si, Gyeonggi-do, the Republic of Korea OL467235 OL462805
SFC20180905-33 5.9.2018 Anyang City, Gyeonggi Province, the Republic of Korea OL467236 OL462806
SFSU: DED5866 Hawaii AY263426
CUH:AM074 India KJ778753 KP100302
SFSU-AWW15 Java/Bali AY263443 AY639424
Co. mesoamericana TFB11005 Costa Rica DQ450035 KY019632
REH7379 Costa Rica AF505768
Co. micromphaleoides TENN 68165
TFB14282
Co. minor TFB11930 USA: Tennessee, GSMNP MN413334 MW396880
TFB5434 USA: South Carolina MW396872 MW396872
Co. neotropica TFB10416 Costa Rica AF505769
Co. nonnulla KA13-0254 20.6.2013 Geochang-gun, Gyeongsangnam-do, the Republic of Korea OL467242 OL462820
KA13-0741 21.8.2013 Geochang-gun, Gyeongsangnam-do, the Republic of Korea OL467243 OL462807
KA15-0129 14.7.2015 Gangneung-si, Gangwon-do, the Republic of Korea OL467244 OL462808
TFB14492 USA: Mississippi KY026699 KY026699
TFB14278 USA: Mississippi KY026701 KY026701
Co. nonnulla var. attenuatus AWW05 Java/Bali AY263445 AY639426
AWW55 Java/Bali AY263446
RAK369.2 Cameroon MN930621
RAK372.2 Cameroon MN930622
Co. obscuroides GB-0150514 Norway: Svalbard KX958399 KX958399
Co. omphalodes FB11021 Costa Rica AF505761
TFB 10427 Costa Rica DQ450011
TFB 10022 Costa Rica AY256700
Co. orientisubnuda * NIBRFG0000500990 19.7.2016 Ulleung-gun, Gyeongsangbuk-do, the Republic of Korea OL467262 OL546546
SFC20170823-39 23.8.2017 Hapcheon-gun, Gyeongsangnam-do, the Republic of Korea OL467263 OL546547
SFC20180830-29 30.8.2018 Hapcheon-gun, Gyeongsangnam-do, the Republic of Korea OL467264 OL462796
(as Gymnopus subnudus) KUC20150911-19 Korea KX513748
Co. parvula TFB10419 Costa Rica DQ450060
TFB10422 Costa Rica AF505774
Co. peronata TFB13743 Belgium KY026677 KY026677
LE-Bin1364 Russia KY026755 KY026755
CBS 223.37 unknown MH855896 MH867405
Co. polygramma SFC20170807-35 7.8.2017 Hapcheon-gun, Gyeongsangnam-do, the Republic of Korea OL467245 OL546542
SFC20180905-63 5.9.2018 Gwanak-gu, Seoul, the Republic of Korea OL467246 OL546544
SFC20210629-01 29.6.2021 Gwanak-gu, Seoul, the Republic of Korea OL467247 OL546543
PR2542TN Puerto Rico DQ450028
CUH:AM082 India KJ778752 KP100303
URM 90015 Brazil: Amapa KY074640 KY088275
MHHNU 30912 China MK214392
TFB9628 Puerto Rico DQ450028
SFC20120821-64 Korea KJ609162
HFJAU 0425 China: Jiangxi MN258643
(as Gymnopus iocephalus) KUC20140804-02 Korea KX513745
Co. pseudoluxurians TFB14290 USA: Mississippi NR_137863
Co. pseudomphalodes REH7348 Costa Rica AF505762
PR24TN Puerto Rico AY842957
Co. quercophila TFB14570 Slovakia KY026728 KY026728
TFB14615 USA: California KY026736 KY026736
Co. ramealis NIBRFG0000508888 29.7.2020 Jeongseon-gun, Gangwon-do, the Republic of Korea OL467260 OL546549
TFB13769 Belgium: Couvin MN413345 MN413345
TFB13770 Belgium: Couvin MN413346 MW396882
DED4425 USA: North Carolina DQ450031 AF042650
TFB14555 Slovakia MW405779 MW396884
BR 72_41 Belgium MW396875 MW396875
Co. ramulicola GDGM 43884 China KU057798
GDGM 44256 China KU321529
GDGM 50060 China KU321530
Co. readiae TFB7571 New Zealand DQ450034
PDD:95844 New Zealand HQ533036
Co. stenophylla TFB13998 USA: Tennessee, MN413331 MW396886
TFB4798 USA: Georgia MN413330 MW396887
Co. subcyathiformis TFB9629
URM 90023 Brazil: Para KY404982 KY404982
URM 90022 Brazil: Para KY404983 KY404983
Co. subnuda TFB12577 USA: Tennessee, GSMNP KY026667 FJ750262
WRW 08-462 USA: West Virginia KY026765 KY026765
TFB14043 USA: North Carolina MW396876 MW396876
Co. subpruinosus BRNM781138 Portugal: Madeira MK646034
TFB11063 USA DQ450025
Co. subumbilicata * SFC20120802-03 2.8.2012 Goseong-gun, Gangwon-do, the Republic of Korea OL467231 OL462786
SFC20140701-03 1.7.2014 Inje-gun, Gangwon-do, the Republic of Korea OL467232 OL462787
SFC20150902-50 2.9.2015 Ulleung-gun, Gyeongsangbuk-do, the Republic of Korea OL467234 OL546540
SFC20170822-14 22.8.2017 Ulleung-gun, Gyeongsangbuk-do, the Republic of Korea OL467233 OL462788
Co. trogioides AWW51 Indonesia AY263428 AY639431
Co. undulata * SFC20120821-04 21.8.2012 Boryeong-si, Chungcheongnam-do, the Republic of Korea OL467239 OL462813
SFC20130808-08 8.8.2013 Sangju-si, Gyeongsangbuk-do, the Republic of Korea OL467240 OL462814
SFC20150813-04 13.8.2015 Goyang-si, Gyeonggi-do, the Republic of Korea OL467241 OL462815
Co. utriformis TFB14334h1 USA: Connecticut KY026708 KY026708
WRW05-1170 USA: West Virginia KY026764 KY026764
Co. vellerea * NIBRFG0000502858 4.9.2018 Ongjin-gun, Incheon, the Republic of Korea OL467265 OL462791
SFC20120708-02 8.7.2012 Seosan-si, Chungcheongnam-do, the Republic of Korea OL467266 OL462809
SFC20140821-29 21.8.2014 Gwanak-gu, Seoul, the Republic of Korea OL467267 OL462810
SFC20180705-90 5.7.2018 Jindo-gun, Jeollanam-do, the Republic of Korea OL467268 OL462792
Co. vallianti TFB13739 USA: Tennessee, GSMNP KY026676 KY026676
Co. villosipes TFB9539 USA DQ450058
TFB12836 New Zealand: Fiordland KJ416255 FJ750264
Collybiopsis cf. ramealis SFC20180829-20 29.8.2018 Shinan-gun, Jeollanam-do, the Republic of Korea OL467261 OL546548
Rhodocollybia butyracea TFB 14382 Canada: New Brunswick KY026716 KY026716
Rhodocollybia dotae REH7007 Costa Rica AF505758
Rhodocollybia maculata TFB 13989 USA: Mississippi KY026688 KY026688
Figure 1. 

Phylogenetic tree based on maximum likelihood analysis using combined sequence data of ITS and nrLSU. ML bootstrap values greater than 70% are indicated at the nodes. Collybiopsis species that were newly sequenced in this study are represented in bold. Species with an asterisk are those proposed as new species.

