Skip to main content
NCBI home page
Fungal Systematics and Evolution logoLink to Fungal Systematics and Evolution
. 2019 Oct 11;5:119–129. doi: 10.3114/fuse.2020.05.07

Phylogenetic placement of Paratrichaptum and reconsideration of Gloeophyllales

C-C Chen 1, B Cao 2, T Hattori 3, B-K Cui 4, C-Y Chen 1, S-H Wu 1,5,*
PMCID: PMC7250016  PMID: 32467918

Abstract

Paratrichaptum accuratum is a large conspicuous polypore fungus growing on dead or living angiosperm trees in subtropical-boreal areas of China, Indonesia, Japan, and Taiwan. The present study places P. accuratum in the family Gloeophyllaceae that belongs to the order Gloeophyllales within Agaricomycetes (Basidiomycota), based on evidence derived from morphological and ecological characteristics, and phylogenetic analyses of sequences of nuclear rDNA regions (5.8S, nuc 18S, nuc 28S) and protein-coding genes (rpb1, rpb2, and tef1). The analyses presented in this study also give strong support for including Jaapia in Gloeophyllaceae and Gloeophyllales. Thus, the names Jaapiaceae and Jaapiales are considered here as synonyms of Gloeophyllaceae and Gloeophyllales. Since Paratrichaptum represents the earliest diverging lineage in Gloeophyllales, pileate basidiocarps and brown rot appear to be ancestral states of Gloeophyllales. Paratrichaptum accuratum may represent a relic species, according to its phylogenetic position, peculiar distribution pattern and rare occurrence.

Keywords: brown rot, eastern and southeastern Asia, systematics, taxonomy, wood-inhabiting fungi, new taxa

INTRODUCTION

The genus Paratrichaptum was described by Corner (1987) to accommodate a monotypic species, P. accuratum, a large conspicuous wood-inhabiting polypore fungus. This genus is characterised by a peculiar combination of morphological features. In macromorphology, it has a pileate and sessile basidiocarp that is soft-corky and spongy in the fresh condition, poroid to daedaleoid hymenophore, and brown tubes and context. Microscopically, it possesses a monomitic hyphal system, nodose-septate generative hyphae, fasciculate cystidia, and pale brown and smooth basidiospores with thin to slightly thick walls, which have a negative reaction in Melzer's reagent. Such a combination is fairly peculiar within the polypore fungi, sustaining its position as a distinct genus (Ryvarden 1991).

Paratrichaptum accuratum is hitherto known only from Asia (Ryvarden, 1991, Núñez & Ryvarden 2001) where it grows on hardwoods (Corner 1987, Núñez & Ryvarden 2001). The holotype was collected from a highland forest of Sumatra (Indonesia), 56 years before Corner's (1987) description. Recently, this species was discovered in subtropical to boreal regions of Japan (Hokkaido, Kagoshima, Nara, Yamagata) based on four specimens collected between 1989 and 1994 (Núñez & Ryvarden 2001, Hattori 2017). Núñez & Ryvarden (2001) reported this species from Taiwan based on a specimen collected in 1922.

According to MycoBank (Robert et al. 2005), P. accuratum is placed in the family Schizoporaceae, in the order Hymenochaetales. However, this placement was never examined through molecular phylogenetic analyses since sequence data related to this species are lacking. In 2017, two specimens of Paratrichaptum accuratum were collected during a field trip in southern Yunnan (China), which enabled us to study the higher-rank classification for this species.

To infer the placement of Paratrichaptum accuratum within Agaricomycetes, the present study conducted phylogenetic analyses based on sequences of nuc rDNA genes and three protein-coding genes. The results allowed us to discuss the limits of the orders Gloeophyllales and Jaapiales.

MATERIALS AND METHODS

Morphological studies

Voucher specimens are deposited at the herbaria of the Kunming Institute of Botany, Chinese Academy of Sciences of PRC (KUN), the Botanical Museum, University of Oslo of Norway (O), the Forestry and Forest Products Research Institute of Japan (TFM), and the National Museum of Natural Science of ROC (TNM). Abbreviations of herbaria follow those in the Index Herbariorum (http://sweetgum.nybg.org/science/ih/). Basidiocarps and the native habitat were photographed with an Olympus TG-4 or a Nikon D5300 digital camera. All microscopic characters were examined from dried specimens with a Leica DM2500 microscope. 5 % Potassium hydroxide (KOH) with 1 % phloxine was used for observation and measurement. Melzer's reagent was used to determine amyloidity and dextrinoidity. Cotton blue (Fluka 61335) was used as a mounting medium to check cyanophily. The following abbreviations were used for basidiospore measurements: L = mean basidiospore length with standard deviation, W = mean basidiospore width with standard deviation, Q = variation in L/W ratio, n = number of measured basidiospores from each specimen.

