Phylogenetic Assessment of Understudied Families in Hymenochaetales (Basidiomycota, Fungi)—Reporting Uncovered Species and Reflecting the Recent Taxonomic Updates in the Republic of Korea

Phylogenetic Analyses

Three to five genetic marker sequences were newly acquired from 15 specimens. The multigenetic marker phylogenetic analysis was conducted using the concatenated alignments of 202 specimen data with 5788 bases, including gaps (Supplementary data 1): nSSU = 1087 bases; ITS = 1499 bases (ITS 1 = 821 bases, 5.8S = 160 bases, ITS2 = 518 bases); nLSU = 1412 bases; RPB2 = 1193 bases (exon 1 = 1106 bases, intron 1 = 62 bases, exon 2 = 25 bases); TEF1 = 597 bases (exon 1 = 150 bases, intron 1 = 85 bases, exon 2 = 107 bases, intron 2 = 89 bases, exon 3 = 166 bases). The BI phylogenetic tree (Fig. S1) topology conformed with the ML tree, supporting all 16 families as independent (Fig. 1).

Fig. 1figure 1figure 1

Phylogeny of Hymenochaetales. The phylogenetic tree was inferred using ML and BI methods (tree topology from ML) based on concatenated nSSU + ITS + nLSU + RPB2 + TEF1 dataset. Statistical values (ML/BI) above 75/0.75 are designated on or below each branch. Strains not indicated by any family are classified under incertae sedis. Colored boxes feature families with species present in Korea, and colored specimens indicate those from Korea

Exclusive of Hymenochaetaceae and Schizoporaceae, 18 species in eight understudied Hymenochaetales families were phylogenetically confirmed to be present in Korea (Fig. 1). Five unreported species were as follows: Rickenella indica in Rickenellaceae, Rigidoporus ginkgonis in Rigidoporaceae, Sidera tibetica in Sideraceae, Skvortzovia dabieshanensis in Skvortzoviaceae, and Tubulicrinis calothrix in Tubulicrinaceae. One species in the Rickenellaceae was phylogenetically revealed to be new to science. The new species, introduced here as Rickenella umbelliformis, was strongly supported (ML/BI support values = 99/1 in Fig. 1), even with two genetic rDNA markers (ITS and nLSU) dataset (85/0.99 in Fig. 2). The remaining 12 indigenous species in Korea were Hirschioporus abietinus, H. acontextus, H. pubescens, and Pallidohirschioporus biformis in Hirschioporaceae, Peniophorella odontiiformis, P. pubera, and P. subpraetermissa in Peniophorellaceae, Resinicium rimulosum in Resiniciaceae, Rickenella fibula in Rickenellaceae, Rigidoporus corticola and R. piceicola in Rigidoporaceae, and Skvortzovia pinicola in Skvortzoviaceae.

Fig. 2figure 2

Phylogeny of Rickenella. The phylogenetic tree was inferred using ML and BI methods (tree topology from ML) based on concatenated ITS + nLSU dataset. Statistical values (ML/BI) above 75/0.75 are designated on or below each branch. Specimens from Korea are in bold

Morphological Characters of Native Specimens

A combination of micromorphological characters of Rickenella umbelliformis sp. nov. was distinct from its closely related species, supporting its novelty. The morphology of five nationally unreported species was generally uniform with descriptions of each respective type or a widely accepted specimen. However, some differences were found in the measurements of microscopic features, such as basidiospores and basidia. Detailed comparisons are listed in the Notes sections of Taxonomy.

Taxonomy

This section includes species descriptions of one new species and five previously unreported species from Korea.

Rickenellaceae Vizzini

Rickenella Raithelh.