Morphological observation

All specimens were preliminarily observed and macro/micro-structures of two to four representative specimens, which were in the best condition among the specimens, were presented in figures. Photographs and notes of fresh basidiomata taken at the time of collection were used for macro-morphological description. For micro-morphological observations, tissues of dried specimens were rehydrated in 5% (w/v) KOH and mounted in Congo red solution (Clémençon 1973) and Melzer’s reagent. The observation was performed by using a Nikon Eclipse 80i optical microscope (Nikon, Tokyo, Japan) at 20 × to 1000 × magnification. More than thirty basidiospores and more than twenty other microstructures (e.g., basidia, cheilocystidia, etc.) were measured to analyze the microstructures based on the microscopic pictures of specimens stained with Congo red. The Methuen Handbook of Colour (Kornerup and Wanscher 1978) was used for color indications. The following abbreviations and acronyms were used: Co. = Collybiopsis; G = Gymnopus; Ma = Marasmiellus; L = the number of complete lamellae; l = the number of lamellulae tiers between neighboring complete lamellae; and Q = the values of the length divided by the width of basidiospores (Petersen and Hughes 2021; Ryoo et al. 2020).

Results

Through ITS sequence analysis of 372 gymnopoid/marasmioid specimens, 201 specimens were confirmed to belong to Collybiopsis. The remaining 160 specimens were identified as members of the following genera: Gymnopus, Marasmius, or Rhodocollybia and were excluded from this study. A total of 201 specimens were segregated into 16 putative taxa based on ITS phylogenetic analyses (Table 2). To confirm the species’ identity and to infer the phylogenetic relationships within Collybiopsis, the nrLSU region was amplified and sequenced from 47 representative specimens of 16 taxa (Table 1). The final phylogenetic analyses were conducted with datasets of two loci from 16 Collybiopsis species (Table 1). In ML analysis, 178 multigene sequences (110 for ITS and 68 for nrLSU) were retrieved from GenBank and used. The adjusted alignments comprised 535 to 794 bases for ITS and 324 to 904 bases for nrLSU. The phylogenetic analysis results of the two combined loci revealed that Collybiopsis specimens from the Republic of Korea were identified as 16 taxa (Fig. 1).

Table 2.

Identification information of Korean Collybiopsis specimens confirmed in the study. Scientific names in bold indicate new species.

Species Specimen Number
Co. albicantipes SFC20170725-35 SFC20180704-86
Co. biformis NIBRFG0000502789 KA14-0259 KA14-0526 KA14-0917 KA14-0924
KA16-0307 KA16-0371 KA16-0526 KA18-0657 KA18-0673
SFC20140724-41 SFC20160719-42 SFC20180704-36 SFC20180706-05 SFC20180831-13
SFC20180831-16
Co. clavicystidiata KA14-0667 KA14-0724 KA15-0211 KA17-0287 KA17-0369
KA18-0282 KA18-0353 SFC20180705-84 SFC20180705-92 SFC20180706-04
SFC20180713-09
Co. confluens NIBRFG0000508913 NIBRFG0000508991 KA16-0696 KA18-0338 SFC20150626-26
SFC20190731-06 SFC20190731-32 SFC20190731-34 SFC20190731-48
Co. dichroa KA14-0969 KA17-0344 SFC20180706-60 SFC20180712-16
Co. fulva KA13-0215 KA13-0216 KA13-0333 KA13-0357 KA14-0168
KA14-0386 KA14-0666 KA14-0691 KA15-0210 KA16-0425
KA16-0428 KA17-0388 KA17-0596 KA18-0233 KA18-0241
Co. koreana SFC20120821-84 SFC20150702-25 SFC20170713-06 SFC20180704-17
Co. luxurians NIBRFG0000502888 SFC20190731-18 SFC20190731-08 SFC20190730-36 SFC20180907-105
SFC20180905-86 SFC20180905-43 KA18-0321 KA14-0579
Co. menehune NIBRFG0000502876 KA13-0887 KA14-0494 KA14-0510 SFC20150811-29
SFC20160719-15 SFC20180905-33
Co. nonnulla KA13-0254 KA13-0741 KA15-0129
Co. orientisubnuda SFC20170823-39 SFC20170708-14 SFC20150902-01 SFC20150820-59 SFC20150820-01
SFC20150811-48 SFC20150701-100 QM20200911-57 QM20200911-52 KA17-0787
KA17-0600 KA16-1154 KA16-0925 KA16-0902 KA16-0780
KA16-0724 KA15-0179 KA14-0985 KA13-1225 F20200730-24
F20200701-11 F20200630-30 F20180904KCM21 F20160719-12
Co. polygramma KA13-0506 KA13-0956 KA13-1101 KA13-1333 KA14-0904
KA14-1089 KA14-1092 KA18-0115 KA18-0724 QM20200721-07
NIBRFG0000508098 NIBRFG0000508059 NIBRFG0000508089 SFC20170712-08 SFC20170807-35
SFC20170822-66 SFC20180905-49 SFC20180905-63
Co. ramealis SFC20130711-05
Co. subumbilicata KA13-1214 KA15-0173 KA15-0185 KA15-0787 SFC20120802-03
SFC20140701-03 SFC20150902-50 SFC20170822-14 SFC20210623-03
Co. undulata KA17-0335 KA18-0651 KA18-0651 SFC20120821-04 SFC20130808-08
SFC20150715-24 SFC20150813-04
Co. vellerea KA14-0132 KA14-0163 KA14-0196 KA14-0245 KA14-0397
KA14-0412 KA14-0446 KA14-0447 KA14-0474 KA14-0725
KA14-0734 KA14-0735 KA14-0774 KA14-0787 KA14-1005
KA14-1061 KA14-1147 KA14-1349 KA14-1426 KA14-1475
KA14-1555 KA14-1558 KA15-0213 KA15-0215 KA15-0473
KA15-0485 KA15-0502 KA15-0527 KA15-0568 KA16-0191
KA16-0252 KA16-0485 KA16-0783 KA16-0982 KA16-0985
KA16-0986 KA16-0992 KA17-0368 KA17-0586 KA17-0742
KA17-1074 KA18-0089 KA18-0139 KA18-0151 KA18-0152
KA18-0348 KA18-0795 KA18-0836 KA18-0987 KA18-1027
KA19-0125 SFC20120708-02 SFC20120820-02 SFC20140821-29 SFC20150630-38
SFC20150714-01 SFC20170705-06 SFC20180705-90 SFC20180829-30 SFC20180901-01
Collybiopsis cf. ramealis F20200729-14

Of the 16 putative taxa, nine matched with previously described species – Co. biformis (Peck) R.H. Petersen, Co. confluens, Co. dichroa (Berk. & M.A. Curtis) Earle, Co. luxurians (Peck) R.H. Petersen, Co. menehune (Desjardin, Halling & Hemmes) R.H. Petersen, Co. nonnulla (Corner) R.H. Petersen, Co. polygramma (Mont.) R.H. Petersen, Co. ramealis (Bull.) Earle, and Marasmiellus koreanus Antonín, Ryoo & H.D. Pictures of basidiomata are shown in Fig. 2. The other seven taxa formed distinct clades and did not correspond to any known Collybiopsis species. Furthermore, based on the comparison with other Collybiopsis species, these seven species have distinct morphological characteristics, confirming that they were new to science – Co. albicantipes sp. nov., Co. clavicystidiata sp. nov., Co. fulva sp. nov., Co. orientisubnuda sp. nov., Co. subumbilicata sp. nov., Co. undulata sp. nov., and Co. vellerea sp. nov. Illustrations of basidiomata and micro-morphological features are shown in Figs 3 and 4.

Figure 2. 

