Research Article |
Corresponding author: Tai-Hui Li ( mycolab@263.net ) Academic editor: Zai-Wei Ge
© 2019 Ming Zhang, Chao-Qun Wang, Tai-Hui Li.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Zhang M, Wang C-Q, Li T-H (2019) Two new agaricoid species of the family Clavariaceae (Agaricales, Basidiomycota) from China, representing two newly recorded genera to the country. MycoKeys 57: 85-100. https://doi.org/10.3897/mycokeys.57.36416
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Two new lamellar species, Camarophyllopsis olivaceogrisea and Hodophilus glaberripes, of the family Clavariaceae were discovered in the subtropical zone of China. Camarophyllopsis olivaceogrisea is morphologically characterized by its hygrophanous basidiomata, greenish gray to dull green pileus, shortly decurrent lamellae, broadly elliptic basidiospores 4–5.5 × 3.5–4.5 μm in size, and cutis-like pileipellis composed of cylindrical cells. Hodophilus glaberripes is mainly characterized by its white to brownish pileus, glabrous stipe, slight yam bean smell, broadly elliptic basidiospores 5–6.5 × 4–5 μm in size, and epithelium-like pileipellis composed of inflated cells. Phylogenetic placement of the two species was determined by the combined analyses of a DNA data matrix containing ITS and LSU, and showed that collections of the two species formed two independent lineages in the Camarophyllopsis and Hodophilus clades respectively. The delimitation of C. olivaceogrisea and H. glaberripes were evaluated using molecular, morphological, and ecological methods. This is the first report of the genera Camarophyllopsis and Hodophilus in China.
Camarophyllopsis, Hodophilus, phylogenetic analysis, subtropical zone, taxonomy
Clavariaceae Chevall. (Agaricales, Basidiomycota) is a genetically monophyletic but morphologically diverse family. Members of this family show variations in the macromorphology of their sporocarps and are pendant-hydnoid, cylindrical, clavate, coralloid, resupinate, pileate, or lamellate-stipitate (
Camarophyllopsis can be easily distinguished from other genera in the family by its small agaricoid basidiomata, hygrophanous pileus, subglobose to broadly ellipsoidal basidiospores, and epithelium pileipellis composed of chains of erect, ascending or repent, subcylindrical to ellipsoid terminal cells (
In this study, some agaricoid collections were identified in China. Morphological observation and phylogenetic analyses confirmed that they are two novel taxa in the genera Camarophyllopsis and Hodophilus. This is the first report of these two genera in China.
Photographs of basidiomata were taken in type localities when collected. Macro-morphological characteristics were recorded for fresh specimen. Specimens were dried and then deposited in the Guangdong Institute of Microbiology (
Total genomic DNA of each voucher specimen was extracted from silica-gel-dried materials using the Sangon Fungus Genomic DNA Extraction kit (Sangon Biotech, Shanghai, China) according to the manufacturer’s instructions. Primer pairs ITS1/ITS4 (
Newly generated sequences, related sequences used in previous studies (
Taxon | Voucher | Country | ITS | LSU |
---|---|---|---|---|
Camarophyllopsis olivaceogrisea | GDGM44497 | China | MK894563 | MK894551 |
GDGM44519 | China | MK894564 | MK894552 | |
Camarophyllopsis sp. | GDGM44501 | China | MK894565 | MK894553 |
Hodophilus glaberripes | GDGM45940 | China | MK894566 | MK894554 |
GDGM52374 | China | MK894567 | MK894555 | |
GDGM52530 | China | MK894568 | – | |
GDGM52545 | China | MK894569 | MK894556 | |
GDGM52583 | China | MK894570 | MK894557 | |
GDGM55689 | China | MK894571 | MK894558 | |
GDGM70329 | China | MK894572 | MK894559 | |
GDGM70331 | China | MK894573 | MK894560 | |
GDGM72434 | China | MK894574 | MK894561 | |
GDGM72518 | China | MK894575 | MK894562 |
ITS and LSU sequences were respectively aligned using Clustal X v1.81 (Thompson et al. 1997) and manually modified where necessary in Bioedit v7.0.9 (Hall 1999), and a combined matrix of ITS and LSU sequences was obtained. The combined dataset was then analyzed using RAxML v7.2.6 (
For phylogenetic analyses, 25 sequences (13 ITS and 12 LSU) were newly generated from 13 collections, 219 related sequences (123 ITS and 96 LSU) were retrieved from GenBank, and Ramariopsis corniculata (Schaeff.) R.H. Petersen selected as an outgroup based on previous studies (
Phylogenetic placements of Camarophyllopsis olivaceogrisea and Hodophilus glaberripes inferred from the combined ITS and LSU dataset using RAxML. Ramariopsis corniculata was selected as an outgroup. The lineages with new species were shown in bold. BS ≥ 50% and PP ≥ 0.90 were indicated around the branches.