Rickenella indica K. P. D. Latha & Manim., Fig. 3

Fig. 3figure 3

Rickenella indica from the Republic of Korea. A Basidiomes of SFC20140626-39. B Micromorphological characters, where ‘s’ refers to basidiospores, ‘b1’ for basidia, ‘b2’ for basidioles, ‘c1’ for cheilocystidia and pleurocystidia, ‘c2’ for pileocystidia, ‘c3’ for caulocystidia, ‘h1’ for hymenial hyphae, ‘h2’ for pileipellis hyphae, and ‘h3’ for stipitipellis hyphae

MycoBank: MB 807702

Description: Basidiomes small, omphalinoid. Pileus 1.0–7.3 mm wide, downy, hygrophanous, paraboloid to convex with a shallow central depression, margin wavy, decurved with age, center reddish orange (9B8), surface yellowish orange (7A8), bleaching towards margin. Stipe 8.0–46.3 × 0.5–1.7 mm, central, cylindrical, downy, gelatinous, brownish yellow (5B7), gradually becomes lighter in color to the base, white at the base.

Basidiospores (5.6–)6.0–6.7(–7.2) × 2.8–3.4(–3.6) µm, L = 6.6 µm, W = 3.1 µm, Q = 1.8–2.2, subcylindrical, thin-walled, smooth, guttules present, cyanophilous, and neither amyloid nor dextrinoid. Basidia (15.5–)16.2–20.4(–20.6) × (4.3–)4.7–5.1 µm, thin-walled, clavate to narrowly utriform, 4-spored. Cheilocystidia and pleurocystidia indistinguishable, 38.8–53.8(–54.6) × (6.5–)7.0–12.0 µm, abundant, narrowly lageniform and obclavate, thin-walled, hyaline. Pileus trama hyphae septate, subregular, cylindrical or subfusoid, 13.3 µm wide on average, moderately thick-walled, hyaline, inamyloid. Pileocystidia 51.9–66.9 × 10.8–16.6 µm, narrowly lageniform to tibiiform, some septate, moderately thick-walled. Stipitipellis hyphae septate, moderately thick-walled, hyaline, inamyloid. Caulocystidia similar to cheilocystidia and pleurocystidia in all aspects. Clamp connections present.

Ecology/Substrate/Host: Grows on moss bed on ground.

Distribution: India, Republic of Korea

Specimens examined: Republic of Korea: Gyeonggi-do, Guri-si, Donggu-dong, Donggureung, deciduous forest, on ground moss bed of Plagiomnium acutum; 26 June 2014, Young Woon Lim (SFC20140626-39). Republic of Korea: Seoul, Seongdong-gu, Seoulsup 2-gil; 37°32′44″N 127°2′19″E, 16 m, Seoul forest park, mixed trees, on ground moss bed of Trachycystis microphylla; 02 July 2023, Shinnam Yoo (SFC20230702-01).

Notes: Rickenella indica from Korea largely resembles the holotype from India morphologically with overlapping ranges of the pileus, basidia, and pleurocystidia in size and also, ecologically, sharing the same lineage of symbiotic moss (Bryopsida). These biogeographically discrete specimens are also supported as the same species in the multigenetic marker phylogeny. However, they are different in several other morphological characters. Rickenella indica from Korea has longer and thicker stipe, more cylindrical basidiospores, and larger pileocystidia than those of the holotype with stipe 3–22 × 0.5–1 µm, basidiospores Q = 1.14–2.16, and pileocystidia similar to cheilocystidia (Latha et al., 2015).

Rickenella umbelliformis Y. Cho & Y.W. Lim, sp. nov. Fig. 4

Fig. 4figure 4

Rickenella umbelliformis sp. nov. A Basidiomes of SFC20150701-65 (holotype). B Micromorphological characters, where ‘s’ refers to basidiospores, ‘b1’ for basidia, ‘b2’ for basidioles, ‘c1’ for cheilocystidia and pleurocystidia, ‘c2’ for pileocystidia, ‘c3’ for caulocystidia, ‘h1’ for hymenial hyphae, ‘h2’ for pileipellis hyphae, and ‘h3’ for stipitipellis hyphae

MycoBank: MB 849306

Etymology: ‘umbelliformis’ refers to the umbrella shape of the mushroom in Latin.