Basidiomata of the described Collybiopsis species in the Republic of Korea A Co. biformis (SFC20180706–05) B Co. confluens (SFC20190731–06) C Co. dichroa (KA18–0389) D Co. koreana (SFC20180704–17) E Co. luxurians (SFC20190731–18) F Co. menehune (SFC20150811–29) G Co. nonnulla (KA13–0254) H Co. polygramma (SFC20170712–08) I Co. ramealis (SFC20180829–20). Scale bar: 1 cm (A–I).

Figure 3. 

Basidiomata and microscopic characters of the four new Collybiopsis species A, B Co. albicantipes (SFC20170725–35) C, D Co. clavicystidiata (SFC20180705–84) E, F Co. fulva (KA15–0210) G, H Co. orientisubnuda (NIBRFG0000502862). Scale bars: 1cm (A, C, E, G); 20 µm (B, D, F, H). Abbreviations: s basidiospores; b basidia; ch cheilocystidia; p pleurocystidia; ca caulocystidia.

Figure 4. 

Basidiomata and microscopic characters of the three new Collybiopsis species A, B Co. subumbilicata (SFC20120802–03) C, D Co. undulata (SFC20150813–04) E, F Co. vellerea (SFC20140821–29). Scale bars: 1cm (A, C, E); 20 µm (B, D, F). Abbreviations: s basidiospores; b basidia; ch cheilocystidia; p pleurocystidia; ca caulocystidia.

Five species (G. omphalodes Halling & J.L. Mata, G. pseudomphalodes J.L. Mata, G. ramulicola T.H. Li & S.F. Deng, Ma. istanbulensis E. Sesli, Antonín and E.Aytaç, and Ma. koreanus), previously placed in Gymnopus section Vestipedes, were confirmed to belong to the genus Collybiopsis, and we thus propose to reclassify them as Co. omphalodes comb. nov., Co. pseudomphalodes comb. nov., Co. ramulicola comb. nov., Co. istanbulensis comb. nov., and Co. koreana comb. nov. respectively.

Taxonomy

Collybiopsis albicantipes J.S. Kim & Y.W. Lim, sp. nov.

MycoBank No: 842053
Fig. 3A–B, Suppl. material 1: Fig. S1A

Etymology

Epithet “albicantipes” refers to having a whitish base of the stipe.

Holotype

The Republic of Korea, Jeollanam-do: Yeosu-si, Dolsan-eup, Hyangiram, 34°35'27"N, 127°47'55"E, alt. 183 m, 25 July 2017, Jae Young Park, Komsit Wisitrassameewong, SFC20170725–35 (GenBank accession no. ITS: OL467272; nrLSU: OL462811).

Diagnosis

This species notably has hemispherical to convex, 4–23 mm pileus, distant lamellae, central to eccentric, tomentose, 5–15 × 0.5‒1.5 mm stipe with a white base; ellipsoid to ovoid, 5.8–7.4 × 2.8–4 μm basidiospores, clavate (often constricted), 25.5–34.8 × 4.8–6.7 μm basidia, broadly clavate, irregular, sometimes lobed, 26–49 × 5.4–10.6 μm cheilocystidia, and a habit of fruiting on branches.

Description

Pileus: 4‒23 mm, eccentric, convex to hemispherical when young, becoming depressed and undulating with age; Surface smooth, brownish orange (5C3 to 6D4) at the center, becoming paler to the margin (4A3 to 3A2). Lamellae: distant, L = 10–16, l = 3–7, adnate, whitish to yellowish white (3A2). Stipe: 5–15 × 0.5‒1.5 mm, central to eccentric, cylindrical, tomentose, apex brownish orange (5C3) to light brown (6D4), gradually becoming paler downwards (5B2 to 6C2), with whitish basal tomentum. Basidiospores: 5.8–7.4 × 2.8–4 μm (average 5.5 × 3.2 μm), Q = 1.6–2.1 (mean = 1.97), ellipsoid to ovoid, amygdaliform, smooth, hyaline, non-dextrinoid, with drops. Basidia: (23) 25.5–34.8 × 4.8–6.7 (7) μm, 4-spored, clavate, often constricted. Cheilocystidia: 26–49 × 5.4–10.6 (14) μm, broadly clavate, irregular, sometimes lobed. Pleurocystidia: 25.8–56.4 (62) × 6.2–12.5 μm, clavate, subulate, sometimes lobed. Trama hyphae: cylindrical, often sub-inflated, smooth, non-dextrinoid 1.7–9 (12) μm wide. Pileipellis: a cutis made up of cylindrical, often sub-inflated, with weak annular ornamentation, 2.0‒7.5 μm wide hyphae; terminal elements adpressed, cylindrical, clavate, sometimes constricted or curved, 2.0‒5 μm wide. Stipitipellis: a cutis of cylindrical, smooth, 2.7‒9.7 (11) μm wide hyphae. Caulocystidia: 21.7–90 × 3.9–11.7 μm, cylindrical, flexuose, sometimes curved. Clamp connections: present in all tissues.

Other specimens examined

The Republic of Korea, Jeollanam-do: Jindo-gun, Maenggoldo island, 34°12'21"N, 125°51'41"E, alt. 24 m, 4 July 2018, Jae Young Park, SFC20180704–86.

Habit and habitat

Scattered to gregarious on the branch in mixed forest dominated by Camellia japonica Linne, in summer.

Distribution

The Republic of Korea.

Remark

Collybiopsis albicantipes is similar to Co. ramulicola and Co. koreana when comparing macro-morphological characteristics. Collybiopsis ramulicola is distinguishable from Co. albicantipes by a reddish pileus, fewer and buff lamellulae (1–4), a shorter and thinner stipe (12–23 × 2–3 mm), shorter and slightly elongated basidiospores (6.6–8.4 × 3.5–4.5 μm), shorter basidia (23–27 × 3.8–5.5 μm), and shorter cheilocystidia (23–27 × 3–6 μm) (Deng et al. 2016). Collybiopsis koreana differs from Co. albicantipes by having a larger pileus (27–60 mm), more lamellae (15–20) and lamellulae (2–3), longer and thicker stipe (14–70 × 2–3.5 μm), bigger and elongated basidiospores (7.5–10 × 4–5 μm), cheilocystidia with different shapes and sizes (25–55 × 4–10 μm), and incrustation dark brown in KOH (Antonín et al. 2010).

Collybiopsis clavicystidiata J.S. Kim & Y.W. Lim, sp. nov.

MycoBank No: 842054
Fig. 3C–D, Suppl. material 1: Fig. S1B

Etymology

Epithet “clavicystidiata” indicates that the new species has clavate cheilocystidia.

Holotype

The Republic of Korea, Jeollanam-do: Jindo-gun, Jodo-myeon, Donggeocha island, 34°23'34"N, 125°93'84"E, alt. 70 m, 05 July 2018, Jae Young Park, Tae Heon Kim, SFC20180705–84, (GenBank accession no. ITS: OL467252; nrLSU: OL462817).

Diagnosis

The prominent features of this species include a greyish orange to brownish, 6–45 mm pileus, whitish lamellae, a subinstitious, tomentose, whitish, 15–26 × 1.2‒1.6 mm stipe, oblong to subcylindrical, 6.7‒9.4 × 3.1‒4.6 μm basidiospores, utriform, clavate, 20.1–37.5 × 6.8–12.2 μm cheilocystidia, and cylindrical, flexuose, irregular, 17–50 × 3.5–7 μm caulocystidia.