The tree topologies generated in this study are similar to those obtained by
The epithet “olivaceogrisea” refers to the olive-gray pileus color.
This new species is morphologically distinguished from other taxa in the genus by its smaller basidiomata, greenish gray to dull green pileus, white and short decurrent lamellae, and broadly elliptic basidiospores.
CHINA. Guizhou Province: Leishan County, Leigongshan National Nature Reserve, alt. 1260 m, 22 July 2014, M. Zhang (holotype: GDGM44519!).
Basidiomata small-sized. Pileus 7–12 mm broad, hemispherical, convex to plano-convex at first, then gradually applanate, becoming depressed at disc when mature, non-striate to weakly striate; margin slightly inflexed at first, soon straight, slightly crenate or lacerate when mature; surface matt, velvety, hygrophanous, greenish gray (or olive gray) to dull green (27D 2–30D2, 27D3–30D3, 27E2–30E2, 27E3–30E3), often paler at margin. Flesh 1–3 mm thick in the stipe, white to grayish white, unchanging when exposed. Lamellae 1–2 mm deep, L = 20–34, l = 1–3, short to moderately decurrent, white to weakly grayish white (1A1–1B1) at first, white to weakly greenish white (27A2–30A2) when mature, unchanging when bruised; edge entire, concolorous with the sides. Stipe 13–25 × 1.5–2.5 mm, central, cylindrical and becoming narrower downwards; glabrous and shiny, hardly tomentulose or pruinose, hygrophanous, white to greenish white at first (28A1–28A2, 29A1–29A2), becoming greenish white to light greenish gray (28A2–28B2, 29A2–29B2) when mature and in dry condition. Odor none. Taste mild.
Basidiospores [60/2/2] 4–5.5(–6) × 3.5–4.5(–5) μm, av. 4.6 × 3.8 μm, Q = (1.12)1.14–1.28(1.43), av. Q = 1.21 ± 0.08, broadly ellipsoid, hyaline, smooth, inamyloid, thin-walled. Basidia 4-spored, occasionally 2-spored, (10–)15–26(–30) × 5–7 μm, av. 24.5 × 5.8 μm, hyaline, narrowly clavate, attenuated and flexuous toward base, sterigmata up to 4 μm long. Basidioles cylindrical to narrowly clavate, often flexuous, obtuse, (18–)20–37.5(–40) × 6–8 μm, av. 23 × 6.8 μm. Pleurocystidia absent. Marginal cells on the lamellar edges not well differentiated, similar to basidioles on lamellar sides. Lamellar trama composed of sub-parallel or occasionally interwoven and irregularly inflated hyphae (23–)35–50(–104) × 4–8(–10) μm, av. 46.5 × 7 μm. Pileipellis a cutis of numerous repent branched hyphal 4–8 μm wide, with terminal chains of ellipsoid or cylindrical cells. Pileus trama composed of cylindrical and occasionally branched hyphae (23–)35–50(–70) × (4–)6–10 μm, av. 45.5 × 7.6 μm. Stipitipellis formed of parallel, thin-walled and narrow hyphae 3–8 μm diam. Caulocystidia not observed. Clamp connections absent in all tissues.
Solitary, scattered on soil in mixed forests; currently only known from the Guizhou Province of China.
CHINA. Guizhou Province: Leishan County, Leigongshan National Nature Reserve, alt. 1120 m, 22 July 2014, J. Xu (GDGM44497).
The epithet refers to the glabrous stipe.
