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Article

Austroboletus brunneisquamus (Boletaceae, Boletales), a New Ectomycorrhizal Fungus from a Tropical Rainforest, China

1
Key Laboratory of Tropical Translational Medicine of Ministry of Education, Transgenic Laboratory, School of Pharmacy, Hainan Medical University, Haikou 571199, China
2
College of Science, Hainan University, Haikou 570228, China
3
Key Laboratory of Prevention and Treatment of Cardiovascular and Cerebrovascular Diseases of Ministry of Education, Gannan Medical University, Ganzhou 341000, China
4
Yinggeling Branch of Hainan Tropical Rainforest National Park, Baisha 572800, China
*
Authors to whom correspondence should be addressed.
Forests 2021, 12(11), 1438; https://doi.org/10.3390/f12111438
Received: 3 September 2021 / Revised: 5 October 2021 / Accepted: 19 October 2021 / Published: 22 October 2021

Abstract

:
Austroboletusbrunneisquamus (Boletaceae/Boletales), an ectomycorrhizal fungus, is described as a new species from a tropical rainforest in China based on morphological and molecular evidence. It is morphologically characterized by a subtomentose pileal surface when young, which cracks into areolae, having large, pale brown and brown to dark brown scales, a stipe with yellowish brown reticulation, basidiospores measuring (11–)12–14.5(–15) × 6–8(–8.5) μm, with fine cristate to subreticulate ornamentation, and a pileipellis in the form of a cutis. A detailed description, color photographs of fresh basidiomata, and line drawings of microscopic features of the new species are presented.

1. Introduction

Austroboletus (Corner) Wolfe (Boletaceae, Boletales), typified by A. dictyotus (Boedijn) Wolfe, is characterized by a pinkish pore surface at maturity, context usually unchanging in color when injured, a stipe, often with conspicuous reticulation, fusiform or amygdaliform basidiospores with verrucose, warted, irregularly pitted, cristate, subcylindrical, ridged or subreticulate ornamentations, and forming ectomycorrhizae with Fagaceae, Pinaceae and Dipterocarpaceae [1,2,3,4,5]. Species of Austroboletus are mostly distributed in tropical regions [6,7,8,9,10,11]. In China, five taxa of the genus, viz. A. dictyotus, A. fusisporus (Kawam. ex Imazeki & Hongo) Wolfe, A. gracilis (Peck) Wolfe, A. malaccensis (Pat. & C.F. Baker) Wolfe and A. subvirens (Hongo) Wolfe were reported in previous studies [1,12,13,14,15]. Hainan, a tropical area covered mostly by rainforests, is considered as a hotspot of biodiversity, and many new taxa of macrofungi were described from the region in the past [16,17,18,19,20,21,22,23,24,25]. With further investigations, more new taxa are expected to be uncovered. During a fieldtrip to the area, we encountered a few collections of Austroboletus. Subsequent morphological and molecular phylogenetic analyses confirmed that it is different from all known species of Austroboletus, and thus we describe these collections as a new species.

2. Materials and Methods

2.1. Morphological Studies

Collections were described and photographed in the field and deposited in the Fungal Herbarium of Hainan Medical University, Haikou City, Hainan Province of China (FHMU). Color codes are from Kornerup and Wanscher [26]. Sections of the pileipellis were cut radial-perpendicularly and halfway between the center and the margin of the pileus. Sections of the stipitipellis were taken from the middle part along the longitudinal axis of the stipe. As a mounting medium for microscopic studies, 5% KOH was used. All microscopic structures were drawn freehand from rehydrated material. The number of measured basidiospores is given as n/m/p, where n represents the total number of basidiospores measured from m basidiomata of p collections. Dimensions of basidiospores are given as (a–)b–c(–d), where the range b–c represents a minimum of 90% of the measured values (5th to 95th percentile), and extreme values (a and d), whenever present (a < 5th percentile, d > 95th percentile), are in parentheses. Q refers to the length/width ratio of basidiospores; Qm refers to the average Q of basidiospores and is given with a sample standard deviation [19,20]. Basidiospores from dried specimens were also examined with a FEI Quanta 250 (USA) scanning electron microscope (SEM) [27].