Description

Pileus: 6–45 mm, convex to hemispherical, becoming plano-convex to flat with an uplifted margin with age; Surface smooth, dull, hygrophanous, greyish orange (6B3) to brownish (7D8 to E8) at the center, being whitish at the margin (4A2 to 6C8), being paler with age. Lamellae: subdistant, L = 20–32, l = 1–7, adnexed, white. Stipe: 15–26 × 1.2‒1.6 mm, cylindrical, tomentose, subinsititious, whitish to reddish grey (9B2). Basidiospores: 6.7‒9.4 × 3.1‒4.6 μm, average 8.13 × 3.62 μm, Q = 2–2.4 (mean = 2.26), oblong to cylindrical, smooth, hyaline, non-dextrinoid, with drops. Basidia: 18.3–30 × 4.1–8.8 μm, 4-spored, narrowly clavate, narrowly utriform, often curved. Cheilocystidia: 20.1–37.5 × 6.8–12.2 μm, utriform, clavate, sometimes with mucronate apex. Pleurocystidia: absent. Trama hyphae: cylindrical, often subinflated, smooth, branched, non-dextrinoid, 2‒12 μm wide. Pileipellis: transition between cutis and trichoderm, composed of cylindrical, with heavy annular ornamentation, 4‒12 μm wide hyphae; terminal elements adpressed to suberect, cylindrical, clavate, often incrusted (often incrusted), thin-walled, 3‒6 μm wide. Stipitipellis: a cutis of cylindrical, smooth, 2‒7 μm wide hyphae. Caulocystidia: 17–50 × 3.5–7 μm, cylindrical, flexuose, irregular or curved. Clamp connections: present in all tissues.

Other specimens examined

The Republic of Korea, Jeollanam-do: Haenam-gun, Mt. Duryun, 34°29'6"N, 126°38'54"E, alt. 169 m, 5 July 2018, Young Woon Lim, Abel Severin Lupala, Jun Won Lee, SFC20180705–26. The Republic of Korea, Seoul: Gwanak-gu, Gwanak-ro 1, Seoul National University, 37° 27' 37"N, 126° 56' 59"E, alt. 80m, 13 July 2018, Jae Young Park, SFC20180713–09.

Habit and habitat

Solitary to scattered on dead wood debris of conifers, in summer.

Distribution

The Republic of Korea

Remark

Collybiopsis clavicystidiata is morphologically similar to G. omphalodes and Co. menehune. Collybiopsis omphalodes differs in their larger pileus (2–30 mm), a darker colored stipe, smaller basidiospores (5–6 × 2.5–3 μm), and thinner hyphae in the pileipellis (5–8 μm wide). Collybiopsis menehune can be distinguished from Co. clavicystidiata by its larger pileus (8–30 mm), buff lamellae, longer stipe (15–60 mm), longer basidiospores (7.5–9.5 × 3.5–4.2 μm, Q = 2.2), and longer caulocystidia (16–67 × 3–5 μm) (Desjardin et al. 1999). Co. clavicystidiata is phylogenetically close to Co. pseudomphalodes. Collybiopsis pseudomphalodes has relatively few references for comparison, but differences can be found in the lengths of the stipe (3–4 mm) and cheilocystidia (40 × 3 μm) when compared with Co. clavicystidiata (Dennis 1961).

Collybiopsis fulva J.S. Kim & Y.W. Lim, sp. nov.

MycoBank No: 842055
Fig. 3E–F, Suppl. material 1: Fig. S1C

Diagnosis

This species has a pale orange to brownish-colored, 4–20 mm pileus, an orange white colored to light brownish colored, 7–30 × 0.7–1 mm stipe with pubescence, spheropedunculate, pleurocystidia, oblong to subcylindrical, 6.8–9.2 × 3.1–4.9 μm basidiospore, lobed, clavate with rostrate apex, 24.8–38.4 × 6.5–11.8 μm cheilocystidia.

Etymology

Epithet “fulva” referring to fox-colored pileus.

Holotype

The Republic of Korea, Gyeonggi-do: Pocheon-si, Soheul-eup, Gwangneungsumogwon-ro 415, 37°45'17"N, 127°9'59"E, alt. 101 m, Sang Kook Han, 21 July 2015, KA15–0210 (GenBank accession no. ITS: OL467259; nrLSU: OL462795).

Description

Pileus: 4–20mm, hemispherical, convex to plane, sometimes concave with slightly reflexed, wavy margin, hygrophanous, pale orange (6A3) to greyish orange, becoming more brownish to the center (5B4 to 7C4). Lamellae: distant, L = 16–28, l = 1–5, sinuate, broad, whitish to yellowish white (4A2) to brownish orange (6C4 to 7C4). Stipe: 7–30 × 0.7–1 mm, cylindrical, gradually widened towards the base, tomentose, apex orange white (5A2) to brownish orange (6C6), becoming dense downwards (6D8), covered with pubescence. Basidiospores: 6.8–9.2 × 3.1–4.9 μm (average 7.47 × 3.69 μm), Q = 2.05, oblong to cylindrical, smooth, colorless, non-dextrinoid, with drops. Basidia: 20.4–29.4 × 4.7–7.8 μm, 4-spored, narrowly clavate, sometimes constricted or curved. Cheilocystidia: (20.5) 24.8–38.4 × 6.5–11.8 μm, lobed, clavate, sometimes with rostrate apex. Pleurocystidia: 31.5–46.9 × 12–20.6 μm, spheropedunculate, obovoid, sometimes with mucronate apex. Trama hyphae: cylindrical to subinflated, irregular, thin-walled, smooth, branched, non-dextrinoid, 2.0‒15 μm wide. Pileipellis: a cutis of cylindrical, thin-walled, 4–15 μm wide hyphae; terminal elements adpressed to suberect, narrowly clavate, thin-walled, with heavy annular ornamentation, 3–8 μm wide. Stipitipellis: a cutis of cylindrical, thin-walled, smooth, 5‒15 μm wide hyphae. Caulocystidia: 45.6–108.3 (131) × 6.8–14.8 μm, cylindrical, irregular, curved. Clamp connections: present in all tissues.

Other specimens examined

The Republic of Korea, Gyeonggi-do: Pocheon-si, Soheul-eup, Gwangneung forest exhibition hall, 37°45'19"N, 127°9'58"E, alt. 99 m, 8 July 2016, Sang Kook Han, KA16–0428. The Republic of Korea, Gyeongsangnam-do: Geochang-gun, Mt. Gibaek, 35°43'6"N, 127°45'49"E, alt. 1095 m, 19 June 2013, Sang Kook Han, KA13–0216.

Habit and habitat

Scattered or gregarious on the bark of deciduous trees or on the rotting branch of both broadleaf trees and conifers, in summer.

Distribution

The Republic of Korea.

Remark

Collybiopsis fulva morphologically resembles Co. menehune and Co. ramealis. They can be distinguished based on several morphological differences. Collybiopsis menehune has a longer stipe (15–60 mm length), denser lamellae, and larger basidiospores (7.5–9.5 × 3.5–4.2 μm) (Desjardin et al. 1999). Collybiopsis ramealis has a smaller basidiocarp (2–20 mm), shorter basidiospores (7.8–11 × 2.5–4 mm) and different type of pileipellis (Rameales-structure) (Noordeloos 1983; Desjardin et al. 1997). Phylogenetically, Co. fulva is closely related to Co. ramulicola. Collybiopsis ramulicola differs in having a more yellowish pileus, fewer lamellae (9–12) that are brighter in color, a more reddish and thicker stipe (2–3 mm), and smaller sized cheilocystidia (23–27 × 3–6 mm) (Deng et al. 2016).

Collybiopsis orientisubnuda J.S. Kim & Y.W. Lim, sp. nov.

MycoBank No: 842056
Fig. 3G–H, Suppl. material 1: Fig. S1D

Etymology

Epithet “orientisubnuda” meaning the new species has originated from the East and is morphologically similar to Co. subnuda.