DNA extraction, PCR amplification, and DNA sequencing

Genomic DNA was extracted from dried specimens using a Plant Genomic DNA Extraction Miniprep System (Viogene, New Taipei, Taiwan), based on manufacturer's instructions. The sample was first homogenised with the aid of liquid nitrogen and a Tissue Lyser II (Qiagen, Hilden, Germany). We used primer pairs ITS1/ITS4 for nuc rDNA ITS1–5.8S-ITS2 (nuc ITS); PNS1/NS8 for nuc 18S rDNA (nuc 18S) (White et al. 1990); LR0R/LR5 for D1-D2 domains of nuc 28S rDNA (nuc 28S) (Moncalvo et al. 2000); RPB1-Int2f/RPB1-Cr for RNA polymerase II largest subunit (rpb1) (Frøslev et al. 2005); RPB2-f5F/RPB2-b7.1R for RNA polymerase II second largest (rpb2) (Liu et al. 1999, Matheny 2005); EF1–983F/EF11953R for translation elongation factor 1-α (tef1) (Rehner & Buckley 2005). The PCR conditions to amplify ITS, nuc 18S and nuc 28S gene regions were as follows: initial denaturation at 95 °C for 5 min, followed by 40 cycles at 94 °C for 45 s, 53 °C for ITS and 50 °C for the nuc 18S and nuc 28S for 45 s and 72 °C for 45 s and a final extension of 72 °C for 10 min. The protocols for amplifying rpb1, rpb2, and tef1 were performed as described in Chen et al. (2018). The PCR products were purified and sequenced by the MB Mission Biotech Company (Taipei, Taiwan). The newly obtained sequences were edited and assembled using BioEdit v. 7.2.5 (Hall 1999), and submitted to the DNA Data Bank of Japan (DDBJ) (Table 1).

Table 1.

Species and sequences used in the phylogenetic analyses. Newly generated sequences are set in bold