2.2. Molecular Procedures

Total genomic DNA was obtained with the Plant Genomic DNA Kit (KANGWEI Company, China) from materials dried with silica gel according to the manufacturer’s instructions. Primer pairs used for amplification were: LR0R/LR5 [28,29] for the nuclear ribosomal large subunit RNA (28S), the nuclear rDNA region encompassing the internal transcribed spacers 1 and 2, along with the 5.8S rDNA (ITS), with ITS5/ITS4 [30], and EF1-2F/EF1-2R [27] for the translation elongation factor 1-α gene (TEF1). PCR was performed in a total volume of 25 μL containing 13 μL 2 × Taq PCR MasterMix (KANGWEI Company, China), 2 μL per primer (10 mM), 2 μL DNA template and 8 μL nuclease-free water. PCR reactions were performed with 4 min initial denaturation at 95°, followed by 35 cycles of denaturation at 94° for 30 s, annealing at an appropriate temperature (50° for 28S and ITS, 53° for TEF1) for 30 s, extension at 72° for 120 s and a final extension at 72° for 7 min. PCR products were checked in 1% (w/v) agarose gels, and positive reactions with a bright single band were purified and directly sequenced using an ABI 3730xl DNA Analyzer (Guangzhou Branch of BGI, China) with the same primers used for PCR amplifications [19,20]. BioEdit [31] was used to compile forward or reverse sequences.

2.3. Dataset Assembly

Five DNA sequences (two of 28S, two of ITS, and one of TEF1) from two specimens were newly generated. Mucilopilus castaneiceps Hongo was chosen as an outgroup following Wu et al. [1]. To test for phylogenetic conflict among the different genes in the combined dataset, the single-gene phylogenetic trees based on 28S, ITS and TEF1, respectively, were analyzed and conducted using the ML method to detect the topologies of genes used. The results of analyses showed that the different gene fragments were not in conflict. Then, the sequences of different genes in the combined dataset were aligned using MUSCLE. The sequences of the different genes were concatenated using Phyutility v. 2.2 for further analyses [19,20] (Table 1).

2.4. Phylogenetic Analyses

The combined nuclear dataset (28S + ITS + TEF1) was analyzed with maximum likelihood (ML) and Bayesian Inference (BI). Maximum likelihood tree generation and bootstrap analyses were performed with the program RAxML 7.2.6 running 1000 replicates combined with an ML search. Bayesian analysis with MrBayes 3.1 implementing the Markov Chain Monte Carlo (MCMC) technique and parameters predetermined with MrModeltest 2.3 was performed [19,20]. The best-fit likelihood models for the combined dataset were GTR + I + G, GTR + I + G and SYM + G for 28S, ITS and TEF1, respectively. Bayesian analysis of the combined nuclear dataset (28S + ITS + TEF1) was repeated for 10 million generations. Trees sampled from the first 25% of generations were discarded as burn-in, and Bayesian posterior probabilities (PP) were then calculated for a majority consensus tree of the retained Bayesian trees [19,20].

3. Results

3.1. Molecular Data

The combined dataset (28S + ITS + TEF1) included 81 taxa with 2225 nucleotide sites, and the alignment was deposited in TreeBASE (S27641). Bayesian analyses resulted in identical topologies to the ML analysis, while statistical supports showed slight differences. Figure 1 is a branch-length phylogram with the support values, and inferred with RAxML. The molecular phylogenetic analyses show that the collections numbered FHMU5875 and FHMU5876 grouped together with a strong statistical support (BS = 99, PP = 1.0), forming an independent lineage within Austroboletus (Figure 1).

