Two New Species of Hymenogaster (Hymenogastraceae, Agaricales) from China Based on Morphological and Molecular Markers
1
Department of Life Sciences, National Natural History Museum of China, 126 South Tianqiao Street, Beijing 100050, China
2
College of Life Science, Capital Normal University, 105 Xisanhuan Beilu, Beijing 100048, China
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(5), 303; https://doi.org/10.3390/d16050303
Submission received: 11 April 2024
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Revised: 15 May 2024
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Accepted: 16 May 2024
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Published: 17 May 2024
Abstract
:Two new species from China, Hymenogaster pseudoniveus and H. zunhuaensis, are described and illustrated based on morphological and molecular evidence. Hymenogaster pseudoniveus is distinguished from other species of the genus based on the color of peridium, which is snow white to white when unexcavated but then turns yellowish to earth yellow, and the basidiospores, which are ornamented with nearly longitudinally arranged ridges up to 2 μm high. H. zunhuaensis is diagnosed by its dirty white to pale yellow peridium, yellow brown to brown gleba, and the smaller (Lm × Wm = 11.7 μm × 9.8 μm) broadly ellipsoidal to subglobose basidiospores (Q = 1.1–1.3). ITS/LSU-based phylogenetic analysis supports the erection of the two new species, each placed in distinct clades with strong statistical support, suggesting that they represent two distinct species novel to science. Based on the morphological and molecular evidence, we have published two new species of Hymenogaster. A key for Hymenogaster species from China is provided.
1. Introduction
As a globally widespread genus, the Hymenogaster are found in Europe [1,2,3,4], Asia [5,6], North America [7] of the Northern Hemisphere, Australia [8], Oceania [9,10], South America [11], and Central Africa [12] of the Southern Hemisphere. In China, Hymenogaster has been recorded across 21 provinces or cities, notably in areas such as Hebei, Shaanxi, Shanxi, and Yunnan [13,14], which are recognized for their high species richness.
As hypogeous fungi, the Hymenogaster species symbiotically form ectomycorrhizae with various tree species, helping plants uptake nutrients and rebuild the ecosystems [6,15,16,17,18,19,20,21,22]. They also serve as food sources for small mammals in the forest, such as Clethrionomys gapperi, Napaeozapus insignis, Sus scrofa, Tamias striatus, Tamiasciurus hudsonicus, and Zapus hudsonius, as well as some birds and invertebrates, and in this way, these small animals can also help spread Hymenogaster spores [23,24,25,26].
To date, about 170 species of this group have been reported globally [27], but only 32 species and variants of Hymenogaster have been reported in China, and most of them lack molecular data. Recently, seven species have been identified based on morphological and molecular evidence [14]. In this study, two new species were recognized from our collections based on morphological and molecular evidence, which have been described and illustrated.
2. Materials and Methods
2.1. Morphological Studies
Fresh specimens were collected from Hebei, Shanxi, Shaanxi, and Yunnan provinces over a period of several years in China and were subsequently dried and deposited at BJTC (Herbarium Biology Department, Capital Normal University). Several older specimens were also examined from HMAS (Herbarium Mycologicum Academiae Sinicae, Institute of Microbiology, Chinese Academy of Sciences). Macroscopic characters were recorded from fresh specimens whenever possible. Microscopic characters were examined in both fresh and dried materials by mounting free-hand sections of basidiomata in 5% KOH and Melzer’s reagent [28]. Basidiospores dimensions, excluding ornamentation, were based on 30 spores for each basidiome, with the measurements presented as the diameter (mean diam ± SD, n = 30) for each species. For scanning electron microscopy (SEM), spores were scraped from the dried gleba, placed onto double-sided adhesive tape that was mounted directly on the SEM stub, coated with an 8 nm thick platinum–palladium film using an ion-sputter coater (HITACHI E-1010), and examined with a HITACHI S-4800 SEM.
2.2. DNA Extraction, PCR Amplification, Sequencing and Nucleotide Alignment
Dried gleba was ground by shaking for 45 s at 30 Hz 2–4 times (Mixer Mill MM 301, Retsch, Haan, Germany) in a 1.5 mL tube along with a 3 mm diameter tungsten carbide ball, and total genomic DNA was extracted using the modified CTAB method [29]. The internal transcribed spacer (ITS) region of nuclear ribosomal DNA (nrDNA) was amplified using primers ITS1f/ITS4 [29,30]. The 28S large subunit (nrLSU) nrDNA region was amplified using primers LR0R/LR5 [31]. Polymerase chain reactions (PCRs) were performed in 50 µL reactions containing 2 μL of each DNA primer (10 μM), 25 μL of 2 × Master Mix (Tiangen Biotech (Beijing) Co., Beijing, China), 17 μL ddH2O, and 4 μL of dNTPs. Amplification reactions were implemented as follows: for the ITS gene—an initial denaturation at 95 °C for 4 min, followed by 35 cycles at 95 °C for 30 s, 55 °C for 45 s, 72 °C for 1 min, and a final extension at 72 °C for 10 min; for the nrLSU gene—an initial denaturation at 95 °C for 4 min, followed by 35 cycles at 95 °C for 30 s, 55 °C for 1 min, 72 °C for 1 min, and a final extension at 72 °C for 10 min. The PCR products were sent to Beijing Zhongkexilin Biotechnology Co., Ltd. (Beijing, China) for purification and sequencing. Validated sequences are stored in the NCBI database (http://www.ncbi.nlm.nih.gov/, accessed on 10 April 2024) under the accession numbers provided; other sequences used in this study were downloaded from GenBank (Table 1).