Classification Source Accession numbers
nr18S nr28S rpb1 rpb2 5.8S tef1
Agaricomycetes / Agaricales
Asterophora lycoperdoides CBS 170.86 AF223190 DQ367417 EF421021 DQ367431 AF357037 DQ367424
Coprinus comatus AFTOL-ID 626 AY635772 AY665772 AY857983 AY780934 AY854066 —
Gymnopilus picreus ZRL2015011 KY418882 KY418948 KY418980 KY419027 LT716066 KY419077
Gymnopus confluens ZRL20151148 KY418870 KY418936 — KY419016 LT716054 KY419070
Hydropus marginellus AFTOL-ID 1720 DQ457674 DQ444856 — DQ472722 DQ490627 —
Lepiota cristata ZRL20151133 KY418841 KY418910 — KY418992 LT716026 KY419048
Marasmius oreades ZRL2015086 KY418864 KY418930 KY418972 KY419010 LT716048 KY419066
Psathyrella candolleana ZRL20151400 KY418879 KY418945 KY418978 KY419024 LT716063 KY419075
Agaricomycetes / Amylocorticiales
Amylocorticium cebennense HHB-2808 GU187561 GU187612 GU187439 GU187770 GU187505 GU187675
Anomoloma myceliosum MJL-4413 GU187559 GU187614 GU187441 GU187766 GU187500 GU187677
Podoserpula ailaoshanensis ZJL2015015 KU324487 KU324491 — — KU324484 KU324494
Podoserpula pusio AFTOL-ID 1522 DQ470821 — — — DQ494688 —
Agaricomycetes / Atheliales
Athelia arachnoidea CBS 418.72 GU187557 GU187616 GU187436 GU187769 GU187504 GU187672
Leptosporomyces raunkiaerii HHB-7628 GU187588 GU187640 GU187471 GU187791 GU187528 —
Piloderma fallax S-12 GU187591 GU187644 — GU187797 GU187535 GU187738
Agaricomycetes / Auriculariales
Auricularia heimuer Xiaoheimao KY418890 — — KY419035 LT716074 KY419083
Exidia sp. PBM2527 AY700191 — — — DQ241774 DQ408144
Agaricomycetes / Boletales
Coniophora arida FP104367 GU187573 GU187622 GU187445 GU187775 GU187510 GU187684
Gomphidius roseus MB 95-038 DQ534669 DQ534682 GU187459 GU187818 DQ534570 GU187702
Gyrodontium sacchari MUCL40589 GU187579 GU187632 GU187460 GU187764 GU187522 GU187703
Leucogyrophana lichenicola DAOM194172 GU187583 GU187638 GU187467 GU187789 GU187531 GU187715
Serpula lacrymans REG-383 GU187596 GU187649 GU187485 GU187809 GU187542 GU187752
Suillus pictus MB03-093 AY684154 — AY858965 AY786066 AY854069 AY883429
Agaricomycetes / Cantharellales
Botryobasidium botryosum AFTOL-ID 604 DQ089013 AY662667 — — DQ267124 —
Hydnum repandum BB 07.341 KF294643 — — KF294720 — JX192980
Multiclavula mucida AFTOL-ID 1130 AY885163 — — — DQ521417 —
Agaricomycetes / Corticiales
Corticium roseum MG46 AY463401 — — — GU590877 —
Dendrothele maculata — AY586652 — — — AY463404 —
Punctularia strigosozonata AFTOL-ID 1248 AF518642 AF518586 DQ831031 DQ381843 DQ398958 DQ408147
Agaricomycetes / Geastrales
Geastrum recolligens OSC41996 DQ218486 — — DQ219052 — DQ219230
Pyrenogaster pityophilus OSC59743 DQ218519 — — DQ219057 — DQ219232
Agaricomycetes / Gloeophyllales
Boreostereum radiatum RLG-9717-sp HM536050 HM536051 — HM536101 HM536085 —
Chaetodermella luna NH 8482 EU118615 — — — — —
Gloeophyllum sepiarium Wilcox-3BB HM536061 HM536062 — — HM536091 HM536110
Gloeophyllum striatum ARIZAN027866 HM536063 HM536064 — — HM536092 —
Gloeophyllum subferrugineum FPRI-508 HM536065 HM536066 — — — —
Gloeophyllum trabeum 1320 HM536067 HM536068 — HM536112 HM536094 HM536113
Griseoporia carbonaria FP-97972-Sp HM536054 HM536055 — HM536104 — HM536105
Griseoporia taiwanense Dai 11560 KC782730 — — — JX524624 —
Heliocybe sulcata IBUG-9930 HM536069 HM536070 — HM536114 HM536095 HM536115
Hispidaedalea imponens He 1546 KC782742 — — — KC345726 —
Jaapia argillacea CBS 252.74 GU187581 AF518581 GU187463 GU187788 GU187524 GU187711
Jaapia ochroleuca MA-Fungi 23942 — — — — LN824166 —
Neolentinus adhaerens DAOM214911 — HM536072 — — HM536096 HM536117
Neolentinus kauffmanii DAOM214904 HM536073 HM536074 — — HM536097 HM536118
Neolentinus lepideus DAOM208724 HM536077 HM536078 — HM536121 — HM536122
Osmoporus mexicanum FP-104133-Sp HM536056 HM536057 — — HM536088 HM536106
Osmoporus odoratus Wu 0309-92 EF153195 — — — — —
Osmoporus protractum H-80 HM536059 HM536060 — HM536107 HM536090 HM536108
Paratrichaptum accuratum GC 1708-180 LC473734 LC473736 LC473738 LC473740 LC473732 LC473742
Paratrichaptum accuratum GC 1708-183 LC473735 LC473737 LC473739 LC473741 LC473733 LC473743
Veluticeps abietina GBB-398 HM536079 HM536080 — HM536123 — HM536124
Veluticeps berkeleyi HHB-8594 HM536081 HM536082 — HM536125 HM536099 —
Veluticeps fimbriata L-10628 HM536083 HM536084 — HM640260 HM536100 HM536127
Agaricomycetes / Gomphales
Clavariadelphus truncatus OSC67280 AY574649 — — DQ219064 — DQ219240
Phaeoclavulina grandis OSC122773 DQ218618 — — DQ219074 — DQ219252
Agaricomycetes / Hymenochaetales
Alloclavaria purpurea AFTOL-ID 1736 DQ457657 DQ437679 — — — —
Oxyporus corticola ZRL20151459 KY418899 KY418954 — KY419038 LT716075 KY419087
Peniophorella praetermissa AFTOL-ID 518 AY700185 AY707094 — AY787221 AY854081 —
Tropicoporus linteus MUCL47139 GU462002 — — — GU461973 GU461936
Agaricomycetes / Hysterangiales
Aroramyces gelatinosporus H4010 DQ218524 — — DQ218941 — DQ219118
Chondrogaster pachysporus OSC49298 DQ218538 — — DQ218958 — DQ219136
Agaricomycetes / Lepidostromatales
Ertzia akagerae BR FJ171733 — — — — —
Lepidostroma calocerum R05 FJ171737 — — — — —
Sulzbacheromyces caatingae DNA5385 KC170318 — — — — —
Agaricomycetes / Phallales
Dictyophora duplicata OSC38819 DQ218481 — — DQ219087 — DQ219265
Phallus costatus MB02040 DQ218513 — — DQ219104 — DQ219279
Agaricomycetes / Polyporales
Antrodia serialis KHL12010 JX109844 — — JX109870 JX109844 —
Bjerkandera adusta HHB 12826 KP135198 — KP134784 KP134913 KP134983 —
Climacodon septentrionalis ZW AY684165 AY705964 AY864872 AY780941 AY854082 AY885151
Daedalea quercina FP-56429 KY948883 — KY948989 — KY948809 —
Fomitopsis pinicola AFTOL-770 AY684164 AY705967 AY864874 AY786056 AY854083 AY885152
Ganoderma australe ZRL20151500 KY418900 KY418955 — — LT716076 KY419088
Grifola frondosa DSH s.n. AY629318 AY705960 AY864876 AY786057 AY854084 AY885153
Irpex lacteus DO 421/951208 JX109852 — — JX109882 JX109852 —
Lentinus strigosus ZRL20151738 KY418901 KY418956 — KY419039 LT716077 KY419089
Phanerochaete chrysosporium FPL5175 AF287883 AF026593 AY864880 — AY854086 AY885155
Postia lactea Kotiranta 20058 KC595939 — KY948979 — KC595939 —
Trametes sanguinea ZRL2015009 KY418902 KY418957 KY418983 KY419040 LT716078 KY419090
Trametes versicolor ZRL20151477 KY418903 KY418958 — KY419041 LT716079 KY419091
Agaricomycetes / Russulales
Bondarzewia montana AFTOL-ID 452 DQ234539 — DQ256049 AY218474 DQ200923 DQ059044
Hericium americanum AFTOL-ID 469 DQ411538 — — — DQ206987 DQ028585
Heterobasidion annosum AFTOL-ID 470 — — DQ667160 AH013701 DQ206988 DQ028584
Lactifluus deceptivus AFTOL-ID 682 AY631899 AY707093 — AY803749 AY854089 AY885158
Agaricomycetes / Sebacinales
Craterocolla cerasi TUB020203 KF061265 — — KF061300 KF061265 —
Tremellodendron pallidum AFTOL-ID 699 — AY766081 — DQ408132 DQ411526 DQ029196
Agaricomycetes / Stereopsidales
Stereopsis radicans OLR45395 KC203496 KC203496 — KC203502 — KC203516
Stereopsis sp. OKHL15544 — KC203499 — KC203505 — KC203519
Agaricomycetes / Thelephorales
Boletopsis leucomelaena PBM2678 DQ154112 DQ435797 GU187494 GU187820 DQ484064 GU187763
Thelephora ganbajun ZRL20151295 KY418908 KY418962 KY418987 KY419043 LT716082 KY419093
Tomentella sp. AFTOL-ID 1016 DQ835997 DQ092920 — DQ835999 DQ835998 —
Agaricomycetes / Trechisporales
Subulicystidium sp. KHL10780 AY586714 — — — AY463468 —
Trechispora alnicola AFTOL-ID 665 AY635768 AY657012 — — DQ411529 DQ059052
Dacrymycetes
Dacryopinax spathularia AFTOL-ID 454 AY701525 AY771603 AY857981 — AY854070 AY881020
Calocera cornea AFTOL-ID 438 AY701526 AY771610 AY857980 AY536286 AY789083 AY881019
Tremellomycetes
Bullera alba CBS 501 AF075500 X60179 KF036334 KF036745 AF444368 KF037016
Dioszegia antarctica CBS 10920 FJ640575 KF036667 KF036444 KF036858 DQ402529 KF037129
Open in a new tab