3.2. Taxonomy

Austroboletus brunneisquamus N.K. Zeng, Chang Xu and S. Jiang, sp. nov. (Figure 2, Figure 3 and Figure 4).
Mycobank: MB838577
Etymology—Latin “brunneisquamus” refers to the pileus of new species displaying distinctive brown scales.
Diagnosis—Characterized by a subtomentose pileal surface when young, which cracks into into areolae, with large, pale brown and brown to dark brown scales, a stipe with yellowish brown reticulation, basidiospores measuring (11–)12–14.5(–15) × 6–8(–8.5) μm, with fine cristate to subreticulate ornamentation, and a cutis in form of pileipellis.
Holotype—CHINA. Hainan Province: Ledong County, Yinggeling of Hainan Tropical Rainforest National Park, 109°17′17″ E, 18°51′6″ N, elev. 650 m, 2 July 2020, N.K. Zeng4294 (FHMU5876). GenBank accession numbers: 28S = MW506829, ITS = MZ855495, TEF1 = MW512637.
DescriptionBasidiomata: small to medium-sized. Pileus: 3–6.5 cm in diam, subhemispherical when young, then convex to applanate; margin: decurved; surface: dry, subtomentose when young, which cracks into areolae, with large, pale brown (3C7–8) and brown to dark brown (5E7–8) scales; context: 0.5–1.2 cm thick in the center of the pileus, white (1A1), unchanging in color when injured. Hymenophore: poroid, depressed around the stipe; pores: subrounded, white (1A1) when young, then pink (8A2), unchanging in color when injured; tubes: 0.6–1.5cm in length, pinkish (9A2), unchanging in color when injured. Stipe: 4.5–9 × 0.7–1.4 cm, central, subcylindrical, solid; surface: distinctly covered with a yellowish brown (4B5–6) reticulation; context: white (1A1), unchanging in color when injured; basal mycelium: white (1A1). Odor: indistinct.
Basidiospores: [60/3/3] (11–)12–14.5(–15) × 6–8(–8.5) μm, Q = (1.57–)1.60–2.00 (–2.17), Qm = 1.80 ± 0.14 (including ornamentation), [60/3/3] (9–)11–13.5(–14.5) × 4–6 (–6.5) μm, Q = (1.8–)1.92–2.78 (–3.25), Qm = 2.37 ± 0.29 (excluding ornamentation), fusiform or amygdaliform, with a fine cristate to subreticulate ornamentation, pale yellowish brown in KOH. Basidia: 18–26 × 11–15 μm, broadly clavate, thin to slightly thick-walled (up to 0.7 μm), 4-spored, colorless in KOH; sterigmata: 4–6 μm long. Cheilocystidia: 27–54 × 7–14 μm, abundant, fusiform or subfusiform, slightly thick-walled (up to 0.9 μm), colorless in KOH. Pleurocystidia: 27–62 × 4–12 μm, mostly fusiform, occasionally subclavate or subcylindrical, slightly thick-walled (up to 0.9 μm), colorless in KOH. Pileipellis: a cutis up to 315 μm thick, composed of cylindrical hyphae 6.5–13 μm wide, occasionally branched, slightly thick-walled (up to 0.9 μm), colorless in KOH; terminal cells: 44–64 × 6–10.5 μm, subcylindrical, with obtuse apex. Pileal trama: made up of hyphae 4–12 μm in diam, slightly thick-walled (up to 0.9 μm), colorless in KOH. Stipitipellis: a trichoderm-like structure, 70–105 μm thick, composed of slightly thick-walled (up to 0.9 μm) hyphae, 5.5–7.5 μm wide, colorless in KOH; terminal cells: 24.5–53 × 6–6.5 μm, clavate, subclavate or subcylindrical. Stipe trama: composed of parallel hyphae, 4–15 μm wide, cylindrical, slightly thick-walled (up to 0.9 μm), colorless in KOH. Clamp connections: absent in all tissues.
Habitat—solitary on the ground in tropical rainforests dominated by fagaceous trees.
Known distribution—Southern China (Hainan Province).
Additional specimens examined—CHINA. Hainan Province: Ledong County, Yinggeling of Hainan Tropical Rainforest National Park, elev. 650 m, 2 July 2020, N.K.Zeng4291, 4292 (FHMU5874, 5875).