2.3. Phylogenetic Analysis
The ITS-LSU combined dataset was assembled and aligned utilizing the MAFFT algorithm [32], adhering to default parameters, and manually adjusted to allow maximum sequence similarity in Se-Al v.2.03a [33]. Alignments of all datasets used in this study were submitted to TreeBASE (No. 31314). Maximum likelihood (ML) and Bayesian inference (BI) analysis were used to construct a phylogenetic tree separately using two methods. ML analysis was performed with RAxML v.8.0.14 [34,35,36] employing the GTRGAMMAI substitution model with the parameters unlinked, which was determined by MrModeltest v.2.3 [37]. ML bootstrap replicates (1000) were computed in RAxML using a rapid bootstrap analysis and a search for the best-scoring ML tree was conducted. The ML trees were visualized using TreeView v.32 [38]. Clades with bootstrap support (BS) ≥70% were considered significant [39]. BI was conducted using MrBayes v.3.1.2 [40] as an additional method of evaluating branch support. In the BI analysis, after selecting the best substitution models (GTRGAMMAI) determined by MrModeltest [37], two independent runs of four chains were conducted for 1,440,000 Markov chain Monte Carlo (MCMC) generations using the default settings. Average standard deviations of split frequency values were far less than 0.01 at the end of the generations. Trees were sampled every 100 generations after burn-in (well after convergence), and a 50% majority-rule consensus tree was constructed and visualized using TreeView [38]. Clades with Bayesian posterior probability (PP) ≥ 0.95 were considered significantly supported [41].
3. Results
3.1. Molecular Phylogenetics
The ITS and LSU datasets were concatenated to find the phylogenetic positions of the new species described in this study. The final alignment of this comprehensive dataset comprises 111 sequences from 25 different species, inclusive of 26 newly generated sequences derived from our collections. The length of the aligned dataset was 1360 bp after the exclusion of poorly aligned sites, with 618 bp for ITS and 742 bp for nrLSU. Sequences were analyzed by ML and BI, which yielded identical tree topologies, and only the tree inferred from the ML analysis is shown (Figure 1). The sequences isolated from our collections were grouped into two independent clades with strong statistical support (Figure 1), suggesting that they represent two distinct species novel to science. We described them as Hymenogaster zunhuaensis sp. nov. and H. pseudoniveus sp. nov. in this paper. Hymenogaster zunhuaensis further clustered together with H. minisporus with relatively strong statistical support, suggesting that both species are related. Hymenogaster pseudoniveus is resolved in an independent clade with strong statistical support, and it is basal to a large clade formed by H. minisporus, H. latisporus, H. variabilis, H. zunhuaensis, and three undescribed species.
3.2. Taxonomy
Hymenogaster pseudoniveus L. Fan & T. Li, sp. nov. (Figure 2)
MycoBank: MB853450
Etymology: pseudoniveus, referring to the snow white basidiome when freshly excavated, which is similar to that of Hymenogaster niveus.
Holotype: China. Shanxi Province, Linfen City, Pu County, Wulu Mountain, Gelaozhang Village, alt. 1700 m, 26 October 2017, in soil under Pinus tabuliformis Blume, LT054 (BJTC FAN1075).
Diagnosis: Hymenogaster pseudoniveus is characterized by the color of the peridium that is snow white to white when freshly excavated, turning yellowish to earth yellow, with a slight reddish tinge, brown to dark brown gleba, and the basidiospores ornamented with ridges scattered, sometimes longitudinally arranged, occasionally verrucose, up to 2 μm high.
Basidiome subglobose to irregular globose, 0.8–2.5 cm diam, soft and elastic, snow white to white when freshly excavated, which turns yellowish to earth yellow or light yellow brown, with a distinct depression at the white sterile base. Surface smooth, glabrous.
Peridium 110–265 μm thick, composed of elliptic cells of 4.1–9.3 × 4.3–9.6 µm, light yellow brown to pale yellow, and more or less parallel interwoven hyphae of 2.1–3.9 µm broad, light yellow brown. Gleba has a slight reddish tinge, brown to dark brown at maturity, loculate, locules irregular oblong to subglobose, empty, filled with spores at maturity. Hymenium 18–30 μm thick. Hymenial cystidia 29–44 μm long, only present when young, collapses and disappeares at maturity. Basidia clavate, 2–3-spored, mostly 2-spored, sterigmata short, 1–3(–4) μm, basidia collapses and disappeares at maturity. Basidiospores ellipsoidal to broadly ellipsoidal, yellow brown to dark brown at maturity, ornamented with ridges up to 2 μm high, ridges scattered, sometimes longitudinally arranged, occasionally verrucose, (10.2–)13–17 (–20) × (8–)10–13(–14) μm (Lm × Wm = 15.3 ± 1.1 × 11.4 ± 0.8, n = 30), Q = 1.2–1.5 (Qav = 1.3), excluding ornamentations, with gelatinous perisporium when young, with a pronounced apex, obtuse, nearly hyaline, 2–3 μm high, with appendix, truncate, nearly hyaline, 1–2 μm long.