Sequence alignments and phylogenetic analyses

The dataset of concatenated 5.8S+nuc 18S+nuc 28S+rpb1+rpb2 +tef1 was used to investigate the systematic position of Paratrichaptum accuratum among 21 recognised orders of the class Agaricomycetes. Since P. accuratum was recovered near the orders Gloeophyllales and Jaapiales based on our preliminary phylogenies, sequences from species belonging to these two orders were selected as candidate references (Binder et al. 2010, Garcia-Sandoval et al. 2011, He et al. 2014, Telleria et al. 2015). For other representative species from Agaricomycetes, as well as representatives of Dacrymycetes and Tremellomycetes, we consulted studies of Lutzoni et al. (2004), Hibbett et al. (2007), Matheny et al. (2007), Hodkinson et al. (2014), Sjökvist et al. (2014), and Zhao et al. (2017). Bullera alba and Dioszegia antarctica, belonging to Tremellomycetes, were selected as the outgroup.

All intron regions of protein-coding genes (rpb1, rpb2, and tef1) and non-coding nuc rDNA were omitted. Sequences of each single-gene dataset were aligned with MAFFT v. 7.409 (Katoh & Standley 2013), using the default algorithm. Poorly aligned regions were detected by GUIDANCE2 webserver (Sela et al. 2015), and manually adjusted with MEGA v. 7 (Kumar et al. 2016), when necessary. Maximum likelihood (ML) analyses were performed for each gene with RAxML-HPC BlackBox v. 8.2.10 (Stamatakis 2014) on CIPRES Science Gateway (Miller et al. 2010), using 500 bootstrap (BS) replicates and the default GTR+G model. A conflict between two genes was assumed to happen when a monophyletic clade was supported with BS ≥ 70 % in a single tree but was contradicted with significant support in another (Hillis & Bull 1993). Congruence among genes was visually compared. Conflict-free alignments were concatenated and subjected to subsequent analyses. Sequence alignments are deposited at TreeBASE (submission ID: S24457; www.treebase.org).

Partitioned ML and Bayesian inference (BI) analyses were carried out for the concatenated dataset, respectively, with RAxML-HPC2 v. 8.2.10 (Stamatakis 2014) and MrBayes v. 3.2.6 (Ronquist et al. 2012), on CIPRES Science Gateway (Miller et al. 2010). ML analysis was run for 1 000 bootstrap (BS) replicates with the GTR+CAT model. For BI analysis, we used the GTR+G model for 5.8S and the GTR+I+G model for nuc 18S, nuc 28S, rpb1, rpb2, and tef1 as selected by jModeltest v. 2.1.10 (Darriba et al. 2012), based on the Akaike information criterion (AIC). BI analysis was conducted for four runs with four chains each for 10 M generations, sampling one tree every 1 000 generations. The first 25 % of trees were discarded as burn-in. Remaining trees were used to construct a 50 % majority-rule consensus phylogram with Bayesian posterior probabilities (PP). Tracer v. 1.7 (Rambaut et al. 2018) was used to confirm that the average standard deviation of split frequencies (= 0.006589) had reached an appropriate level with Effective Sampling Sizes (ESS) > 200. TreeGraph v. 2 (Stöver & Müller 2010) and Adobe Illustrator (Adobe Systems, Inc.) were used to edit and visualise resulting trees.

RESULTS

Molecular phylogeny

In this study, we generated new sequences of six genes (5.8S, nuc 18S, nuc 28S, rpb1, rpb2, tef1) from two specimens of Paratrichaptum accuratum (Table 1). The 5.8S+nuc 18S+nuc 28S+rpb1+rpb2+tef1 dataset included 96 species and 97 sequences. The final alignment had 7 181 positions, including gaps, of which 38 % (2696/7181) were parsimony-informative. Phylograms obtained from BI and ML analyses had similar topologies, and, thus, only the ML tree with BP and PP support values is shown (Fig. 1).

Fig. 1.

Fig. 1.

Open in a new tab

Phylogenetic relationships of orders among Agaricomycetes inferred from 5.8S, nuc 18S, nuc 28S, rpb1, rpb2, and tef1 sequences. Nodes are labeled with Maximum Likelihood bootstrap proportional values (BS) ≥ 50 % and Bayesian Posterior Probabilities (PP) ≥ 0.8. Thickened branches obtained supports by both BS ≥ 70 % and PP ≥ 0.95. The greyish box indicates taxa in Gloeophyllales. Scale bar = substitutions per site.

In our six-gene phylogenetic analysis, three classes, Agaricomycetes, Tremellomycetes and Dacrymycetes, were resolved as monophyletic clades with BP = 93–100 and PP = 1. Sequences of two specimens of Paratrichaptum accuratum were almost identical. They, together with Boreostereum radiatum, formed a basal lineage in Gloeophyllales (Fig. 1). Jaapia was recovered in Gloeophyllales (Fig. 1), which makes Jaapiales a synonym of Gloeophyllales. Of the 20 currently recognized orders in the Agaricomycetes, 19 were monophyletic (Agaricales, Amylocorticiales, Atheliales, Auriculariales, Boletales, Cantharellales, Corticiales, Geastrales, Gloeophyllales, Hymenochaetales, Hysterangiales, Lepidostromatales, Phallales, Polyporales, Russulales, Sebacinales, Stereopsidales, Thelephorales, and Trechisporales), with BP = 81–100 and PP = 1; only Gomphales lacked support (Fig. 1).