4. Discussion

In the present study, our newly collected specimens were placed into the genus Austroboletus with high statistical support (Figure 1), and morphological features of A. brunneisquamus are highly compatible with the typical characteristics of the genus.
Phylogenetically, A. brunneisquamus is related to A. appendiculatus Semwal, D. Chakr., K. Das, Indoliya, D. Chakrabarty and S. Adhikari & Karun. However, A. appendiculatus, a species originally described from India [42], has a distinctively larger pileus (7.5–9 cm) with a yellowish orange to grayish yellow surface, a longer stipe (8–12 cm), and large basidiospores measuring 14.2–16.5 × 7.3–9.1 μm, and it is associated with Dipterocarpaceae trees [42]. Moreover, A. brunneisquamus is also morphologically similar to A. dictyotus, A. fusisporus and A. subflavidus (Murrill) Wolfe. However, A. dictyotus, originally discovered in Indonesia, has a larger basidioma (pileus up to 11 cm), larger basidiospores measuring (11–)13–16 × (6–)7–8.5 μm with reticulations, and a pileipellis in the form of a trichoderm [1,2]; A. fusisporus, originally discovered in Japan, has a smaller pileus with a viscid surface, large basidiospores measuring 13.5–18.5 × 8–11 μm with subcylindrical ornamentation, and a trichodermium pileipellis [1,43]; A. subflavidus has longer basidiospores measuring 13.1–19.5 × 5.5–8.7 μm with Qm = 2.26, a pileipellis in the form of a trichoderm, and a distribution in North America–Central America–northern South America [5]. Molecular evidence provided in this study also indicated that A. brunneisquamus is genetically distant from A. dictyotus and A. fusisporus, respectively, and it is somewhat related to A. subflavidus, as these two taxa belong to the same clade (not species level) (Figure 1).

Author Contributions

Conceptualization, Z.-Q.L. and N.-K.Z.; Methodology, C.X. and M.-S.S.; Performing the experiment, C.X.; Formal analysis, C.X. and Z.-Q.L.; Resources, N.-K.Z., S.J., Y.C. and Y.-G.F.; Writing—original draft preparation, C.X.; Writing—review and editing, Z.-Q.L. and N.-K.Z.; Supervision, N.-K.Z.; Project administration, N.-K.Z.; Funding acquisition, N.-K.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the Hainan Provincial Natural Science Foundation of China (no. 820RC633), and the National Natural Science Foundation of China (nos. 31760008 and 31560005).

Data Availability Statement

The sequence data generated in this study are deposited in NCBI GenBank.

Acknowledgments

The first author is very grateful to Hui-Jing Xie, Xu Zhang, and Yu-Zhuo Zhang, Hainan Medical University, for their help with molecular data analyses, and the forest rangers, Yinggeling Branch of Hainan Tropical Rainforest National Park, China, for their kind help during the field investigations.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