Figure 1.
Phylogeny derived from maximum likelihood analyses of the ITS/LSU sequences from Hymenogaster. Two sequences of Anamika lactariolens were selected as the outgroup. Values on the left represent the likelihood of bootstrap support values (≥70%). Values on the right represent significant Bayesian posterior probability values (≥0.95). Chinese sequences from basidiomates are in bold; two new species in this study are in green background. Super index “H” in red means “Holotype”.
Figure 1.
Phylogeny derived from maximum likelihood analyses of the ITS/LSU sequences from Hymenogaster. Two sequences of Anamika lactariolens were selected as the outgroup. Values on the left represent the likelihood of bootstrap support values (≥70%). Values on the right represent significant Bayesian posterior probability values (≥0.95). Chinese sequences from basidiomates are in bold; two new species in this study are in green background. Super index “H” in red means “Holotype”.
Figure 2.
Hymenogaster pseudoniveus (BJTC FAN1075, holotype). (a) Basidiomes. (b) Peridium under LM. (c) Basidiospores under LM. (d) Basidiospore under SEM.
Figure 2.
Hymenogaster pseudoniveus (BJTC FAN1075, holotype). (a) Basidiomes. (b) Peridium under LM. (c) Basidiospores under LM. (d) Basidiospore under SEM.
Habit, habitat, and distribution: hypogeous, gregarious, in the soil under Betula platyphylla Sukaczev, Castanea mollissima Blume, Larix gmelinii (Rupr.) Rupr., Pinus armandii Franch., P. bungeana Zucc. ex Endl., P. tabuliformis Carr., Quercus mongolica Fisch. ex Ledeb., Hebei, Shanxi and Shaanxi Provinces, Northern China.
Additional specimens examined:China. Hebei Province, Tangshan City, Zunhua County, Zhangzhuangzi Village, alt. 100 m, 16 November 2019, in soil under Castanea mollissima, LT124 (BJTC FAN1238); Shanxi Province, Yuncheng City, Yuanqu County, Lishan Town, Shunwangping scenic spot, alt. 2276 m, 17 October 2016, in soil under Pinus armandii, YXY026 (BJTC FAN662), CM015 (BJTC FAN667), SXY011 (BJTC FAN672), CM011 (BJTC FAN675), CM016 (BJTC FAN679), HKB030 (BJTC FAN705), WYW027 (BJTC FAN709); Lvliang City, Jiaocheng Country, Pangquangou, alt. 1897 m, 8 September 2017, in soil under Larix gmelinii, HKB099 (BJTC FAN874); Linfen City, Xi Country, Shenjiagou, alt. 1321 m, 10 September 2017, YXY 080 (BJTC FAN894), HKB114 (BJTC FAN940); Linfen City, Pu County, Wulu Mountain, Gelaozhang Village, alt. 1321 m, 10 September 2017, in soil under Pinus bungeana, LT024 (BJTC FAN916), LT027 (BJTC FAN919), LT028 (BJTC FAN920), LT029 (BJTC FAN921), HKB107 (BJTC FAN933), HKB108 (BJTC FAN934), 11 September 2017, HKB109 (BJTC FAN943), HKB118 (BJTC FAN945), XYY037 (BJTC FAN963), Chaoyanggou, alt. 1645 m, 11 September 2017, in soil under Quercus mongolica, XYY041 (BJTC FAN967); Gelaozhang Village, alt. 1321 m, 12 September 2017, in soil under Pinus bungeana, HKB128 (BJTC FAN997); Gelaozhang Village, alt. 1730 m, 26 October 2017, in soil under Quercus sp., XYY068 (BJTC FAN1068), XYY069 (BJTC FAN1069), alt. 1700 m, in soil under Pinus tabuliformis, LT054 (BJTC FAN1075); Yuncheng City, Xia County, Sijiao Town, Xigou Village, Taikuanhe, alt. 900 m, 26 October 2017, in soil under Pinus tabuliformis, HKB155 (BJTC FAN1117); Shaanxi Province, Yanan City, Huangling County, Diantou Town, Huangling National Forest Park, alt. 1100 m, 15 September 2020, in soil under Larix gmelinii, LT135 (BJTC FAN1251).
Hymenogaster zunhuaensis L. Fan & T. Li, sp. nov. (Figure 3)
MycoBank: MB853448
Etymology: zunhuaensis, referring to the locality where the type specimen was collected.
Holotype: China. Hebei Province, Tangshan City, Zunhua County, alt. 107 m, 17 September 2017, in soil under Castanea mollissima, XYY062 (BJTC FAN1062).
Diagnosis: Hymenogaster zunhuaensis is characterized by the dirty white to pale yellow peridium, yellow brown to brown gleba, and small, broadly ellipsoidal to subglobose basidiospores.
Basidiomes subglobose to irregular globose, gibbous, 1.0–2.5 cm diam, soft and elastic, dirty white to pale yellow, partial with pale brown when fresh, earth yellow to yellow brown when dry, with a distinct depression at the sterile base. Surface smooth, glabrous.