Taxonomy

Gloeophyllales Thorn, Mycol. Res. 111: 540. 2007.

Synonym: Jaapiales Manfr. Binder, K.H. Larss. & Hibbett, Mycologia 102: 871. 2010

Type genus: Gloeophyllum.

Notes: Jaapiales is placed here in synonymy with Gloeophyllales based on our phylogram (Fig. 1). Gloeophyllales, including a single family Gloeophyllaceae, mostly accommodates polypore genera (e.g., Gloeophyllum, Griseoporia, Heliocybe, Hispidaedalea, Paratrichaptum, Neolentinus, and Osmoporus), and some agaricoid (e.g., Heliocybe and Neolentinus) and corticoid genera (e.g., Boreostereum, Chaetodermella, Jaapia, and Veluticeps).

The concept of Gloeophyllales is in agreement with Hibbett et al. (2007) but expanded to encompass the genus Jaapia with pigmented, narrowly fusoid, and cyanophilous basidiospores. Almost all genera in Gloeophyllales cause brown rot, except for Boreostereum and Jaapia for which rot type remains unclear. Boreostereum is possibly associated with white rot (Martin & Gilbertson 1980) but also viewed as brown rot (Chamuris 1988); Jaapia may belong to a new type of brown rot based on genomic analyses (Riley et al. 2014).

Gloeophyllaceae Jülich, Bibl. Mycol. 85: 368. 1981.

Synonyms: Boreostereaceae Jülich, Bibl. Mycol. 85: 357. 1981.

Jaapiaceae Manfr. Binder, K.H. Larss. & Hibbett, Mycologia 102: 871. 2010.

Type genus: Gloeophyllum.

Note: The names Boreostereaceae and Jaapiaceae are considered here as synonyms of Gloeophyllaceae based on our phylogram (Fig. 1).

Paratrichaptum Corner, Nova Hedwigia, Beih. 86: 136. 1987.

Type species: Paratrichaptum accuratum.

Basidiocarps pileate, sessile. Pilei yellowish brown to dark brown, applanate to triquetrous. Pore surface grey to pale purplish grey when fresh, turning to brown to blackish brown when dry; pores angular to daedaleoid, with thick dissepiments. Hyphal system monomitic in both context and trama. All hyphae nodose-septate, branching from the clamp. Context hyphae yellowish brown, thick-walled. Tramal hyphae yellowish brown, thick-walled. Cystidia fasciculate, thick-walled. Basidia subclavate to clavate, pale yellowish brown, thin- to slightly thick-walled, with two to four sterigmata. Basidiospores broadly ellipsoid to ellipsoid, pale brown, thin- to slightly thick-walled, smooth, inamyloid, non-dextrinoid, acyanophilous.

Paratrichaptum accuratum Corner, Nova Hedwigia, Beih. 86: 136. 1987. Figs 2, 3.

Fig. 2.

Fig. 2.

Open in a new tab

Paratrichaptum accuratum. A. Native habitat of GC 1708-180 at Maguan County, Yunnan, China, 9 August 2017. B–C. Basidiocarp on living angiosperm trunk (GC 1708-180). D. Pore surface in situ (GC 1708-180). E. Partial dried specimen of GC 1708-180. F–G. Dried specimen of GC 1708-183. H–I. Dried specimen of O-F-911778 (photographed by Katriina Bendiksen). This specimen seems to be a duplicate from the herbarium of Government Forest Experiment Station, Tokyo, Japan. It is noted that the correct name for the collector is R. Kanehira, a Japanese botanist. Bars: B–C = 5 cm; D = 4 mm; E = 2 cm; F–G, I = 1 cm.

Fig. 3.

Fig. 3.

Open in a new tab

Microscopic structures of Paratrichaptum accuratum (GC 1708-183). A, B. Hyphae from context. C. Cystidia. D. Basidia. E. Basidiospores. Bars: A–D = 10 µm; E = 5 µm.

Typus: Indonesia, Sumatra, Brastagi, alt. 2 000 m, on a dead fallen trunk in montane forest, 15 Sep. 1931, E.J.H. Corner, holotype (E?).