Holotype

The Republic of Korea, Gyeongsangbuk-do: Ulleung-gun, 37°31'21"N, 130°53'14"E, alt. 757 m, 19 July 2016, Changmu Kim, Jinsung Lee, Jae Young Park, NIBRFG0000500990 (GenBank accession no. ITS: OL467262; nrLSU: OL546546).

Diagnosis

It features a brownish, 15‒50 mm pileus, orangish cream-colored lamellae, greyish to brownish orange, tomentose, 20–80 × 2.5‒6 mm stipe, subcylindrical to fusoid, 6.7–8.6 × 1.8–3.2 μm basidiospores, and cylindrical, flexuose, sometimes irregular or curved, 26.3–52 (63) × 3.5–6.5 μm caulocystidia. This species is morphologically similar to Co. subnuda.

Description

Pileus: 15‒50 mm, convex to plano-convex, sometimes subumbonate; Surface smooth, brownish orange (6C5 to 7C4), becoming paler to the margin (5A2). Lamellae: distant, L = 16–28, l = 3–7, adnexed, pale yellow (4A3) to orange white (5A2). Stipe: 20–80 (100) × 2.5‒6 mm, central to eccentric, cylindrical, tomentose, often twisted, greyish orange (6B4) to brownish orange(7C4), becoming paler and thinner to the base. Basidiospores: 6.7–8.6 × 1.8–3.2 μm (average 7.5 × 2.5 μm), Q = 2.5–3.2 (mean = 2.92), cylindrical to fusoid, smooth, hyaline, non-dextrinoid, with drops. Basidia: (17) 19.8–28.7 (29) × 3.7–7.3 μm, 4-spored, narrowly clavate, often constricted. Cheilocystidia: variable in shape and size, 21–33.3 × 4.7–8.2 μm, lobed, clavate, slightly sphaeropendunculate, sometimes constricted or with rostrate apex. Pleurocystidia: 24.7–52.3 × 5.1–9.1 μm, narrowly utriform, clavate, sometimes clavate with rostrate apex. Trama hyphae: cylindrical, often subinflated, smooth, branched, non-dextrinoid, 2.0–7.0 μm wide. Pileipellis: a cutis made up of cylindrical, 2‒8 μm wide hyphae; terminal elements adpressed, cylindrical, often subinflated, with weak annular ornamentation, 3‒6 μm wide. Stipitipellis: a cutis of cylindrical, smooth, 2.5–7 μm wide hyphae. Caulocystidia: 26.3–52 (63) × 3.5–6.5 μm, cylindrical, flexuose, sometimes irregular or curved. Clamp connections: present in all tissues.

Other specimens examined

The Republic of Korea, Chungcheongnam-do: Yesan-gun, Mt. Gaya, 35°48'14"N, 128°5'49”E, alt. 863 m, 23 August 2017, Hae Jin Cho, Ki Hyeong Park, SFC20170823–39. The Republic of Korea, Gangwon-do: Pyeongchang-gun, Mt. Odae, 37°43'54"N, 128°35'42"E, alt. 683 m, 8 July 2017, Nam Kyu Kim, SFC20170708–14. The Republic of Korea, Gyeongsangbuk-do: Ulleung-gun, 37°31'30"N, 130°52'21"E, alt. 718 m, 2 September 2015, Jae Young Park, SFC20150902-01.

Habit and habitat

Scattered to gregarious on the ground covered with dead and decaying leaves of broadleaf forest, from summer to autumn.

Distribution

The Republic of Korea.

Remark

Collybiopsis orientisubnuda is morphologically similar to Co. peronata (Bolton) R.H. Petersen and Co. subnuda (Ellis ex Peck) R.H. Petersen. Collybiopsis peronata can be distinguished from Co. orientisubnuda by fewer and buff lamellulae (1–3), a thicker stipe (3–8 mm), smaller Q value (2.3), longer basidia (20–40 μm), and longer cheilocystidia (25–90 × 5–10 μm) (Noordeloos et al. 1999). Collybiopsis subnuda differs from Co. orientisubnuda with thinner stipe (~3 mm), larger basidiospores (8–11 × 3–4.5 μm) and the absence of pleurocystidia (Tekpınar and Acar 2020).

Collybiopsis subumbilicata J.S. Kim & Y.W. Lim, sp. nov.

MycoBank No: 842057
Fig. 4A, B, Suppl. material 1: Fig. S1E

Etymology

Epithet “subumbilicata” referring to having a small depressed center in pileus.

Holotype

The Republic of Korea, Seoul, Gwanak-gu, Mt. Gwanak, 37°12'39"N, 128°19"E, alt. 877 m, 01 July 2014, Young Woon Lim, SFC20140701–03 (GenBank accession no. ITS: OL467232; nrLSU: OL462787).

Diagnosis

The distinctive features include a brownish, 10–35 mm pileus, white colored lamellae, a brownish, 25–60 × 1‒3 mm stipe covered with pubescence, ellipsoid to oblong basidiospores, narrowly clavate and cylindrical, 17–24.3 × 3.5–5.1 μm basidia, and cylindrical, flexuose, sometimes curved, 12.6–38.2 × 2.4–6.6 μm caulocystidia.

Description

Pileus: 10–35 mm, plano-convex to plano-concave, subumbilicate, becoming undulate and uplifted in age; Surface smooth, greyish orange (5B3) to brown (6E5). Lamellae: subdistant, L = 22–38, l = 3–7, free to adnexed, white. Stipe: 25–60 × 1‒3 mm, cylindrical, tomentose, hollow, light brown (7D4) to dark brown (9F8), becoming paler to the apex, covered with pubescence. Basidiospores: 5.5‒7.5 × 2.5‒3.6 μm (average 6.47 × 3.0 μm), Q = 1.8–2.2 (mean = 2), oblong to fusiform, smooth, hyaline, non-dextrinoid, with drops. Basidia: (15.6) 17–24.3 (27.6) × 3.5–5.1 (5.9) μm, 4-spored, narrowly clavate, cylindrical. Cheilocystidia: 17.6–38.4 × 5–7.8 μm, various in shape, lobed. Pleurocystidia: 20.3‒30.7 × 6.8‒9.5 μm, clavate, fusiform, slightly sphaeropedunculate. Trama hyphae: cylindrical, subinflated, branched, smooth, non-dextrinoid, 1.5‒8 μm wide. Pileipellis: a cutis made up of cylindrical, often incrusted, with heavy annular ornamentation, 5.0‒15 μm wide hyphae; terminal elements adpressed to suberect, fusoid, clavate, 6.0‒16 μm wide. Stipitipellis: a cutis of cylindrical, smooth, thin-walled, 2.0‒6.0 μm wide hyphae. Caulocystidia: 12.6–38.2 × 2.4–6.6 μm, cylindrical, flexuose, sometimes irregular or curved. Clamp connections: present in all tissues.

Other specimens examined

The Republic of Korea, Gangwon-do: Goseong-gun, Hwajinpo, Hwajinpo Condominium, 38°28'24"N, 128°26'30"E, alt. 7 m, 2 August 2012, Young Woon Lim, SFC20120802–03. The Republic of Korea, Gyeongsangbuk-do: Ulleung-gun, Ulleung island, 37°30'38"N, 130°51'44"E, alt. 429 m, 22 August 2017, Jae Young Park, Nam Kyu Kim, SFC20170822–14.

Habit and habitat

Scattered to gregarious on the ground covered with dead leaves in temperate mixed forests, from summer to autumn.

Distribution

The Republic of Korea.