Peridium 70–280 μm thick, pseudoparenchymatous, composed of ellipsoid cells of 7–12 × 12–17 μm in diam, with some interwoven hyphae of 2.8–3.9 µm broad, pale yellow to nearly hyaline. Gleba has reddish to rusty tinge, yellow brown to brown when maturity, deep brown when dry, loculate, locules irregular, oblong or irregular globose, empty, filled with spores at maturity. Hymenium 27.8–55 μm thick. Hymenial cystidia hypha-like, 42–60 µm long, only present when young, collapses and disappears at maturity. Basidia narrow clavate, not inflate on the apex, 1–3-spored, mostly 2-spored, 42.5–65 µm long, sterigmata 2–4 μm long, basidia collapses and disappeares at maturity. Basidiospores broadly ellipsoidal to subglobose, yellow brown to dark brown at maturity, ornamented with short ridges of about 1 μm high, some ridges anastomosed, forming an irregular reticulum, 10–13.4(–15.6) × (7.2–)8.2–11.6(–13.3) μm (Lm × Wm = 11.7 ± 0.9 × 9.8 ± 0.8, n = 30), Q = 1.1–1.3 (Qav = 1.2), excluding ornamentations, without gelatinous perisporium, with a pronounced apex, obtuse, nearly hyaline, 2–3 µm high, with appendix, truncate, occasionally tenuous, hyaline, 1–3 μm long.
Habit, habitat, and distribution: hypogeous, gregarious, in the soil under Castanea mollissima, Quercus acutissima Carruth., Q. mongolica, Q. palustris Münchh., and Q. variabilis Blume, Hebei, Shaanxi, Shanxi, and Yunnan provinces, China.
Figure 3.
Hymenogaster zunhuaensis (BJTC FAN1062, holotype). (a) Basidiomes. (b) Peridium under LM. (c) Basidiospores under LM. (d) Basidiospore under SEM.
Figure 3.
Hymenogaster zunhuaensis (BJTC FAN1062, holotype). (a) Basidiomes. (b) Peridium under LM. (c) Basidiospores under LM. (d) Basidiospore under SEM.
Additional specimens examined: China. Shanxi Province, Yuncheng City, Yuanqu County, Lishan Town, Houwentang Village, alt. 1250 m, 4 June 1988, in soil under mixed forest, J.L. Wang 414 (HMAS83127 ex MHSU 2031), 7 July 1990, Y. Ma, B. Qiao & X.K. Bai 386 (HMAS96762 ex MHSU 2032), 1 August 1990, Y. Ma & B. Qiao 377 (HMAS81693, HMAS 83128 ex MHSU 2033); Yunnan Province, Kunming City, Heilongtan Park, 10 August 1990, in soil under Quercus acutissima, M.C. Chang & L. Wang 408 (HMAS83129 ex MHSU 2034); Hebei Province, Chengde City, Pingquan County, Liaoheyuan National Forest Park. alt. 1193 m, 1 October 2018, in soil under Quercus mongolica, GLJ010 (BJTC FAN1162); Tangshan City, Zunhua County, alt. 107 m, 17 September 2017, in soil under Castanea mollissima, XYY061 (BJTC FAN1061), XYY063 (BJTC FAN1063), XYY064 (BJTC FAN1064), XYY065 (BJTC FAN1065), LT080 (BJTC FAN1161); Shanxi Province, Yuncheng City, Xia County, Sijiao Town, Yujialing Village, alt. 970 m, 27 October 2017, in soil under Quercus variabilis, LT056 (BJTC FAN1082), LT057 (BJTC FAN1083), LT058 (BJTC FAN1084), LT060 (BJTC FAN1086), YXY125 (BJTC FAN1093), XYY073 (BJTC FAN1103), XYY075 (BJTC FAN1105), XYY077 (BJTC FAN1107), Xigou Village, alt. 900 m, 27 October 2017, in soil under Quercus sp., YXY132 (BJTC FAN1100), HKB148 (BJTC FAN1110), HKB149 (BJTC FAN1111), HKB150 (BJTC FAN1112), HKB157 (BJTC FAN1119), alt. 1057 m, 29 October 2017, in soil under Castanea mollissima, HKB163 (BJTC FAN1127); Jincheng City, Yangcheng County, Manghe Natural Reserve, alt. 580 m, 31 October 2017, YXY145 (BJTC FAN1145), YXY146 (BJTC FAN1146), Sijiao Town, alt. 1270 m, 5 October 2020, in soil under Quercus palustris, LT 141 (BJTC FAN1256), alt. 970 m, in soil under Quercus sp., LT143 (BJTC FAN1258), LT144 (BJTC FAN1259), alt. 1370 m, LT145 (BJTC FAN1260); Shaanxi Province, Hanzhong City, Fuoping country, Liangfengya Natural Reserve, alt. 890 m, 12 September 2020, in soil under Castanea mollissima, LT133 (BJTC FAN1249).
4. Discussion
Hymenogaster pseudoniveus is differentiated from other species of Hymenogaster based on the color of peridium changes, a slight reddish tinge, brown to dark brown gleba, and spore ornamentations up to 2 μm high. Hymenogaster pseudoniveus is similar to H. arenarius [42] in spore shape, but H. pseudoniveus has larger spores and longer apex than H. arenarius (Lm × Wm = 13.3 μm × 10.2 μm, 1–1.5 μm).