Basidiocarps probably perennial, broadly sessile, pileate, solitary, soft-corky and spongy when fresh, corky and light in weight when dry, without odour, temporarily becoming black in KOH in all parts of the fruiting body. Pilei applanate to triquetrous, semicircular, projecting up to 14 cm, up to 28 cm wide and up to 15 cm thick at base. Pileal surface yellowish brown to dark brown, glabrous to velutinous, covered by mosses in old specimens; margin obtuse when young, sharper with age. Pore surface grey to pale purplish grey when fresh, turning to brown to blackish brown when dry; pores angular to irregular when young, becoming daedaleoid with age, 0.5–1.5 per mm, dissepiments thick, entire and sterile; single pores up to 1 cm long and 2 mm wide when daedaleoid. Tubes brown, corky, up to 1.5 cm deep, tube layers distinct, new layer successively grow from the dead ones. Context, dark brown, corky, fibrous, up to 6 cm thick, homogeneous. Hyphal system monomitic in both context and trama. All hyphae nodose-septate, branching from the clamp. Context hyphae yellowish brown, fairly straight, occasionally branched, 5–7.5 µm diam, with 0.5–1 µm diam thick walls, loosely interwoven. Tramal hyphae yellowish brown, fairly straight, occasionally branched, 2.5–5.5 µm diam, with 0.5–1 µm diam thick walls, loosely interwoven. Cystidia cylindrical to subclavate, with obtuse apex, straight to slightly flexuous, fasciculate, projecting, pale brown to yellowish brown, 30–90 × 3–6 µm, with 0.5–1 µm diam thick walls. Basidia subclavate to clavate, usually with four sterigmata, rarely with two or three sterigmata, pale brown, thin- to slightly thick-walled, with 0.2–0.4 µm diam walls, 20–34 × 4–5.5 µm. Basidiospores broadly ellipsoid to ellipsoid, pale brown, thin- to slightly thick-walled, with 0.2–0.4 µm thick walls, smooth, sometimes with small oil-drops, inamyloid, non-dextrinoid, acyanophilous, mostly 3.4–4.9 × 2.4–3.2 µm. (3.1–)3.4–4.4(–5.2) × (2.1–)2.4–3(–3.5) µm, L = 3.9 ± 0.5 µm, W = 2.7 ± 0.3 µm, Q = 1.45 (n = 30) (GC 1708-180); (3.2–)3.6–4.6(–5.1) × (2.2–)2.4–2.9 (–3.3) µm, L = 4.1 ± 0.5 µm, W = 2.7 ± 0.3 µm, Q = 1.54 (n = 30) (GC 1708-183); (3.5–)4–4.9 (–5.3) × (2.4–)2.6–3.2(–3.6) µm, L = 4.4 ± 0.4 µm, W = 2.9 ± 0.3 µm, Q = 1.53 (n = 30) (TFM F-17203).

Distribution: Asian species. First described from a highland forest in Indonesia (Sumatra) (Corner 1987), later reported from subtropical to boreal regions of Japan (Hokkaido, Kagoshima, Nara, Yamagata), Taiwan (Núñez & Ryvarden 2001, Hattori 2017), and China (Yunnan, this study).

Ecology: On dead or living angiosperm trunks in old-growth forest, occurring in August to October (Corner 1987, Hattori 2017).

Type of rot: Brown rot (Hattori 2017).

Specimens examined: China, Yunnan Province, Wenshan Zhuang and Miao Autonomous Prefecture, Maguan County, Gulinjing Township, 22°51ʹ33ʺ N 104°00ʹ25ʺ E, alt. 1 772 m, on living angiosperm trunk, 9 Aug. 2017, C.C. Chen, GC 1708–183 (TNM F32585); 22°51ʹ34ʺN 103°59ʹ36ʺE, alt. 1 895 m, on living angiosperm trunk in a subtropical evergreen broad-leaved forest dominated by Alcimandra, Lithocarpus and Manglietia, 9 Aug. 2017, C.C. Chen, GC 1708–180 (KUN HKAS104962 & TNM F32584). Japan, Nara Prefecture, Mt. Wasamata, 30 Aug. 1994, N. Iwata (TFM F-17203). Taiwan, 25 Sep. 1922, R. Kanehira (miswritten as A. Kanehira on specimen label, Fig. 2H) (O-F-911778).

Notes: Paratrichaptum accuratum was described based on a single specimen (Corner 1987). Hattori (2001), as well as this study, failed to trace the holotype or other original material of P. accuratum deposited in the herbarium of Royal Botanic Garden Edinburgh (E). Instead, we studied some specimens from China, Japan, and Taiwan. The peculiar combination of morphological features makes P. accuratum easy to identify. Our studied specimens correspond well with Corner's (1987) descriptions and illustrations for this species, although some minor differences were noticed. First, the basidiocarp tissue of P. accuratum temporarily turns black in KOH, which was not mentioned in the protologue. Second, the species was reported as annual (Corner 1987). However, one of our specimens (GC 1708–180) developed a new tube layer successively growing from old ones (Fig. 2B–E). Third, we found some mature basidiospores of P. accuratum that are of a slightly darker colour and with thicker walls (Fig. 3E).

A Taiwanese specimen of P. accuratum (O-F-911778), collected on 25 September 1922 by the Japanese botanist R. Kanehira, lacks detailed location information (Fig. 2H). However, we presume it is likely collected from montane areas near to Lala Mountain, Taoyuan, because he made a field trip to Lala Mountain during the same period according to plant specimen records retrieved from the online database of TAIF (http://taif.tfri.gov.tw/search.php). Lala Mountain area lies in the warm temperate region, within the native range of P. accuratum.

DISCUSSION

The present study places Paratrichaptum in the family Gloeophyllaceae (Gloeophyllales, Agaricomycetes) based on studies derived from morphological features and phylogenetic analyses of sequences of six genes (Figs 1–3). Our study also shows that a corticoid genus Jaapia with two species (viz., J. argillacea and J. ochroleuca) is classified in Gloeophyllaceae and Gloeophyllales according to phylogenetic evidence (Fig. 1), although Jaapia was placed in the family Jaapiaceae and the order Jaapiales by Binder et al. (2010). As a result, Jaapiaceae and Jaapiales become synonyms of Gloeophyllaceae and Gloeophyllales, respectively.

Regarding the family-level classification of Gloeophyllales, we unite all taxa in a single family (viz., Gloeophyllaceae) because the resolution of the six-gene phylogeny and taxon sampling are not enough to resolve the family relationships at the moment. Nevertheless, the possibility to recover the families Boreostereaceae and Jaapiaceae, or even to introduce a new family for Paratrichaptum cannot be excluded when data from whole-genome studies become available.