Holotype: Republic of Korea: Jeju-do, Jeju-si, Jocheon-eup; Jeju Provincial Park entrance Gotjawal, mixed forest, on moss bed of Brachythecium populeum; 1 July 2015, Young Woon Lim (SFC20150701-65, dried specimen).

Description: Basidiomes small, omphalinoid. Pileus 5–15 mm wide, hygrophanous, downy, paraboloid to hemispherical, slightly campanulate when young, forming central depression and wavy decurved margin with age, plicate, center reddish orange (10B8), surface yellowish orange (6A8), bleaching towards margin. Lamellae 12–16, deeply decurrent, white, single lamellula present between two lamellae, edge entire. Stipe 21–42 × 1.2–1.7 mm, central, cylindrical, downy, gelatinous, yellow (4A8) when young, yellowish orange (6A8) when mature, gradually becomes lighter in color to the base, white at the base.

Basidiospores [20/3/2] (4.9–)5.3–6.1(–6.5) × 2.4–2.9(–3.2) µm, L = 5.5 µm, W = 2.8 µm, Q = 1.7–2.2, subcylindrical, thin-walled, smooth, guttules present, cyanophilous, and neither amyloid nor dextrinoid. Basidia (15.9–)16.4–20.0 × (3.3–)3.5–5.4(–5.8) µm, thin-walled, narrowly utriform, 4-spored, sterigmata up to 3.6 µm. Lamellar trama hyphae septate, subregular, cylindrical or subfusoid, moderately thick-walled, hyaline, inamyloid. Cheilocystidia and pleurocystidia indistinguishable, (21.9–)31.6–43.3(–48.0) × (6.1–)6.3–8.9(–9.6) µm, either rare or very frequent, narrowly lageniform and sub-capitate with apex of 2.3–3.6 µm in width, thin-walled, hyaline. Pileipellis hyphae septate, subregular, cylindrical or subfusoid, up to 18.8 µm in width, moderately thick-walled, hyaline, inamyloid, longer than tramal hyphae. Pileocystidia 39.0–48.0(–60.8) × (8.4–)11.4–16.1(–17.8) µm, narrowly lageniform and sub-capitate, moderately thick-walled but thinning towards the apex of 3.0–5.5 µm in width. Stipitipellis hyphae septate, moderately thick-walled, hyaline, inamyloid. Caulocystidia (45.0–)48.2–73.2(– 95.6) × (9.2–)9.5–23.6(– 25.7) µm, narrowly lageniform and sub-capitate, moderately thick-walled but thinning towards the apex of 2.7–4.1 µm in width. Clamp connections observed in lamellar trama only.

Ecology/Substrate/Host: Grows on various Bryophyta moss beds on ground.

Distribution: The Republic of Korea

Additional specimens examined: Republic of Korea: Gyeonggi-do, Guri-si, Donggu-dong, Donggureung, deciduous forest, on ground moss bed of Plagiomnium acutum; 12 May 2016, Hae Jin Cho, Seobihn Lee, Vladimir Li (SFC20160512-10). Republic of Korea: Gyeongsangbuk-do, Ulleung-gun, Ulleung-eup, deciduous forest, on ground moss bed of Trachycystis microphylla; 13 July 2016, Jae young Park, Myung Soo Park, Nam Kyu Kim (SFC20160713-77). Republic of Korea: Jeollanam-do, Wando-gun, Gunoe-myeon, Chopyeong 1-gil, Wando Arboretum, mixed forest, on ground moss bed of Trachycystis microphylla; 4 July 2018, Hae Jin Cho, Ki Hyung Park (SFC20180704-81). Republic of Korea: Seoul, Gwanak-gu, Gwanak-ro; 37°27′34″N 126°56′53″E, 87 m, on ground moss bed of Brachythecium populeum; 12 June 2023, Yoonhee Cho, Dohye Kim, Minseo Cho (SFC20230612-01).