Hymenogaster zunhuaensis is similar to H. gilkeyae [43] and H. minisporus [14] in spore size. However, the peridium is earth yellow to yellowish and relatively uniform in thickness (112.5–185 μm thick) in H. gilkeyae, while it is of a different color with very variable thickness in H. zunhuaensis (see description). Hymenogaster minisporus clustered together with new species in the phylogenetic tree (Figure 1), while the former has light brown gleba, with a small apex (1–1.3 μm high), which is different from those of H. zunhuaensis.
Currently, nine Hymenogaster species have been supported with morphological and molecular data in China. A key for them is provided below.
Key to the species of Hymenogaster from China:
| 1. Basidiome pale yellow, white to dirty white when fresh | 2 |
| 1. Basidiome earth yellow to yellow brown when fresh | 6 |
| 2. Gleba reddish brown to brown when fresh | 3 |
| 2. Gleba light brown when fresh | H. minisporus |
| 3. Basidiospores length >17 μm | 4 |
| 3. Basidiospores length ≤17 μm | 5 |
| 4. Basidiospores 21–25.5 × 14–18.5 μm | H. citrinus |
| 4. Basidiospores 17–22 × 12–15 μm | H. perisporius |
| 5. Basidiospores 10–13.5 × 8–11.5 μm | H. zunhuaensis |
| 5. Basidiospores 13–17 × 10–13 μm | H. pseudoniveus |
| 6. Peridium exhibits substantial variation in thickness, differing by at least 120 μm | 7 |
| 6. Peridium exhibits substantial variation in thickness, differing by at the most 120 μm | 8 |
| 7. Basidiospores broad ellipsoidal to subglobose, Q = 1.1–1.3 | H. variabilis |
| 7. Basidiospores broad fusiform to broad citriform, Q = 1.3–1.4 | H. papilliformis |
| 8. Basidiospores fusiform, Q = 1.2–1.4 | H. arenarius |
| 8. Basidiospores broadly ellipsoidal to subglobose, Q = 1.1–1.3 | H. latisporus |
Author Contributions
Conceptualization, L.F.; Formal analysis, T.L.; Funding acquisition, T.L.; Investigation, N.M., H.F. and Y.Z.; Methodology, T.L.; Resources, L.F.; Software, N.M.; Writing—original draft, T.L. All authors have read and agreed to the published version of the manuscript.
Funding
This study was supported by the BJAST Budding Talent Program (Grant No. 24CE-BGS-19), the National Natural Science Foundation of China (No. 32370010), and the Beijing Government.
Institutional Review Board Statement
Not applicable.
Data Availability Statement
The sequencing data have been submitted to GenBank.
Acknowledgments
We thank the three anonymous reviewers for their suggestions and corrections to improve this paper.
Conflicts of Interest
The authors declare no conflicts of interest.
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Table 1.
Sources of specimens and GenBank accession numbers for sequences used in this study. Chinese sequences from basidiomates are in bold, and newly generated sequences are in red.
Table 1.
Sources of specimens and GenBank accession numbers for sequences used in this study. Chinese sequences from basidiomates are in bold, and newly generated sequences are in red.
| Taxon Name in Analysis | Taxon Name | Collection | Country | GenBank Accession Number | |
|---|---|---|---|---|---|
| ITS | nrLSU | ||||
| Anamika lactariolens AY818352 | Anamika lactariolens | taxon:301353 | AY818352 | - | |
| Anamika lactariolens NR_119524 | Anamika lactariolens | HC 88/95 | NR_119524 | - | |
| Hymenogaster arenarius BJTC FAN786 China | Hymenogaster arenarius | BJTC FAN786 | China | PP467413 | PP467449 |
| Hymenogaster arenarius BJTC FAN856 China | Hymenogaster arenarius | BJTC FAN856 | China | PP467414 | PP467450 |
| Hymenogaster arenarius GU479233 Germany | Hymenogaster arenarius | it10_26_2 | Germany | GU479233 | - |
| Hymenogaster arenarius GU479272 Germany | Hymenogaster arenarius | it5_2 | Germany | GU479272 | - |
| Hymenogaster arenarius GU479278 Germany | Hymenogaster arenarius | it6_3 | Germany | GU479278 | - |
| Hymenogaster bulliardii GU479261 Germany | Hymenogaster bulliardii | it20_4 | Germany | GU479261 | - |
| Hymenogaster bulliardii GU479262 Germany | Hymenogaster thwaitesii | it20_4_1 | Germany | GU479262 | - |