The topology of our six-gene phylogram (Fig. 1) is consistent with previous studies (Binder et al. 2010, Garcia-Sandoval et al. 2011, Floudas et al. 2012, Hodkinson et al. 2014, Sjökvist et al. 2014, Nagy et al. 2015, Garnica et al. 2016, Zhao et al. 2017). However, deviating taxon- or gene-sampling applied to different analyses may result in different positions of the taxa on trees. For example, a six-gene phylogeny placed Boreostereum radiatum as the sister group to the core group of Gloeophyllales, consisting of the genera Chaetodermella, Gloeophyllum, Heliocybe, Neolentinus, Osmoporus, and Veluticeps (Garcia-Sandoval et al. 2011). In our analysis, B. radiatum is recovered as a sister taxon to Paratrichaptum accuratum, but the position is weakly supported. Another six-gene phylogeny placed Jaapia as the sister group to Agaricomycetidae, consisting of Agaricales, Amylocorticiales, Atheliales, and Boletales (Binder et al. 2010), whereas in our analysis Jaapia is placed in Gloeophyllales.

Paratrichaptum represents the earliest diverging lineage in Gloeophyllales, yielding a new picture of this order. For example, with the addition of Paratrichaptum, pileate basidiocarps and brown rot appear to be ancestral states of Gloeophyllales. Besides, brown rot could be synapomorphic in Gloeophyllales, although the rot type of Boreostereum and Jaapia should be further confirmed. Moreover, genera from the basal lineages of Gloeophyllales (Boreostereum, Jaapia, and Paratrichaptatum) possess pigmented basidiospores, while the rest of the members of Gloeophyllales possess colorless basidiospores. Like most members of Gloeophyllales, Paratrichaptum has brownish context but lacks dimitic to trimitic hyphal system, and posesses clamp connections. There is no morphological synapomorphy to unite Gloeophyllales.

Paratrichaptum accuratum may represent a relic species, according to its phylogenetic position, peculiar distribution pattern and rare occurrence. On the phylogram (Fig. 1), P. accuratum does not have any close relatives and has relatively long genetic distances from other members in Gloeophyllales. Very few collections of P. accuratum were made since 1922. According to available collection information, P. accuratum occurs in old-growth subtropical-boreal forests in some disjunct mountain areas of eastern and south-eastern Asia. Paratrichaptum accuratum is a threatened species and its conservation status should be assessed based on the criteria in Dahlberg & Mueller (2011). Paratrichaptum accuratum grows on dead or living angiosperms, which implies that it presumably colonises living trees and continues to degrade wood after the tree dies.

ACKNOWLEDGEMENTS

This study was financed by the Ministry of Science and Technology of ROC (Taiwan) (Grant no 1072621-B-178-002-MY3). We are grateful for the help of Dr Xiang-Hua Wang, the mycologist of KUN, who arranged the field trip for the first author to Yunnan, China in Aug 2017 and also aided in phylogenetic analyses. We are indebted to Drs Karl-Henrik Larsson and Katriina Bendiksen (O) for kindly providing Taiwanese specimen photographs, Chiung-Chih Chang (TNM) for adjusting figures, Siou-Zhen Chen (TNM) for curating studied specimens, and Ronnie Gicana (NCHU) for improving the manuscript. We also thank the reviewers and editor for their valuable suggestions and discussions.