Remark

Collybiopsis subumbilicata appears similar to Co. villosipes (Cleland) R.H. Petersen. Collybiopsis villosipes is distinguished from Co. subumbilicata by fewer and brownish lamellae (also lamellulae), a noninsititious, light-colored stipe, larger basidiospores (6.5‒10.5 × 3.5‒4.5 μm) and basidia (25‒34 × 6.5‒7.5 μm) (Desjardin et al. 1997). Furthermore, Co. subumbilicata is phylogenetically close to Co. biformis and Co. disjuncta (R.H. Petersen & K.W. Hughes) R.H. Petersen & K.W. Hughes. Collybiopsis biformis is morphologically similar to Co. subumbilicata but can be distinguished by elongated basidiospores (6.4‒9.2 × 2.4‒4.8 μm), thicker basidia (6‒7 μm thick) and cheilocystidia (6‒12 μm thick) (Morgan 1905; Mata 2002). Collybiopsis disjuncta can be distinguished from Co. subumbilicata by a smaller pileus (7–12 mm) with olivaceous tint, pinkish lamellae, slender stipe (0.5–1 mm thick), bigger basidiospores (6–7.5 × 3–3.5 μm), bigger basidia (22–34 × 5–7 μm), and a seldom incrusted pileipellis (Petersen and Hughes 2014).

Collybiopsis undulata J.S. Kim & Y.W. Lim, sp. nov.

MycoBank No: 842058
Fig. 4C–D, Suppl. material 1: Fig. S1F

Etymology

Epithet “undulata” referring to having an undulate margin of pileus.

Holotype

The Republic of Korea, Chungcheongnam-do, Boryeong-si, recreation forest of Mt Sungju, 36°20'4"N, 126°39'50"E, alt. 241 m, 21 August 2012, Jae Young Park, SFC20120821–04 (GenBank accession no. ITS: OL467239; nrLSU: OL462813).

Diagnosis

It is characterized by having 10‒23 mm sized pileus that is particularly brown in the middle with a wavy margin, subdistant and creamy lamellae, a dark brown, 35–55 × 0.8‒2 mm stipe that becomes lighter to the apex, subcylindrical, broadly clavate or irregular, sometimes lobed, 16.7–28 × 4.8–8 μm cheilocystidia, and 27–60 × 3.5–6 μm sized caulocysitida which has a morphology similar to cheilocystidia and sometimes grows in bundles.

Description

Pileus: 10‒23 mm, convex to concave, margin becoming undulate with age; Surface smooth, hygrophanous, brown (7D2 to 7E6) in the center, becoming paler to the margin (5A2–5B3 to 7B2). Lamellae: subdistant, L = 15–30, l = 3–9, adnexed, cream. Stipe: 35–55 × 0.8‒2 mm, cylindrical, tomentose, dark brown (7F5 to 8F8), gradually becoming paler to apex (7B2 to 7C2). Basidiospores: 5.6–9.5 × 2–3.4 μm (average 7.3 × 2.8 μm), Q = 2–3.1 (mean = 2.58), cylindrical, smooth, hyaline, non-dextrinoid, with drops. Basidia: 15–22.3 × 3.6–6.8 μm, 4-spored, cylindrical, narrowly clavate to utriform, often curved. Cheilocystidia: 16.7–28 × 4.8–8 μm, subcylindrical, broadly clavate or irregular, sometimes lobed. Pleurocystidia: absent. Trama hyphae: cylindrical, sometimes subinflated, smooth, branched, non-dextrinoid, 2–8 μm wide. Pileipellis: a cutis made up of cylindrical, often incrusted, slightly brownish, with heavy annular ornamentation, 2.4–7 μm wide hyphae; terminal elements adpressed to suberect, cylindrical to clavate, 3–6 μm wide. Stipitipellis: a cutis of cylindrical, smooth, 2.0‒3.5 μm wide hyphae. Caulocystidia: 27–60 × 3.5–6 μm, irregularly cylindrical, narrowly utriform, seldom apically lobed, sometimes gathered in a bunch. Clamp connections: present in all tissues.

Other specimens examined

The Republic of Korea, Gyeonggi-do: Goyang-si, Deogyang-gu, Seooreung, 37°37'26"N, 126°54'4"E, alt. 35 m, 13 August 2015, Jae Young Park, SFC20150813–04. The Republic of Korea, Gyeongsangbuk-do, Sangju-si, Mt Noheum, 36°26'20"N, 128°5'48"E, alt. 695 m, 8 August 2013, Jae Young Park, SFC20130808–08.

Habit and habitat

Scattered to gregarious on leaf litter in mixed forest dominated with broadleaf trees, in summer.

Distribution

The Republic of Korea.

Remark

Collybiopsis undulata is morphologically similar to Co. subpruinosa (Murrill) R.H. Petersen. Collybiopsis subpruinosa has differences in having small central papilla on pileus, fewer lamellulae (3–4 series), vivid colored lamellae, thicker basidiospores (4.5–5.2 μm wide), larger basidia (30–36 × 7.5–8.5 μm) and cheilocystidia (25–80 × 5–16 μm), thick-walled trama hyphae (0.5–1 μm), caulocystidia with a wider size range, and a habit of growing solitary on rotten twigs or logs (Desjardin et al. 1999). Collybiopsis undulata is phylogenetically close to Co. villosipes but Co. villosipes can be differentiated by having fewer lamelluale (2–3 series), vivid colored lamellae, thicker stipe (1.5–4.0 mm), slightly thicker basidiospores (3.5–4.5 μm wide), and basidia (25–34 × 6.5–7.5 μm) (Desjardin et al. 1997).

Collybiopsis vellerea J.S. Kim & Y.W. Lim, sp. nov.

MycoBank No: 842059
Fig. 4E–F, Suppl. material 1: Fig. S1G

Etymology

Epithet “vellerea” refers to having a velvety stipe.

Holotype

The Republic of Korea, Seoul: Gwanak-gu, Mt. Gwanak, 37°27'32"N, 126°56'49"E, alt. 90 m, 21 August 2014, Young Woon Lim, SFC20140821–29 (GenBank accession no. ITS: OL467267; nrLSU: OL462810).

Diagnosis

It has a dull, greyish orange, 18‒45 mm pileus with darker center, a tomentose (like velvet), insititious, orangish, 15–55 × 3‒5 mm stipe, sphaeropendunculate, subovoid, 23.4–49 × 7.5–13.4 μm pleurocystidia, oblong to subcylindrical basidiospores, narrowly clavate with rostrate apex, sometimes lobed, 7.7–49.7 × 3.8–14.6 μm cheilocystidia.

Description

Pileus: 18‒45 mm, hemispherical, appendiculate to convex, subumbonate with an uplifted margin when old; Surface smooth, dull, hygrophanous, orange white (5A2) to greyish orange (6E8 to 7F8) on the center, gradually becoming paler to the edge (5A1 to 5B2). Lamellae: crowded to close, L = 38‒52, l = 3‒7, furcate, white. Stipe: 15–55 × 3‒5 mm, cylindrical, finely tomentose, insititious, pale orange (5A3) to reddish grey (7B2), becoming darker to the base (6A2 to 7C2). Basidiospores: 5.2‒7 × 2.5‒3.8 μm (average 6.17 × 3.06 μm), Q = 1.8–2.4 (mean = 2.03), oblong to subcylindrical, smooth, hyaline, non-dextrinoid, with drops. Basidia: 16.2–24.8 × 3.3–5.3 μm, 4-spored, (narrowly) clavate, often curved or constricted. Cheilocystidia: 7.7–49.7 × 3.8–14.6 μm, narrowly clavate with rostrate apex, sometimes lobed. Pleurocystidia: 23.4–49 × 7.5–13.4 μm, sphaeropendunculate, subovoid. Trama hyphae: cylindrical, often subinflated, thin-walled, smooth, branched, non-dextrinoid, 2‒5 μm wide. Pileipellis: a cutis made up of cylindrical, thin-walled, with weak annular ornamentation, 3‒10 μm wide hyphae; terminal elements adpressed to suberect, cylindrical, fusoid, clavate, 5‒11 μm wide. Stipitipellis: a cutis of cylindrical, thin-walled, smooth, 2.0‒6.0 μm wide hyphae. Caulocystidia: 12–38 × 2.4–6.6 μm, cylindrical, narrowly utriform, sometimes irregular, or curved. Clamp connections: present in all tissues.