| Hymenogaster cf. niveus MT005942 Germany | Hymenogaster xxx | KR-M-0044217 | Germany | MT005942 | - |
| Hymenogaster cf. niveus MT005967 Germany | Hymenogaster niveus c ‘ryptic species 3’ | KR-M-0044314 | Germany | MT005967 | - |
| Hymenogaster cf. rehsteineri MT005990 Germany | Hymenogaster rehsteineri | KR-M-0044423 | Germany | MT005990 | - |
| Hymenogaster citrinus BJTC FAN1079 China | Hymenogaster citrinus | BJTC FAN1079 | China | PP467412 | PP467448 |
| Hymenogaster citrinus BJTC FAN883 China | Hymenogaster citrinus | BJTC FAN883 | China | PP467410 | PP467446 |
| Hymenogaster citrinus BJTC FAN915 China | Hymenogaster citrinus | BJTC FAN915 | China | PP467411 | PP467447 |
| Hymenogaster glacialis AF325634 | Hymenogaster sp. | GP 5302 | - | AF325634 | - |
| Hymenogaster griseus AF325636 USA | Hymenogaster griseus 2 | Trappe 12841 | USA | AF325636 | - |
| Hymenogaster knappii GU479287 Germany | Hymenogaster thwaitesii | it9_2 | Germany | GU479287 | - |
| Hymenogaster latisporus BJTC FAN1134 China | Hymenogaster latisporus | BJTC FAN1134, holotype | China | PP467404 | PP467440 |
| Hymenogaster luteus cf. trigonospora GU479306 Hungary | Hymenogaster luteus | zb1457 | Hungary | GU479306 | - |
| Hymenogaster luteus GU479341 Hungary | Hymenogaster luteus | zb2603 | Hungary | GU479341 | - |
| Hymenogaster luteus var. berkeleyanus GU479273 Germany | Hymenogaster bulliardii | it5_21 | Germany | GU479273 | - |
| Hymenogaster luteus var. subfuscus GU479358 Hungary | Hymenogaster griseus 2 | zb37 | Hungary | GU479358 | - |
| Hymenogaster luteus var. trigonospora GU479334 Hungary | Hymenogaster luteus | zb235 | Hungary | GU479334 | - |
| Hymenogaster lycoperdineus GU479353 Hungary | Hymenogaster griseus 2 | zb3533 | Hungary | GU479353 | - |
| Hymenogaster megasporus GU479239 Germany | Hymenogaster megasporus | it12_1 | Germany | GU479239 | - |
| Hymenogaster megasporus GU479286 Germany | Hymenogaster megasporus | it8_5_1 | Germany | GU479286 | - |
| Hymenogaster minisporus BJTC FAN1244 China | Hymenogaster minisporus | BJTC FAN1244, holotype | China | PP467407 | PP467443 |
| Hymenogaster niveus GU479255 Germany | Hymenogaster niveus c ‘ryptic species 1’ | it17_3 | Germany | GU479255 | - |
| Hymenogaster niveus GU479307 Hungary | Hymenogaster xxx | zb1461 | Hungary | GU479307 | - |
| Hymenogaster niveus GU479344 Hungary | Hymenogaster niveus c ‘ryptic species 3’ | zb28 | Hungary | GU479344 | - |
| Hymenogaster niveus KU878613 USA | Hymenogaster xxx | SC14_3 | USA | KU878613 | - |
| Hymenogaster olivaceus GU479292 Belgium | Hymenogaster citrinus | dt8293 | Belgium | GU479292 | - |
| Hymenogaster olivaceus GU479313 Hungary | Hymenogaster citrinus | zb1645 | Hungary | GU479313 | - |
| Hymenogaster olivaceus GU479317 Hungary | Hymenogaster citrinus | zb1817 | Hungary | GU479317 | - |
| Hymenogaster olivaceus GU479332 Hungary | Hymenogaster citrinus | zb2300 | Hungary | GU479332 | - |
| Hymenogaster olivaceus GU479345 Hungary | Hymenogaster thwaitesii | zb2804 | Hungary | GU479345 | - |
| Hymenogaster olivaceus GU479359 Hungary | Hymenogaster luteus | zb3721 | Hungary | GU479359 | - |
| Hymenogaster papilliformis BJTC FAN1002 China | Hymenogaster papilliformis | BJTC FAN1002 | China | PP467396 | PP467432 |
| Hymenogaster papilliformis BJTC FAN1070 China | Hymenogaster papilliformis | BJTC FAN1070 | China | PP467399 | PP467435 |
| Hymenogaster papilliformis BJTC FAN1074 China | Hymenogaster papilliformis | BJTC FAN1074, holotype | China | PP467400 | PP467436 |
| Hymenogaster papilliformis BJTC FAN1109 China | Hymenogaster papilliformis | BJTC FAN1109 | China | PP467402 | PP467438 |
| Hymenogaster papilliformis BJTC FAN1156 China | Hymenogaster papilliformis | BJTC FAN1156 | China | PP467406 | PP467442 |
| Hymenogaster papilliformis BJTC FAN1266 China | Hymenogaster papilliformis | BJTC FAN1266 | China | PP467408 | PP467444 |
| Hymenogaster papilliformis BJTC FAN1267 China | Hymenogaster papilliformis | BJTC FAN1267 | China | PP467409 | PP467445 |
| Hymenogaster papilliformis BJTC FAN655 China | Hymenogaster papilliformis | BJTC FAN655 | China | PP467381 | PP467417 |