This species is easily distinguished from other species in the genus Hodophilus by its larger basidiomata, white, brownish orange to brown pileus, glabrous stipe, slightly yam bean smell and broadly elliptic basidiospores.
CHINA. Guangdong Province: Shaoguan City, Danxiashan National Nature Reserve, alt. 240 m, 10 May 2018, M. Zhang (holotype: GDGM72518!).
Basidiomata small to medium-sized. Pileus 15–50 mm broad, hemispherical, convex to plano-convex at first, then becoming broadly convex or plano-convex but hardly fully expanded to plane, often depressed at disc when old; white to yellowish white at first, then gradually becoming orange white, pale yellow, pale orange, brownish orange, light brown, brown to reddish brown (5A2, 3A3–5A3, 5C4–7C4, 5D5–9D5) when mature and dry, hygrophanous; margin first slightly inflexed, soon straight, slightly crenate when mature, non-striate or indistinctly translucently striate up to one third when wet; surface matt, velvety and later with fine and darker granules or pruina, at first even, but becoming rugose or rough towards the center when mature, often concentrically cracked in dry conditions. Flesh 0.5–2 mm thick in half radius of the pileus, white, pinkish white to pale beige; Lamellae 3–5 mm deep, distant to subdistant, L = 21–32, l = 1–3, short decurrent, notched, orange white to pinkish white (5A2–10A2) when young, brownish orange, light brown, reddish brown to brownish red (5C4–7C4, 5D6–10D6) when mature, unchanging when bruised; edge entire, concolorous or slightly paler than lamella sides. Stipe (50) 80–100 × 3–5 mm, cental, usually flexuous, cylindrical and slightly narrower downwards; glabrous smooth and shiny, hygrophanous, white to yellowish white at first, becoming pale yellow to pale orange when mature and in dry condition. Odor none or slight yam bean smell, taste mild.
Basidiospores [210/9/9] (4.5)5–6.5(7) × 4–5(5.5) μm, av. 5.9 × 4.7 μm, Q = (1.0)1.11–1.37(1.4), av. Q = 1.20 ± 0.11, broadly ellipsoid to subglobose, hyaline, smooth, inamyloid, thin-walled. Basidia 4-spored, occasionally 2-spored, (32–) 36–46(–66) × (4–)4.5–6(–7) μm, av. 39.5 × 5.9 μm, tenuated and flexuous towards base, with sterigmata up to 7 μm long. Basidioles cylindrical to narrowly clavate, obtuse, often flexuous, (31–)34–42(–60) × (4–)6–8(–10) μm, av. 40.5 × 6.9 μm. Pleurocystidia absent. Marginal cells on the lamellar edges usually not well differentiated, similar to basidioles on lamellar sides. Lamellar trama composed of sub-parallel or occasionally interwoven and irregularly inflated branched hyphae with elongate cells (38–)52–98(–160) × (4–)6–14(–20) μm, av. 88 × 9.5 μm. Subhymenium poorly developed. Pileipellis a transition from hymeniderm to epithelium, with hyphal elements 3–10 μm wide, thin-walled, hyaline, terminations usually composed of 1–3 inflated cells; terminal cells obpyriform, subglobous or ellipsoid, rarely sphaero-pedunculate or broadly clavate, (15–)19–46(–50)× (7–)12–22(–30) μm, av. 38.5 × 18 μm. Pileus trama composed of subparallel hyphae (34–)46–89(–130) × (4–)5.5–10 μm, av. 74 × 7.6 μm. Stipitipellis formed of parallel, thin-walled and narrow hyphae 3–6 μm diam. Caulocystidia usually in dense fascicles or patches, thin-walled, repent or ascending; with terminal cells mainly clavate, occasionally subcapitate or obpyriform, obtuse, often pedicellate and flexuous, measuring (18–)22–53(–60)× (4–)5.5–13 μm, av. 43 × 7.5 μm. Clamp connections absent in all tissues.
Solitary, scattered on soil in broadleaf forests and mixed forests; currently only known from China.