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Figure 1. Phylogram inferred from a combined dataset (28S, ITS and TEF1) using RAxML. RAxML likelihood bootstrap (BS ≥ 50%) and Bayesian posterior probabilities (PP ≥ 0.95) are indicated above or below the branches as RAxML BS/PP.
Figure 1. Phylogram inferred from a combined dataset (28S, ITS and TEF1) using RAxML. RAxML likelihood bootstrap (BS ≥ 50%) and Bayesian posterior probabilities (PP ≥ 0.95) are indicated above or below the branches as RAxML BS/PP.
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Figure 2. Basidiomata of Austroboletus brunneisquamus ((a) from FHMU5875; (b,c) from FHMU5876, holotype). Photos by Y.G. Fan.
Figure 2. Basidiomata of Austroboletus brunneisquamus ((a) from FHMU5875; (b,c) from FHMU5876, holotype). Photos by Y.G. Fan.
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Figure 3. Microscopic features of Austroboletus brunneisquamus (FHMU5876, holotype). (a) Basidiospores. (b) Basidia. (c) Cheilocystidia. (d) Pleurocystidia. (e) Pileipellis. (f) Stipitipellis. Bars = 10 μm. Drawings by C. Xu.
Figure 3. Microscopic features of Austroboletus brunneisquamus (FHMU5876, holotype). (a) Basidiospores. (b) Basidia. (c) Cheilocystidia. (d) Pleurocystidia. (e) Pileipellis. (f) Stipitipellis. Bars = 10 μm. Drawings by C. Xu.
Forests 12 01438 g003
Figure 4. SEM of basidiospores from a dried specimen of Austroboletus brunneisquamus (FHMU5876, holotype). Bars = 5 μm.
Figure 4. SEM of basidiospores from a dried specimen of Austroboletus brunneisquamus (FHMU5876, holotype). Bars = 5 μm.
Forests 12 01438 g004
Table 1. List of collections used in this study.
Table 1. List of collections used in this study.
TaxonVoucherLocalityGenBank Accession No.References
28SITSTEF1
Austroboletus aff. fusisporusHKAS 53461Hunan, central ChinaKF112486KF112214[32]
Austroboletus aff. rostrupiiG4357GuyanaKJ786636Unpublished
Austroboletus amazonicus2032 AMVColombiaKF714510KF937309[8]
A. amazonicus1839 AMVColombiaKF714508KF937307[8]
Austroboletus asperPerth 06658407AustraliaKP242277KP242216[4]
A.asperPerth 8018251AustraliaKP242267[4]
A. asperMEL:2104343AustraliaKP242260KP242174[4]
A. asperMEL:2300520AustraliaKP242253KP242186[4]
A. asperMEL:2371703AustraliaKP242152[4]
Austroboletus austrovirensBRI:AQ0796003AustraliaKP242228KP242212[10]
A. austrovirensBRI:AQ0795791AustraliaKP242225KP242211[10]
Austroboletus brunneisquamusN.K. Zeng 4292 (FHMU5875)Hainan, southern ChinaMW506828MZ855494This study
A. brunneisquamusN.K. Zeng 4294 (FHMU5876)Hainan, southern ChinaMW506829MZ855495MW512637This study
Austroboletus dictyotusHKAS59804ChinaJX901138[15]
A. dictyotusHKAS 53450Hunan, central ChinaKF112487KF112215[32]
Austroboletus festivusFLOR 51599BrazilKY888001KY886202[33]
A. festivusAMV1941ColombiaKT724096Unpublished
A. festivusFLOR 51601BrazilKY888000KY886203[33]
A. festivusAMV1881ColombiaKT724095KT724086Unpublished
A. festivusAMV1800ColombiaKT724085Unpublished
A. fusisporusHKAS75207ChinaJX889720JX889719JX889718[15]
Austroboletus gracilis112/96USADQ534624KF030425[34]
A. gracilisCNV35MT345212Unpublished
A. gracilisNAMA 2017-106USAMH979242Unpublished
A. gracilisMushroom Observer # 310751MexicoMH167935Unpublished
Austroboletus lacunosusBRI:AQ0795789AustraliaKP242271KP242162Unpublished
A. lacunosusREH9146AustraliaJX889669JX889709[35]
Austroboletus mucosusTH6300GuyanaAY612798[36]
Austroboletus mutabilisBRI:AQ0554121AustraliaKP242241KP242192Unpublished
A. mutabilisBRI:AQ0557644AustraliaKP242237KP242196Unpublished
Austroboletus neotropicalisNY181457Costa RicaJQ924334JQ924301Unpublished
Austroboletus niveusAD-C 54948AustraliaKP242280KP242220Unpublished
A. niveusPerth 6660703AustraliaKP242279KP242217Unpublished
A. niveusBRI:AQ0795772AustraliaKP242276KP242156Unpublished