| Hymenogaster papilliformis BJTC FAN807 China | Hymenogaster papilliformis | BJTC FAN807 | China | PP467384 | PP467420 |
| Hymenogaster papilliformis BJTC FAN820 China | Hymenogaster papilliformis | BJTC FAN820 | China | PP467385 | PP467421 |
| Hymenogaster papilliformis BJTC FAN891 China | Hymenogaster papilliformis | BJTC FAN891 | China | PP467388 | PP467424 |
| Hymenogaster papilliformis BJTC FAN944 China | Hymenogaster papilliformis | BJTC FAN944 | China | PP467389 | PP467425 |
| Hymenogaster papilliformis BJTC FAN958 China | Hymenogaster papilliformis | BJTC FAN958 | China | PP467391 | PP467427 |
| Hymenogaster papilliformis BJTC FAN960 China | Hymenogaster papilliformis | BJTC FAN960 | China | PP467392 | PP467428 |
| Hymenogaster papilliformis BJTC FAN980 China | Hymenogaster papilliformis | BJTC FAN980 | China | PP467393 | PP467429 |
| Hymenogaster papilliformis BJTC FAN983 China | Hymenogaster papilliformis | BJTC FAN983 | China | PP467394 | PP467430 |
| Hymenogaster papilliformis BJTC FAN992 China | Hymenogaster papilliformis | BJTC FAN992 | China | PP467395 | PP467431 |
| Hymenogaster parksii AF325638 USA | Hymenogaster gardneri | Trappe 13296 | USA | AF325638 | - |
| Hymenogaster parksii JN022510 USA | Hymenogaster gardneri | SOC1643 | USA | JN022510 | - |
| Hymenogaster perisporius BJTC FAN1038 China | Hymenogaster perisporius | BJTC FAN1038 | China | PP467397 | PP467433 |
| Hymenogaster perisporius BJTC FAN1049 China | Hymenogaster perisporius | BJTC FAN1049 | China | PP467398 | PP467434 |
| Hymenogaster perisporius BJTC FAN1076 China | Hymenogaster perisporius | BJTC FAN1076 | China | PP467401 | PP467437 |
| Hymenogaster perisporius BJTC FAN1126 China | Hymenogaster perisporius | BJTC FAN1126 | China | PP467403 | PP467439 |
| Hymenogaster perisporius BJTC FAN606 China | Hymenogaster perisporius | BJTC FAN606 | China | PP467379 | PP467415 |
| Hymenogaster perisporius BJTC FAN651 China | Hymenogaster perisporius | BJTC FAN651, holotype | China | PP467380 | PP467416 |
| Hymenogaster perisporius BJTC FAN768 China | Hymenogaster perisporius | BJTC FAN768 | China | PP467383 | PP467419 |
| Hymenogaster perisporius BJTC FAN846 China | Hymenogaster perisporius | BJTC FAN846 | China | PP467386 | PP467422 |
| Hymenogaster perisporius BJTC FAN850 China | Hymenogaster perisporius | BJTC FAN850 | China | PP467387 | PP467423 |
| Hymenogaster perisporius BJTC FAN952 China | Hymenogaster perisporius | BJTC FAN952 | China | PP467390 | PP467426 |
| Hymenogaster populetorum GU479252 Germany | Hymenogaster griseus 1 | it16_1_1 | Germany | GU479252 | - |
| Hymenogaster populetorum GU479289 Hungary | Hymenogaster griseus 1 | aszodvt_1991 | Hungary | GU479289 | - |
| Hymenogaster populetorum GU479304 Hungary | Hymenogaster griseus 1 | zb1436 | Hungary | GU479304 | - |
| Hymenogaster populetorum GU479327 Hungary | Hymenogaster griseus 2 | zb2097 | Hungary | GU479327 | - |
| Hymenogaster populetorum GU479328 Hungary | Hymenogaster griseus 2 | zb2105 | Hungary | GU479328 | - |
| Hymenogaster populetorum GU479340 Hungary | Hymenogaster griseus 1 | zb2576 | Hungary | GU479340 | - |
| Hymenogaster populetorum GU479356 Hungary | Hymenogaster griseus 2 | zb3594 | Hungary | GU479356 | - |
| Hymenogaster populetorum JF908082 Italy | Hymenogaster griseus 2 | 17022 | Italy | JF908082 | - |
| Hymenogaster pruinatus GU479242 Germany | Hymenogaster huthii | it12_3_1 | Germany | GU479242 | - |
| Hymenogaster pruinatus GU479308 Hungary | Hymenogaster bulliardii | zb1485 | Hungary | GU479308 | - |
| Hymenogaster pruinatus GU479366 Hungary | Hymenogaster huthii | zb95 | Hungary | GU479366 | - |
| Hymenogaster pseudoniveus BJTC FAN874 China | Hymenogaster pseudoniveus | BJTC FAN874 | China | PP622380 | PP622367 |
| Hymenogaster pseudoniveus BJTC FAN916 China | Hymenogaster pseudoniveus | BJTC FAN916 | China | PP622383 | PP622370 |
| Hymenogaster pseudoniveus BJTC FAN967 China | Hymenogaster pseudoniveus | BJTC FAN967 | China | PP622382 | PP622369 |
| Hymenogaster pseudoniveus BJTC FAN1069 China | Hymenogaster pseudoniveus | BJTC FAN1069 | China | PP622379 | PP622366 |
