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17 May 2024

Two New Species of Hymenogaster (Hymenogastraceae, Agaricales) from China Based on Morphological and Molecular Markers

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,
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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.
Diversity2024, 16(5), 303;https://doi.org/10.3390/d16050303
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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).
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.

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.
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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”.
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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.
Diversity 16 00303 g003
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 fresh2
1. Basidiome earth yellow to yellow brown when fresh6
2. Gleba reddish brown to brown when fresh3
2. Gleba light brown when freshH. minisporus
3. Basidiospores length >17 μm4
3. Basidiospores length ≤17 μm5
4. Basidiospores 21–25.5 × 14–18.5 μmH. citrinus
4. Basidiospores 17–22 × 12–15 μmH. perisporius
5. Basidiospores 10–13.5 × 8–11.5 μmH. zunhuaensis
5. Basidiospores 13–17 × 10–13 μm H. pseudoniveus
6. Peridium exhibits substantial variation in thickness, differing by at least 120 μm7
6. Peridium exhibits substantial variation in thickness, differing by at the most 120 μm8
7. Basidiospores broad ellipsoidal to subglobose, Q = 1.1–1.3H. variabilis
7. Basidiospores broad fusiform to broad citriform, Q = 1.3–1.4H. papilliformis
8. Basidiospores fusiform, Q = 1.2–1.4H. arenarius
8. Basidiospores broadly ellipsoidal to subglobose, Q = 1.1–1.3H. 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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