Notes: Rickenella umbelliformis sp. nov. either had very few or abundant cystidia based on different individual fruiting bodies. Considering that juvenile specimens often had small immature cheilocystidia and pleurocystidia, the number of cystidia may be dependent on the age and the section of the fruiting body. Rickenella umbelliformis is phylogenetically closely related to R. indica. The two species differ in many morphological features, including the size of the pileus and pleurocystidia. Compared to the new species, Rickenella indica has a smaller pileus (1–7 mm) and longer pleurocystidia of 31–53 µm (Latha et al., 2015). The omphalinoid shape and the size of the fruiting body of R. umbelliformis are similar to those of a globally common Rickenella species, R. fibula (Bull.) Raithelh., but these species are well-divided by rDNA marker-based phylogenetic analyses. Micromorphological characteristics of R. fibula vary widely based on its geographical location, making it difficult to make a definite comparison.

Rigidoporaceae Jülich

Rigidoporus Murrill

Rigidoporus ginkgonis (Y.C. Dai) F. Wu, Jia J. Chen & Y.C. Dai, Fig. 5

Fig. 5figure 5

Rigidoporus ginkgonis from the Republic of Korea. A Basidiome of SFC20230630-23. B Micromorphological characters, where ‘s’ refers to basidiospores, ‘b1’ for basidia, ‘b2’ for basidioles, and ‘h’ for generative hyphae

MycoBank: MB 819205

Description: Basidiomes annual, resupinate, soft corky. Hymenophore porous, cream (4A4), fading to white to the margin; sterile margin indistinct, thinning out; pores round or angular, irregular, 4–5 per mm; dissepiments somewhat thin, entire; tubes up to 4.0 mm deep, concolorous with the pore surface.

Hyphal structure monomitic, generative hyphae thin-walled, hyaline. Basidiospores (4.0–)4.2–5.9 × 3.4–4.4(– 4.6) μm, L = 5.0 μm, W = 4.0 μm, Q = 1.1–1.4, globose to subglobose, thin-walled, hyaline, smooth, acyanophilous, and neither amyloid nor dextrinoid. Basidia 10.5–13.0(– 15.0) × 4.7–6.1 μm, broadly clavate to barrel-shaped, hyaline, 4-spored. Cystidia absent. Clamp connections absent.

Ecology/Substrate/Host: Grows on the trunk of living or dead Ginkgo biloba.

Distribution: China, Republic of Korea, and Uzbekistan

Specimen examined: Republic of Korea: Gangwon-do, Yanggu, Yanggu-eup, Godae-ri; 38°07′41.6″N, 127°59′24.7″E 181 m, sidewalk of Paro-ho, on the trunk of Ginkgo biloba; 30 June 2023, Young Woon Lim, Hannah Suh, Dohye Kim, Yoongil Lee (SFC20230630-23).

Notes: Morphological characters of Rigidoporus ginkgonis specimens from Korea match well with the morphological descriptions of the holotype. Only a few deviations exist, where the length of the tubes is shorter for the specimens from Korea (up to 4.5 mm for the holotype), and the size of the basidiospores is smaller compared to that of the holotype with (4.8–)5.0–6.0(– 6.5) × (3.9–)4.1–5.0(– 5.2) μm, L = 5.4 μm, W = 4.5 μm (Dai & Wang, 2005).

Sideraceae L.W. Zhou & Xue W. Wang.

Sidera Miettinen & K.H. Larss.

Sidera tibetica Z.B. Liu, Jian Yu & F. Wu, Fig. 6

Fig. 6figure 6

Sidera tibetica from the Republic of Korea. A Basidiome of SFC20230317-17. B Micromorphological characters, where ‘s’ refers to basidiospores, ‘b1’ for basidia, ‘b2’ for basidioles, ‘c’ for cystidioles, ‘h1’ for generative hyphae, ‘h2’ for skeletal hyphae, and ‘h3’ for crystallite hyphae

MycoBank: MB 843516

Description: Basidiomes annual, resupinate, soft corky. Hymenophore porous, cream (4A3), fading to white to the margin; sterile margin indistinct, thinning out; pores round but somewhat angular, 8–9 per mm; dissepiments thin, entire to lacerate; tube concolorous with the pore surface.