A. niveusMEL2053830AustraliaKC552058KC552016KC552099Unpublished
A. niveusREH9487AustraliaJX889668JX889708[35]
A. niveusPDD:105246New ZealandMH594049Unpublished
Austroboletus novae-zelandiaeTL2578New ZealandKP191803Unpublished
A. novae-zelandiaePDD:105097New ZealandMH594051Unpublished
A. novae-zelandiaeMEL:2370154AustraliaKP242256KP242175Unpublished
Austroboletus rarusBRI:AQ0794045AustraliaKP242236KP242197Unpublished
A. rarusBRI:AQ0807888AustraliaKP242200Unpublished
Austroboletus rionegrensisINPA 78693BrazilKY886201[33]
Austroboletus roseialbusDoddAustraliaKY872650KY872653[10]
A. roseialbusREH10024AustraliaKY872651KY872652[10]
Austroboletus rostrupiiBRI:AQ0807886AustraliaKP242270KP242163Unpublished
A. rostrupiiBRI:AQ0796694AustraliaKP242258KP242179Unpublished
A. rostrupiiTH8189GuyanaJN168683[37]
Austroboletus sp.HKAS74743ChinaKT990527KT990730[1]
Austroboletus sp.MEL:2382826AustraliaKP242283KP242213Unpublished
Austroboletus sp.BRI:AQ0794271AustraliaKP242259Unpublished
Austroboletus sp.BRI:AQ0794258AustraliaKP242255KP242182Unpublished
Austroboletus sp.Perth 8019207AustraliaKP242245Unpublished
Austroboletus sp.BRI:AQ0794222AustraliaKP242234KP242215Unpublished
Austroboletus sp.MEL2305143New CaledoniaKC552060KC552018KC552101Unpublished
Austroboletus sp.CANB:643163AustraliaKP242201Unpublished
Austroboletus sp.BRI:AQ0794272AustraliaKP242159Unpublished
Austroboletus sp.HKAS 59624Yunnan, SW ChinaKF112485KF112217[32]
Austroboletus sp.HKAS 57756Jiangxi, eastern ChinaKF112383KF112212[32]
Austroboletus sp.OR0891ThailandMH614706[38]
Austroboletus sp.CM13_006New CaledoniaKY774009[39]
Austroboletus sp.CY13_008KY774008Unpublished
Austroboletus sp.CYMy36L1KY774007Unpublished
Austroboletus sp.LAM 0479MalaysiaKY091070Unpublished
Austroboletus sp.DD9852North AmericaAY612797Unpublished
Austroboletus subflavidusCFMR BZ-3178 BOS-625BelizeMK601716MK721070Unpublished; [40]
A. subflavidusFLAS-F-60635USAMH016816Unpublished
A. subflavidusJBSD130771Dominican
Republic
MT580902MT581525[5]
A. subflavidusJBSD130772Dominican
Republic
MT580903MT581526[5]
A. subflavidusCFMR:DR2859Dominican
Republic
MT580901MT581523[5]
A. subflavidusCFMR:DR592Dominican
Republic
MT581524[5]
A. subflavidusCFMR:BZ1824BelizeMT581522[5]
A. subflavidusCFMR:BOTH-3463Florida (USA)MT580900MT581521[5]
Austroboletus subvirensOTU1575JapanMT594990Unpublished
A. subvirensKPM-NC-0017836JapanJN378518JN378458[41]
A. subvirensMEL:2382920AustraliaKP012789Unpublished
Austroboletus viscidoviridisREH9993AustraliaKY872649[10]
A. viscidoviridisPerth 7588682AustraliaKP242282KP242219Unpublished
A. viscidoviridisBRI:AQ0554020AustraliaKP242243KP242189Unpublished
Mucilopilus castaneicepsHKAS50338ChinaKT990555KT990755[1]
M. castaneicepsHKAS71039ChinaKT990547KT990748[1]
New sequences are shown in bold.
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MDPI and ACS Style

Xu, C.; Liang, Z.-Q.; Su, M.-S.; Jiang, S.; Chen, Y.; Fan, Y.-G.; Zeng, N.-K. Austroboletus brunneisquamus (Boletaceae, Boletales), a New Ectomycorrhizal Fungus from a Tropical Rainforest, China. Forests 2021, 12, 1438. https://doi.org/10.3390/f12111438

AMA Style

Xu C, Liang Z-Q, Su M-S, Jiang S, Chen Y, Fan Y-G, Zeng N-K. Austroboletus brunneisquamus (Boletaceae, Boletales), a New Ectomycorrhizal Fungus from a Tropical Rainforest, China. Forests. 2021; 12(11):1438. https://doi.org/10.3390/f12111438

Chicago/Turabian Style

Xu, Chang, Zhi-Qun Liang, Ming-Sheng Su, Shuai Jiang, Yun Chen, Yu-Guang Fan, and Nian-Kai Zeng. 2021. "Austroboletus brunneisquamus (Boletaceae, Boletales), a New Ectomycorrhizal Fungus from a Tropical Rainforest, China" Forests 12, no. 11: 1438. https://doi.org/10.3390/f12111438

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