CHINA. Guangdong Province: Huizhou City, Xiangtoushan National Nature Reserve, alt. 640 m, 18 May 2016, H. Huang (GDGM45940); Shaoguan City, Nanling National Nature Reserve, 800 m, 29 July 2017, M. Zhang (GDGM70329 and GDGM70331); Shaoguan City, Danxiashan National Nature Reserve, 200 m, 27 April 2019, X.R. Zhong (GDGM76367 and GDGM76337), J.P. Li (GDGM76300); Jiangxi Province: Jinggangshan Botanical Garden, 884 m, 20 June 2016, H. Huang (GDGM52374), Z.P. Song (GDGM52545); same location, 21 June 2016, Z.P. Song (GDGM52530 and GDGM52583); Hunan Province: Chenzhou City, Jiulongjiang National Forest Park, alt. 230 m, 14 May 2018 X. R. Zhong (GDGM55689).
1 | Basidiomata agaricoid; pileipellis an epithelium composed of chains of subcylindrical to ellipsoid terminal elements | 2 Camarophyllopsis |
– | Basidiomata agaricoid; pileipellis a hymeniderm composed of broadly inflated, globose, and obpyriform to sphaero-pendunculate terminal elements | 12 Hodophilus |
2 | Pileus diameter usually < 30 mm | 3 |
– | Pileus diameter usually ≥ 30 mm | 11 |
3 | Pileus hygrophanous or subhygrophanous | 4 |
– | Pileus not hygrophanous | 5 |
4 | Pileus greenish gray to dull green; lamellae white, decurrent; basidiospores 4–5.5 × 3.5–4.5 μm | C. olivaceogrisea |
– | Pileus rugulose, buffy brown to dark hazel; lamellae decurrent, pinkish to hazel; stipe olive brown or grayer; basidiospores globose av. 4 × 5 μm | C. rugulosoides |
5 | Lamellae always with pink tinct, pale pink to pink, decurrent; pileus pale pink to whitish, matt; stipe pale pink to whitish; basidiospores av. 7 × 4.5 μm | C. roseola |
– | Lamellae without pink tinct | 6 |
6 | Lamellae white, unchanging when mature | 7 |
– | Lamellae whitish to grayish or brownish | 9 |
7 | Basidiospores < 6 μm; pileus brownish to dark brown, subtomentosus, depress in central when mature; stipe concolorous with pileus or slightly faded | C. atrovelutina |
– | Basidiospores usually ≥ 6 μm | 8 |
8 | Pileus gray, manifestly cleaving at margin when dry; stipe white; basidiospores 5.5–8.5 × 4–5.5 μm | C. leucopus |
– | Pileus gray, sub-velvety; stipe pale gray; basidiospores 7–8 × 5.5–6.5 μm | C. tetraspora |
9 | Basidiospores ≥ 7 μm; pileus fuliginous brown, subfibrillose to fibrillose, infundibuliform; lamellae deep decurrent; stipe brown | C. araguensis |
– | Basidospores < 7 μm | 10 |
10 | Pileus dark brown, subtomentosus; lamellae light grayish, decurrent; stipe white, smooth, basidiospores 5–6.5 × 4–5 μm | C. albipes |
– | Pileus yellowish cinnamon to brownish cinnamon or chocolate gray, silky-tomentose or velvet; lamellae decurrent, whitish to grayish or brownish; stipe concolorous with pileus; basidiospores 4–5 × 4–4.5 μm | C. schulzeri |
11 | Pileus brownish gray to grayish brown; lamellae adnate to subdecurrent, white; stipe smooth, white; basidiospores 5–7 × 3.5–4.5 μm | C. pedicellata |
– | Pileus pearl gray to drab, often rivulose-cracking; lamellae light gray; stipe light gray, slightly longitudinally fibrillose-striped; basidiospores 5–7 × 3.5–5.2 μm | C. dennisiana |
12 | Basidiomata with a napthalene or an unpleasant odor |
see |
– | Basidiomata without napthalene odor | 13 |
13 | Stipe with dark dots on surface | 14 |
– | Stipe never with dark dots on surface | 16 |
14 | Lamellae white to grayish white, pileus pale brown; basidiospores 4.5–6 × 4.0–5 μm, pileipellis an epithelium composed of globose to pyriform elements | ’C. kearneyi’ |
– | Lamellae with orange, brown or light brown tinct | 15 |
15 | Pileus yellowish gray to brown when fresh, light brown, orange gray to beige when mature; lamellae beige or orange gray at first, changing to brownish orange to yellowish brown when mature, basidiospores 4.6–5.4 × 3.5–4.2 μm | H. atropunctus |
– | Pileus dark brown to pale brown; lamellae light brown to grayish brown when young, changing brown to dark brown when mature; basidiospores 4.8–5.4 × 3.9–4.5 μm | H. variabilipes |