Other specimens examined

The Republic of Korea, Chungcheongnam-do: Seosan-si, Mt. Gaya, 36°41'0"N, 126°35'19"E, alt. 260 m, 20 August 2012, Jae Young Park, SFC20120820–02. The Republic of Korea, Incheon: Ongjin-gun, 37°13'10"N, 126°10'4"E, alt. 6 m, 4 September 2018, Changmu Kim, Jin Sung Lee, NIBRFG0000502858. The Republic of Korea, Jeollanam-do: Jindo-gun, Seogeocha island, 34°15'22"N, 125°55'11"E, alt. 38 m, 5 July 2018, Jae Young Park, Tae Heon Kim, SFC20180705–90.

Habit and habitat

Scattered to gregarious on the ground covered with dead and decaying conifer needles, from summer to autumn.

Distribution

The Republic of Korea.

Remark

Collybiopsis vellerea is morphologically similar to Co. menehune and G. spongiosus Halling. Collybiopsis menehune has a paler stipe, a smaller pileus (8–30 mm), and fewer lamellulae (4–6 series) (Desjardin et al. 1999). Gymnopus spongiosus has a smaller pileus (8–20 mm) and longer stipe (20–55 mm). Micromorphologically, Co. menehune has larger basidiospores, basidia, and caulocystidia (Desjardin et al. 1999). Gymnopus spongiosus differs from Co. vellerea in that its pileipellis is a Dryophila-type cutis and its color changes in alkalies. Furthermore, its basidia (18–25 × 6–9 μm) and trama hyphae (3.5–17 μm) are thicker and its caulocystidia (3.5–10.5 μm broad) are smaller (Halling 1996). Collybiopsis vellerea is phylogenetically close to Co. omphalodes. Collybiopsis omphalodes differs in having smaller basidiomata (20–30 mm) and its habit on logs (Dennis 1951).

Proposal for Collybiopsis recombination

In this study, many epithets were found that required an additional transfer of species from Marasmiellus to Collybiopsis apart from the study done by Petersen and Hughes (2021). Oliveira et al. (2019) had previously suggested to replace these species from Gymnopus to Marasmiellus s. str., but this study suggests that these species should be further transferred from Marasmiellus s. str. to Collybiopsis.

Collybiopsis istanbulensis (E.Sesli, Antonín & E.Aytaç) J.S. Kim & Y.W. Lim, comb. nov.

MycoBank No: 842060

Basionym

Marasmiellus istanbulensis E. Sesli, Antonín & E.Aytaç. Pl. Biosystems 152(4): 669. 2018.

Collybiopsis koreana (Antonín, Ryoo & H.D.Shin) J.S. Kim & Y.W. Lim, comb. nov.

MycoBank No: 842061

Basionym

Marasmiellus koreanus Antonín, Ryoo and H.D.Shin. Mycotaxon 112: 190. 2010.

Collybiopsis omphalodes (Berk.) J.S. Kim & Y.W. Lim, comb. nov.

MycoBank No: 842062

Chamaeceras omphalodes (Berk.) Kuntze, Revis. gen. pl. (Leipzig) 3(3): 456. 1898.

Collybia omphalodes (Berk.) Dennis, Trans. Br. mycol. Soc. 34(4): 443. 1951.

Marasmiellus omphalodes (Berk.) Singer. Sydowia 9(1–6): 385. 1955.

Gymnopus omphalodes (Berk.) Halling & J.L. Mata, in Mata, Halling, and Petersen, Fungal Diversity 16: 122. 2004.

Basionym

Marasmius omphalodes Berk., Hooker’s J. Bot. Kew Gard. Misc. 8: 138. 1856.

Collybiopsis pseudomphalodes (Dennis) J.S. Kim & Y.W. Lim, comb. nov.

MycoBank No: 842063

Gymnopus pseudomphalodes (Dennis) J.L. Mata, in Mata, Hughes, and Petersen, Sydowia 58(2): 289. 2006, as “pseudo-omphalodes”.

Marasmiellus pseudomphalodes (Dennis) J.S. Oliveira, in Oliveira, Vargas-Isla, Cabral, Rodrigues and Ishikawa, Mycol. Progr. 18(5): 735. 2019, as “pseudomphalioides”.

Basionym

Collybia pseudomphalodes Dennis, Kew Bull. 15(1): 74 (1961).

Collybiopsis ramulicola (T.H. Li & S.F. Deng) J.S. Kim & Y.W. Lim, comb. nov.

MycoBank No: 842064

Basionym

Gymnopus ramulicola T.H. Li & S.F. Deng, in Deng, Li, Jiang and Song, Mycotaxon 131(3): 665. 2016.

Taxonomic key to Collybiopsis in Korea

1 Pileus < 25 mm diam 2
Pileus > 25 mm diam 11
2 Lamellae subdistant to distant (10–30) 3
Lamellae close to crowded (> 30) 9
3 Basidiomes on bark, branch, or woody debris 4
Basidiomes on duff or on soil 8
4 Pleurocystidia present 5
Pleurocystidia absent 7
5 Stipe base covered with dense whitish basal tomentum Co. albicantipes
Stipe base not covered with whitish basal tomentum 6
6 Pileipellis composed of a coarse Rameales-structure hyphae Co. ramealis
Pileipellis composed of a cylindrical, often sub-inflated hyphae, not a Rameales-structure Co. fulva
7 Pileus distinctly sulcate. Stipe base covered with dense whitish basal tomentum Co. koreana
Pileus slightly sulcate. Stipe base covered with weak whitish basal tomentum Co. nonulla
8 Stipe < 2 cm long. Q value of basidiospores 1.6–2.2 Co. dichroa
Stipe > 2 cm long. Q value of basidiospores 2.0–3.1 Co. undulata
9 Lamellae crowded (> 100) Co. confluens
Lamellae close to crowded (< 100) 10
10 Basidia > 22 µm long Co. menehune
Basidia < 22 µm long Co. biformis
11 Lamellae subdistant to distant (10–38) 12
Lamellae close (> 38) 15
12 Pleurocystidia present 13
Pleurocystidia absent 14
13 Q value of basidiospores > 2.2 Co. orientisubnuda
Q value of basidiospores < 2.2 Co. subumbilicata
14 Pileus convex, hemispherical, plano-convex to flat. Cheilocystidia utriform and clavate Co. clavicystidiata
Pileus convex to broad-convex. Cheilocystidia narrowly clavate Co. polygramma
15 Pleurocystidia present Co. vellerea
Pleurocystidia absent Co. luxurians

Discussion

Of the 372 gymnopoid/marasmioid specimens, we confirmed 201 specimens (54%) to belong to Collybiopsis. These results indicate that the species of Collybiopsis can be confused with those of similar genera as well as with other Collybiopsis members when identification is based solely on morphological information. This is because some characteristics are overlapped between species (Suppl. material 2: Fig. S2) and the characteristics can be different depending on developmental stage or environmental conditions. Further, the high misidentification ratio may be caused by the slow rate of adoption of the current names. Sequence-based taxonomy has introduced rapid changes in the classification of gymnopoid/marasmioid species (Mata 2002; Mata et al. 2004a; Mata et al. 2004c; Hughes et al. 2010; Oliveira et al. 2019; Petersen and Hughes 2017, 2021). As such, taxonomic confusion has been resolved in taxa that have been well researched based on molecular data (Desjardin et al. 1999; Mata 2002; Lee et al. 2019).