| Hymenogaster pseudoniveus BJTC FAN1075 China | Hymenogaster pseudoniveus | BJTC FAN1075, holotype | China | PP622378 | PP622365 |
| Hymenogaster pseudoniveus BJTC FAN1238 China | Hymenogaster pseudoniveus | BJTC FAN1238 | China | PP622384 | - |
| Hymenogaster pseudoniveus BJTC FAN1251 China | Hymenogaster pseudoniveus | BJTC FAN1251 | China | PP622381 | PP622368 |
| Hymenogaster rehsteineri GU479259 Germany | Hymenogaster rehsteineri | it2_4_1 | Germany | GU479259 | - |
| Hymenogaster rehsteineri GU479293 Luxembourg | Hymenogaster rehsteineri | dt8455 | Luxembourg | GU479293 | - |
| Hymenogaster rehsteineri MT005953 Germany | Hymenogaster rehsteineri | KR-M-0044018 | Germany | MT005953 | - |
| Hymenogaster rubyensis AY945303 USA | Hymenogaster sp. | Fogel 2698 | USA | AY945303 | - |
| Hymenogaster sp. MK027200 Slovenia | Hymenogaster niveus c ‘ryptic species 1’ | FV4_04 | Slovenia | MK027200 | - |
| Hymenogaster subalpinus AF325640 USA | Hymenogaster gardneri | Trappe 22752 | USA | AF325640 | - |
| Hymenogaster tener EU784363 UK | Hymenogaster tener | RBG Kew K(M)102406 | UK | EU784363 | - |
| Hymenogaster tener GU479250 Germany | Hymenogaster tener | it15_3 | Germany | GU479250 | - |
| Hymenogaster tener GU479253 Germany | Hymenogaster intermedius | it16_2, holotype | Germany | GU479253 | - |
| Hymenogaster thwaitesii GU479258 Germany | Hymenogaster thwaitesii | it2_2 | Germany | GU479258 | - |
| Hymenogaster thwaitesii GU479264 Germany | Hymenogaster thwaitesii | it3_2 | Germany | GU479264 | - |
| Hymenogaster variabilis BJTC FAN1141 China | Hymenogaster variabilis | BJTC FAN1141 | China | PP467405 | PP467441 |
| Hymenogaster variabilis BJTC FAN656 China | Hymenogaster variabilis | BJTC FAN656, holotype | China | PP467382 | PP467418 |
| Hymenogaster vulgaris EU784365 | Hymenogaster rehsteineri c ‘ryptic species 3’ | RBG Kew K(M)27363 | - | EU784365 | - |
| Hymenogaster vulgaris JQ724028 Sweden | Hymenogaster rehsteineri c ‘ryptic species 3’ | GN_4d_I | Sweden | JQ724028 | - |
| Hymenogaster zunhuaensis BJTC FAN1061 China | Hymenogaster zunhuaensis | BJTC FAN1061 | China | PP622373 | PP622361 |
| Hymenogaster zunhuaensis BJTC FAN1062 China | Hymenogaster zunhuaensis | BJTC FAN1062, holotype | China | PP622376 | PP622363 |
| Hymenogaster zunhuaensis BJTC FAN1083 China | Hymenogaster zunhuaensis | BJTC FAN1083 | China | PP622374 | PP622362 |
| Hymenogaster zunhuaensis BJTC FAN1105 China | Hymenogaster zunhuaensis | BJTC FAN1105 | China | PP622372 | PP622360 |
| Hymenogaster zunhuaensis BJTC FAN1162 China | Hymenogaster zunhuaensis | BJTC FAN1162 | China | PP622375 | - |
| Hymenogaster zunhuaensis BJTC FAN1249 China | Hymenogaster zunhuaensis | BJTC FAN1249 | China | PP622377 | PP622364 |
| Hymenogaster zunhuaensis BJTC FAN1259 China | Hymenogaster zunhuaensis | BJTC FAN1259 | China | PP622371 | PP622359 |
| Uncultured Agaricales HM105539 China | Hymenogaster minisporus | QL054 | China | HM105539 | - |
| Uncultured fungus EU554705 Canada | Hymenogaster sp. | A2N_88 | Canada | EU554705 | - |
| Uncultured fungus EU554717 Canada | Hymenogaster sp. | A3E_60 | Canada | EU554717 | - |
| Uncultured Hymenogaster LT980461 China | Hymenogaster minisporus | taxon:522720 | China | LT980461 | - |
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Li, T.; Mao, N.; Fu, H.; Zhang, Y.; Fan, L. Two New Species of Hymenogaster (Hymenogastraceae, Agaricales) from China Based on Morphological and Molecular Markers. Diversity 2024, 16, 303. https://doi.org/10.3390/d16050303
AMA Style
Li T, Mao N, Fu H, Zhang Y, Fan L. Two New Species of Hymenogaster (Hymenogastraceae, Agaricales) from China Based on Morphological and Molecular Markers. Diversity. 2024; 16(5):303. https://doi.org/10.3390/d16050303
Chicago/Turabian StyleLi, Ting, Ning Mao, Haoyu Fu, Yuxin Zhang, and Li Fan. 2024. "Two New Species of Hymenogaster (Hymenogastraceae, Agaricales) from China Based on Morphological and Molecular Markers" Diversity 16, no. 5: 303. https://doi.org/10.3390/d16050303
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