Hyphal structure dimitic, skeletal hyphae dominant, thin-walled, hyaline, rarely branched, rosette-like crystals frequently present. Basidiospores (1.8–)2.0–2.6(– 2.8) × 0.5–0.9 μm, L = 2.3 μm, W = 0.7 μm, Q = 2.4–4.6, allantoid to cylindrical, thin-walled, hyaline, smooth, acyanophilous, and neither amyloid nor dextrinoid. Basidia (8.1–)8.6–9.6(– 10.1) × (3.5–)4.0–4.4 μm, barrel-shaped to clavate, hyaline, 4-spored. Cystidioles 9.4–12.7 × 2.6–3.9 μm, fusoid, basally swollen, somewhat sharp tip, infrequent, thin-walled, hyaline. Clamp connections present.

Ecology/Substrate/Host: Grows on dead Pinus spp.

Distribution: China, Republic of Korea

Specimen examined: Republic of Korea: Gwangju, Buk-gu, Mudeung-ro; 35°8′59″N 126°59′15″E, 360 m, Mt. Mudeung, mixed forest, on the trunk of a dead Pinus densiflora; 17 Mar 2023, Yoonhee Cho, Dohye Kim (SFC20230317-17).

Notes: Morphological characters of Sidera tibetica specimen from Korea largely correspond to those of the holotype. The only difference lies in the sizes of the basidiospores and cystidioles. The sizes were smaller for the specimen from Korea, where the holotype bore larger basidiospores of (2.8–)2.9–3.1(– 3.3) × 1–1.1(– 1.2) μm, and cystidioles of 13–15 × 3–4 μm (Liu et al., 2022).

Skvortzoviaceae L.W. Zhou & Xue W. Wang

Skvortzovia Bononi & Hjortstam

Skvortzovia dabieshanensis Jia Yu, Xue W. Wang, S.L. Liu & L.W. Zhou, Fig. 7

Fig. 7figure 7

Skvortzovia dabieshanensis from the Republic of Korea. A Basidiome of SFC20190322-05. B Micromorphological characters, where ‘s’ refers to basidiospores, ‘b1’ for basidia, ‘b2’ for basidioles, ‘c’ for cystidioles, ‘t’ for hymenial tissue, and ‘h’ for generative hyphae

MycoBank: MB 840228

Description: Basidiomes annual, resupinate, closely adnate, not easily separable, thin, white to ash-gray (1B1). Hymenophore minutely grandinoid, 9–10 aculei per mm; margin thinning out, white.

Hyphal structure monomitic, hyaline, thin-walled, frequently branched. Basidiospores 4.5–4.6 × 1.7–1.9 μm, L = 4.6 μm, W = 1.8 μm, Q = 2.4–2.6, reniform, hyaline, smooth, acyanophilous, and neither amyloid nor dextrinoid. Basidia 10.0–14.9(– 20.9) × 3.1–4.2 μm, narrowly obpyriform, hyaline, 4-spored. Leptocystidia 17.8 × 3.5 μm, cylindrical, capitate, hyaline, thin-walled. Clamp connections present.

Ecology/Substrate/Host: Grows mostly on dead Pinus spp.

Distribution: China, Republic of Korea

Specimens examined: Republic of Korea: Gangwon-do, Yangyang-gun, Osaek-ri; 38°4′20″N 128°26′54″E, 415 m, Mt. Jeombong, Pinus koraiensis forest, on the trunk of a dead P. koraiensis; 7 May 2016, Young Woon Lim, Jae Young Park (SFC20160907-26). Republic of Korea: Gyeongsangnam-do, Hapcheon-gun, Mt. Gaya, Pinus densiflora forest, on the trunk of a dead P. densiflora; 9 Feb 2017, Young Woon Lim, Nam Kyu Kim, Hae Jin Cho (SFC20170209-12). Republic of Korea: Gyeongsangnam-do, Hapcheon-gun, Mt. Gaya, Pinus densiflora forest, on the trunk of a dead P. densiflora; 7 Sep 2018, Hyun Lee, Nam Hwi Kim, Abel Severin Lupala (SFC20180907-152). Republic of Korea: Gangwon-do, Inje-gun, Jindong-ri, on the trunk of a dead P. densiflora; 29 Sep 2018, Young Woon Lim, Ki Hyeong Park, Abel Severin Lupala (SFC20180929-32). Republic of Korea: Gyeongsangbuk-do, Bonghwa-gun, Seokpo-myeon, Daehyeon-ri; 37°4′16″N 128°57′60″E, Mt. Taebaek National Park, mixed forest, on the trunk of a dead P. densiflora; 22 Mar 2019, Young Woon Lim, Myung Soo Park, Min-Ji Kim, Hyun Lee, Ki Hyeong Park, Shinnam Yoo, Nam Hwi Kim (SFC20190322-05).