16 | Stipe with yellow tinct |
see |
– | Stipe without yellow tinct | 17 |
17 | Species has south hemisphere distribution, pileus creamy buff-brown or pinkish fawn; lamellae decurrent, pale pinkish; basidiosproes 4.5–6.0 × 4.5–5.5 μm; pileipellis an epithelium of globose or pyriform elements; known from Australia | ’C. darminensis’ |
– | Species has north hemisphere distribution | 18 |
18 | Pileus yellowish white, brownish orange to reddish brown; lamellae orange white to brownish red; basidiospores 5–6.5 × 4–5 μm; known from China | H. glaberripes |
– | Pileus grayish brown to brownish orange; lamellae subdecurrent, pale orange; stipe grayish orange, glabrous; basidiospores 4–5 × 3–5 µm; known from India | H. indicus |
Phylogenetic relationships of the genera within Clavariaceae have been investigated in several studies, and Camarophyllopsis and Hodophilus were well supported as two independent groups at generic level (
According to the phylogram (Figure
In the Hodophilus clade, H. glaberripes is closely related to H. indicus K.N.A. Raj, K.P.D. Latha & Manim., and together formed a well-supported branch, which is a sister clade to the yellow stipe clade (or H. micaceus superclade) as defined by Adamčík et al. (2017,
Morphologically, the most distinctive features of C. olivaceogrisea are the small basidiomata with a greenish gray to dull green pileus, white and decurrent lamellae, broadly ellipsoid basidiospores, narrowly clavate basidia, and a cutis pileipellis composed of chains of cylindrical cells. Camarophyllopsis microspora (A.H. Sm. & Hesler) Bon is similar to C. olivaceogrisea to some extent. However, C. microspora, originally reported in Michigan, differs on account of its fuscous pileus and stipe, dark grayish context and smaller basidiospores (4–4.5 × 2.5–3 μm) (
Hodophilus glaberripes is characterized by its larger basidiomata, hygrophanous pileus with white, brownish orange to brown color, glabrous stipe, larger and broadly elliptic basidiospores, epithelium-like pileipellis with obpyriform or subglobous terminal cells, and slightly yam bean smell. The combination of these characteristics makes H. glaberripes easily distinguishable from other members of the genus. Hodophilus glaberripes is somewhat similar to H. albofloccipes (Kovalenko, E.F. Malysheva & O.V. Morozova) Looney and Adamčík, H. anatinus Dima, Adamčík & Jančovičová, H. subfoetens Adamčík, Jančovičová & Looney, and H. pallidus Adamčík, Jančovičová & Looney in morphology. However, H. albofloccipes mainly differs by its smaller baisdiomata, ochre or ochre yellow to pale olives pileus, yellow to brownish stipe covered with white pruina or squamula, smaller basidiospores (4–5.7 × 3.5–5 μm), and naphthalene-like odor (
Ecologically, very little is known about the ecology of Camarophyllopsis species, as for most species only a few verified collections are known and little molecular data is available. Camarophyllopsis species are widely distributed in the southern and northern hemispheres, from tropical zones to cool temperate zones, and in monsoon forest, bushy forest, and grassland habitats, and some species have been shown to be saprotrophic (
Hodophilus taxa were mainly reported in temperate to boreal zones of the northern hemisphere and can be found in forest, bushy forest margin, grassland and bare soil habitats (
Sincere acknowledgements are expressed to Dr. J. Xu, Mr. H. Huang, J.P. Li, Z.P. Song, X.R. Zhong and S.H. Zhou (Guangdong Institute of Microbiology, China) for their kind help during the field trips. This study was supported by the National Natural Science Foundation of China (Nos. 31700021, 31770014, 31670029), the Science and Technology Project of Guangdong Province (2017A030303050, 2018B030324001) and the GDAS’ Special Project of Science and Technology Development (2019GDASYL-0104009).