Nine of the sixteen Collybiopsis species were identified as already known species. Of the nine described species, seven species were identified as the species previously recorded in the Republic of Korea: Collybiopsis biformis, Co. confluens, Co. koreana, Co. luxurians, Co. menehune, Co. polygramma, and Co. ramealis. Two species, Co. dichroa and Co. nonnulla, were reported for the first time in the Republic of Korea. Most of the nine described species formed a monophyletic clade with each corresponding species. However, sequence variations by continent were detected in Co. biformis, Co. confluens, Co. dichroa, and Co. nonnulla. Asian samples, including our specimens, were clearly separated from those of Europe, North America, and Africa. These results have also been reported in previous studies on Collybiopsis biformis (Mata 2002; Petersen and Hughes 2014; Razaq et al. 2020) and Co. confluens (Hughes and Petersen 2015). Especially, Co. confluens is known as a representative example of intra-specific variation between continents. Percent ITS sequence divergence of this species was reported to be 3.25% when comparing the sequences of the North America and Europe (Hughes and Petersen 2015). We confirmed that percent ITS sequence divergence of Asian Co. confluens (our Korean samples and Chinese sequences) were each about 3% when compared to American and European sequences.

Similarly, Co. dichroa showed sequence variations that were previously reported in association with intraspecific hybridization and dramatic sequence variations including frequent nucleotide substitutions of Adenine and Guanine (Hughes et al. 2015). The Korean Co. dichroa was closely related to Co. dichroa taxa 2 mentioned in Hughes et al. 2015. Similarly, the intraspecific genetic variation depending on environmental conditions or geographical distribution has been reported in many other fungal species (Manian et al. 2001; Kauserud et al. 2007; Seierstad et al. 2013). For the last, Korean Co. nonnulla showed high intra-specific divergence when matching with sequences of Co. nonnulla of America and Cameroon. According to the phylogenetic analysis results, there is a slight sequence variation, but it forms a clade supported by a high bootstrap and morphologically almost coincides with the reference. Therefore, we view this sequence variation as due to different environments by continent and identify the specimens as Co. nonnulla. Nevertheless, compared to the fact that it was reported as a new species a long time ago, only seven sequences were deposited in the NCBI, so further study on this species is necessary.

Morphologically, the morphological characteristics of the seven described species were also in agreement with the previous descriptions (Suppl. material 2: Fig. S2). However, Co. luxurians and Co. polygramma found in the Republic of Korea showed few differences compared to the Western descriptions in the previous literature (Mata 2003; Noordeloos et al. 1999). In the case of the Co. luxurians, Korean sequences formed a slightly distinct clade in the phylogenetic tree, along with the Chinese sequence (ZD16102301), from European sequences. In this study, direct morphological comparison studies with European and Chinese samples were difficult and there was no significant morphological difference from the references. For these reasons, we identified Korean specimens as Co. luxurians, but further studies are needed with more samples from other countries for this species.

Seven new species have common characteristics of Collybiopsis such as insititious to subinsititious stipe, ellipsoid to oblong, inamyloid basidiospores, and presence of caulocystidia. However, it is difficult to distinguish them from other Collybiopsis species based on morphological characteristics alone. Upon molecular phylogenetic analyses, each of them clearly formed a distinct clade clearly in the ML phylogenetic tree (Fig. 1). Their morphological features may or may not be distinguished from their phylogenetically close relatives. The morphological differences between new species and morphologically similar or phylogenetically close species are discussed in the remarks for each species.

Two species previously reported in the Republic of Korea, Co. peronata (Cho & Lee, 1979) and Co. subnuda (National list of species of Korea 2020), were not confirmed in this study. Co. peronata and Co. subnuda, which are typical collybioid mushrooms, have been reported in Asia based on their morphological characteristics (Cho and Lee 1979; Kim et al. 1991; Park and Cho 1992; Yoshida and Muramatsu 1998; Tolgor and Yu 2000). Molecular analyses showed that none of the Korean specimens examined in this study could be identified as Co. peronata nor Co. subnuda. Instead, the specimens labelled as Co. peronata or Co. subnuda were identified as different species – Gymnopus similis Antonín, Ryoo & Ka and Co. orientisubnuda. Collybiopsis peronata were originally mostly reported from Europe and America and Co. subnuda were originally reported from America (Desjardin et al. 1999; Mata et al. 2006). Furthermore, there have been no recent sequence uploads to GenBank or reports of Co. peronata and Co. subnuda from Asia, making it difficult to confirm whether they exist in the Republic of Korea. Although Co. orientisubnuda is closely related to Co. peronata and Co. subnuda, there are clear differences in the ITS regions of these three species (Suppl. material 3: Fig. S3). Morphologically, Co. orientisubnuda is highly similar to Co. subnuda and considerably different from Co. peronata. The detailed comparisons of the morphological features are provided in the remarks for each species.

In conclusion, we identified 16 Collybiopsis species in the Republic of Korea through morphological and molecular analyses and we update the Korean inventory of Collybiopsis. Our study showed that the identification of Collybiopsis species requires both morphological and molecular analyses. Further, this study has the following significance as in the previous study conducted by Petersen and Hughes (2021): additional combinations of Marasmiellus species under Collybiopsis, detailed morphological characterization of Collybiopsis species in the Republic of Korea along with photographs and drawings, and specific approaches to species differentiation and identification through morphological and molecular analyses. Furthermore, we believe that this study will be helpful for further studies such as research of Collybiopsis distribution worldwide as it provides additional molecular information about Collybiopsis in the Republic of Korea and proposes seven new species identified from the Republic of Korea. These data will be useful for the identification and taxonomic arrangement of gymnopoid/marasmioid mushrooms.

Acknowledgements

We greatly appreciate Prof. R.H. Petersen for his valuable comments on this manuscript. This study was supported by the National Institute of Biological Resources (NIBR202203112) and the Korea National Arboretum (KNA1-1-25, 19-2).

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Supplementary materials

Supplementary material 1 

Figure S1

Ji Seon Kim, Yoonhee Cho, Ki Hyeong Park, Ji Hyun Park, Minkyeong Kim, Chang Sun Kim, Young Woon Lim

Data type: Jpg file.

Explanation note: Pileipellis elements of seven new species. A Collybiopsis albicantipes B Co. clavicystidiata C Co. fulva D Co. orientisubnuda E Collybiopsis subumbilicata F Co. undulata G Co. vellerea. Scale bars: 10 µm.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (507.78 kb)
Supplementary material 2 

Figure S2

Ji Seon Kim, Yoonhee Cho, Ki Hyeong Park, Ji Hyun Park, Minkyeong Kim, Chang Sun Kim, Young Woon Lim

Data type: Jpg file.

Explanation note: Comparison of the morphological characters of 16 Korean Collybiopsis species.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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Supplementary material 3 

Figure S3

Ji Seon Kim, Yoonhee Cho, Ki Hyeong Park, Ji Hyun Park, Minkyeong Kim, Chang Sun Kim, Young Woon Lim

Data type: Jpg file.

Explanation note: Sequence difference between the three species in the ITS region.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (572.55 kb)
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