Notes: Most specimens of Skvortzovia dabieshanensis in Yu et al. (2021) and all our observed specimens developed basidiomes on Pinus as a host plant. Despite the geographical separation, specimens from Korea share similar morphological characteristics with those of the holotype. Still, they are distinctive in having smaller and more frequent aculei than the holotype, which bears 5–6 aculei per mm (Yu et al., 2021). Specimens from Korea also have narrower basidiospores and broader but shorter basidia than those of the holotype with basidiospores of (3.5–)3.8–4.7(− 4.9) × 1.8–2.4(− 2.6) μm and basidia of 10–20 × 3.5–5 μm (Yu et al., 2021).

Tubulicrinaceae Jülich

Tubulicrinis Donk

Tubulicrinis calothrix (Pat.) Donk, Fig. 8

Fig. 8figure 8

Tubulicrinis calothrix from the Republic of Korea. A Basidiome of SFC20180822-18. B Micromorphological characters, where ‘s’ refers to basidiospores, ‘b1’ for basidia, ‘b2’ for basidioles, ‘c’ for cystidioles, and ‘h’ for thin- and thick-walled hyphae

MycoBank: MB 307182

Description: Basidiomes annual, resupinate, adnate, thin, discontinuous, rimulose, soft. Hymenophore smooth, white to light brown (4A3); margin indistinct, white, thinning out.

Hyphal structure monomitic, hyphae thin- to thick-walled, hyaline, rarely branched in subiculum, highly branched and septate in trama. Basidiospores (3.3–)3.7–4.9(– 5.0) × 1.1–1.9 μm, L = 4.3 μm, W = 1.5 μm, Q = 2.3–3.7, allantoid, thin-walled, hyaline, smooth, acyanophilous, and neither amyloid nor dextrinoid. Basidia (9.6–)9.7–12.3(– 13.5) × (2.7–)2.9–3.6(– 3.8) μm, subclavate, hyaline, 4-spored. Cystidia 50.0–88.1(– 93.4) × 4.8–9.9 μm, cylindrical to setiform, numerous, hyaline, some with bent and elongated base, thick-walled but narrowing to the obtuse and sometimes encrusted apex, capillary lumen abruptly expanded near the apex, amyloid. Clamp connections present.

Ecology/Substrate/Host: Commonly found in the northern and highland; grows on coniferous wood

Distribution: Widely reported across all continents except for South America

Specimen examined: Republic of Korea: Seoul, Gwanak-gu, Mt. Gwanak, mixed forest, on the trunk of a dead Pinus densiflora; 22 Aug 2018, Young Woon Lim, Abel Severin Lupala (SFC20180822-18).

Notes: There were very few fertile cells and basidiospores in tissue where cystidia were abundant, and vice versa. The specimen from Korea largely corresponded to the morphological characters described for the specimens from Northern Europe, but several micromorphological characters were disparate. Tubulicrinis calothrix in Korea has shorter basidiospores, smaller basidia, and shorter cystidia than those of T. calothrix from Northern Europe with basidiospores of 6–7(– 8) × 1.5–1.8(– 2) μm, basidia of 12–15 × 4–5 μm, and cystidia of 80–120 × 6–8 μm (Hjortstam et al., 1988).

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