REFERENCES

  1. Binder M, Larsson KH, Matheny PB, et al. (2010). Amylocorticiales ord. nov. and Jaapiales ord. nov.: early diverging clades of Agaricomycetidae dominated by corticioid forms. Mycologia 102: 865–880. [DOI] [PubMed] [Google Scholar]
  2. Chamuris G. (1988). The non-stipitate stereoid fungi in the northeastern United States and adjacent Canada. Mycologia Memoir 14: 41–45. [Google Scholar]
  3. Chen CC, Wu SH, Chen CY. (2018). Hydnophanerochaete and Odontoefibula, two new genera of phanerochaetoid fungi (Polyporales, Basidiomycota) from East Asia. MycoKeys 39: 75–96. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Corner EJH. (1987). Ad Polyporaceas IV. The genera Daedalea, Flabellophora, Flavodon, Gloeophyllum, Heteroporus, Irpex, Lenzites, Microporellus, Nigrofomes, Nigroporus, Oxyporus, Paratrichaptum, Rigidoporus, Scenidium, Trichaptum, Vanderbylia, and Steccherinum. Beihefte zur Nova Hedwigia 86: 1–265. [Google Scholar]
  5. Dahlberg A, Mueller GM. (2011). Applying IUCN red-listing criteria for assessing and reporting on the conservation status of fungal species. Fungal Ecology 4: 147–162. [Google Scholar]
  6. Darriba D, Taboada GL, Doallo R, et al. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772–772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Drummond AJ, Suchard MA, Xie D, et al. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 1969–1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Floudas D, Binder M, Riley R, et al. (2012). The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336: 1715–1719. [DOI] [PubMed] [Google Scholar]
  9. Frøslev T, Matheny PB, Hibbett DS. (2005). Lower level relationships in the mushroom genus Cortinarius (Basidiomycota, Agaricales): a comparison of RPB1, RPB2, and ITS phylogenies. Molecular Biology and Evolution 37: 602–618. [DOI] [PubMed] [Google Scholar]
  10. Garcia-Sandoval R, Wang Z, Binder M, et al. (2011). Molecular phylogenetics of the Gloeophyllales and relative ages of clades of Agaricomycotina producing a brown rot. Mycologia 103: 510–524. [DOI] [PubMed] [Google Scholar]
  11. Garnica S, Riess K, Schön ME, et al. (2016). Divergence times and phylogenetic patterns of Sebacinales, a highly diverse and widespread fungal lineage. PLoS One 11: e0149531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hall TA. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98. [Google Scholar]
  13. Hattori T. (2001). Type studies of the polypores described by EJH Corner from Asia and West Pacific areas II. Species described in Gloeophyllum, Heteroporus, Microporellus, Oxyporus, Paratrichaptum, and Rigidoporus. Mycoscience 42: 19–28. [Google Scholar]
  14. Hattori T. (2017). Biogeography of polypores in Malesia, Southeast Asia. Mycoscience 58: 1–13. [Google Scholar]
  15. He SH, Vlasák J, Dai YC. (2014). Hispidaedalea gen. nov. and Griseoporia taiwanense sp. nov. (Gloeophyllales, Basidiomycota) based on morphological and molecular characters. Mycological Progress 13: 833–839. [Google Scholar]
  16. Hibbett DS, Binder M, Bischoff JF, et al. (2007). A higher-level phylogenetic classification of the Fungi. Mycological Research 111: 509–547. [DOI] [PubMed] [Google Scholar]
  17. Hillis DM, Bull JJ. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42: 182–192. [Google Scholar]
  18. Hodkinson BP, Moncada B, Lücking R. (2014). Lepidostromatales, a new order of lichenized fungi (Basidiomycota, Agaricomycetes), with two new genera, Ertzia and Sulzbacheromyces, and one new species, Lepidostroma winklerianum. Fungal Diversity 64: 165–179. [Google Scholar]
  19. Katoh K, Standley DM. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kumar S, Stecher G, Tamura K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Liu YJ, Whelen S, Hall BD. (1999). Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Molecular Biology and Evolution 16: 1799–1808. [DOI] [PubMed] [Google Scholar]
  22. Lutzoni F, Kauff F, Cox CJ, et al. (2004). Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. American Journal of Botany 91: 1446–1480. [DOI] [PubMed] [Google Scholar]
  23. Martin K, Gilbertson R. (1980). Synopsis of wood-rotting fungi on spruce in North America: III. Mycotaxon 10: 479–501. [Google Scholar]
  24. Matheny PB. (2005). Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales). Molecular Phylogenetics and Evolution 35: 1–20. [DOI] [PubMed] [Google Scholar]
  25. Matheny PB, Wang Z, Binder M, et al. (2007). Contributions of rpb2 and tef1 to the phylogeny of mushrooms and allies (Basidiomycota, Fungi). Molecular Phylogenetics and Evolution 43: 430–451. [DOI] [PubMed] [Google Scholar]
  26. Miller MA, Pfeiffer W, Schwartz T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceeding of the Gateway Computing Environments Workshop (GCE). 14 November 2010. Los Angeles, USA: 1–8. [Google Scholar]
  27. Moncalvo JM, Lutzoni FM, Rehner SA, et al. (2000). Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences. Systematic Biology 49: 278–305. [DOI] [PubMed] [Google Scholar]
  28. Nagy LG, Riley R, Tritt A, et al. (2015). Comparative genomics of earlydiverging mushroom-forming fungi provides insights into the origins of lignocellulose decay capabilities. Molecular Biology and Evolution 33: 959–970. [DOI] [PubMed] [Google Scholar]
  29. Núñez M, Ryvarden L. (2001). East Asian polypores 2. Polyporaceae s. lato. Synopsis Fungorum 14: 170–522. [Google Scholar]
  30. Rambaut A, Drummond AJ, Xie D, et al. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901–904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rehner SA, Buckley E. (2005). A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97: 84–98. [DOI] [PubMed] [Google Scholar]
  32. Riley R, Salamov AA, Brown DW, et al. (2014). Extensive sampling of basidiomycete genomes demonstrates inadequacy of the whiterot/brown-rot paradigm for wood decay fungi. Proceedings of the National Academy of Sciences 111: 9923–9928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Robert V, Stegehuis G, Stalpers J. (2005). The MycoBank engine and related databases. 16 September 2019. http://www.mycobank.org. [Google Scholar]
  34. Ronquist F, Teslenko M, Van der Mark P, et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ryvarden L. (1991). Genera of polypores: nomenclature and taxonomy. Synopsis Fungorum 5: 1–363. [Google Scholar]
  36. Sánchez-Ramírez S, Tulloss RE, Amalfi M, et al. (2015). Palaeotropical origins, boreotropical distribution and increased rates of diversification in a clade of edible ectomycorrhizal mushrooms (Amanita section Caesareae). Journal of Biogeography 42: 351–363. [Google Scholar]
  37. Sela I, Ashkenazy H, Katoh K, et al. (2015). GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Research 43: W7–W14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sjökvist E, Pfeil BE, Larsson E, et al. (2014). Stereopsidales - a new order of mushroom-forming fungi. PLoS One 9: e95227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Stamatakis AJB. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Stöver BC, Müller KF. (2010). TreeGraph 2: Combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11: 1–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Telleria MT, Dueñas M, Melo I, et al. (2015). Spelling out Jaapia species. Mycological Progress 14: 57. [Google Scholar]
  42. White TJ, Bruns T, Lee S, et al. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications (Innis MA, Gelfand DH, Sninsky JJ, et al., eds). Academic Press, San Diego, USA: 315–322. [Google Scholar]
  43. Zhao RL, Li GJ, Sánchez-Ramírez S, et al. (2017). A six-gene phylogenetic overview of Basidiomycota and allied phyla with estimated divergence times of higher taxa and a phyloproteomics perspective. Fungal Diversity 84: 43–74. [Google Scholar]

Articles from Fungal Systematics and Evolution are provided here courtesy of Westerdijk Fungal Biodiversity Institute

RESOURCES