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Article

Notes on the Ecology and Distribution of Species of the Genera of Bondarzewiaceae (Russulales and Basidiomycota) with an Emphasis on Amylosporus

by
Shah Hussain
1,2,
Moza Al-Kharousi
2,
Dua’a Al-Maqbali
2,
Arwa A. Al-Owaisi
2,
Rethinasamy Velazhahan
1,
Abdullah M. Al-Sadi
1,3,* and
Mohamed N. Al-Yahya’ei
2,*
1
Department of Plant Sciences, College of Agricultural and Marine Sciences, Sultan Qaboos University, P.O. Box 34, AlKhoud 123, Oman
2
Oman Animal and Plant Genetic Resources Center (Mawarid), Ministry of Higher Education, Research and Innovation, P.O. Box 515, AlKhoud 123, Oman
3
College of Agriculture, University of Al Dhaid, Sharjah P.O. Box 27272, United Arab Emirates
*
Authors to whom correspondence should be addressed.
J. Fungi 2024, 10(9), 625; https://doi.org/10.3390/jof10090625
Submission received: 6 August 2024 / Revised: 27 August 2024 / Accepted: 30 August 2024 / Published: 1 September 2024
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Abstract

:
The family Bondarzewiaceae is an important and diverse group of macrofungi associated with wood as white rotting fungi, and some species are forest tree pathogens. Currently, there are nine genera and approximately 89 species in the family, distributed in tropical, subtropical, and temperate climates. To address the phylogenetic relationships among the genera, a combined ITS-28S dataset was subjected to maximum likelihood (ML), Bayesian inference (BI), and time divergence analyses using the BEAST package. Both ML and BI analyses revealed two major clades, where one major clade consisted of Amylosporus, Stecchericium, and Wrightoporia austrosinensisa. The second major clade is composed of Bondarzewia, Heterobasidion, Gloiodon, Laurilia, Lauriliella, and Wrightoporia, indicating that these genera are phylogenetically similar. Wrightoporia austrosinensisa recovered outside of Wrightoporia, indicating that this species is phylogenetically different from the rest of the species of the genus. Similarly, time divergence analyses suggest that Bondarzewiaceae diversified around 114 million years ago (mya), possibly during the Early Cretaceous Epoch. The genus Amylosporus is well resolved within the family, with an estimated stem age of divergent around 62 mya, possibly during the Eocene Epoch. Further, the species of the genus are recovered in two sister clades. One sister clade consists of species with pileate basidiomata and generative hyphae with clamp connections, corresponding to the proposed section Amylosporus sect. Amylosporus. The other consists of species having resupinate basidiomata and generative hyphae without clamps, which is treated here as Amylosporus sect. Resupinati. We provided the key taxonomic characters, known distribution, number of species, and stem age of diversification of each section. Furthermore, we also described a new species, Amylosporus wadinaheezicus, from Oman, based on morphological characters of basidiomata and multigene sequence data of ITS, 28S, and Tef1-α. With pileate basidiomata and phylogenetic placement, the new species is classified under the proposed A. sect. Amylosporus. An identification key to the known species of Amylosporus is presented. Ecology and distribution of species of the genera in the family are discussed.

1. Introduction

The family Bondarzewiaceae Kotl. and Pouzar was originally introduced to accommodate the wood-rotting mushrooms, with type genus Bondarzewia Singer [1]. The family is characterized by fleshy fruiting bodies with annual growth habit with porioid, hydnoid, or clavarioid hymenophore [1]. Later on, other genera, such as Amylaria Corner, Amylosporus Ryvarden, Heterobasidion Bref., and Echinodontium Ellis and Everh., were added to the family [2]. However, in several later studies, it was suggested that Echinodontium is sister to Amylostereum Boidin and has been treated under Echinodontiaceae Donk [3,4,5,6].
Macroscopically, Bondarzewiaceae is characterized by an annual to perennial growth habit with resupinate, effused-reflexed, pileate-sessile, pileate-stipitate to clavarioid fruiting bodies, and with smooth, tuberculate, poroid, and hydnoid hymenophore. Microscopically, species in the family have monomitic, pseudodimitic to dimitic hyphal systems, rarely trimitic hyphal systems, generative hyphae inamyloid, with or without clamps, skeletal hyphae inamyloid or dextrinoid (Amylosporus), gloeoplerous hyphae and gloeocystidia present or absent, and basidiospores usually asperulate to spinulose, verrucose to echinulate, hyaline to pigmented, and amyloid [7]. Currently, the family is composed of nine genera and 89 species [7,8,9]. Members of the family are widespread in distribution and found in tropical, subtropical, and temperate climates [7]. Ecologically, these species are mostly associated with wood as decaying fungi; however, some members, such as Bondarzewia berkeleyi (Fr.) Bondartsev and Singer, B. montana (Quél.) Singer, Heterobasidion annosum (Fr.) Bref., and H. parviporum Niemelä and Korhonen, are tree pathogens [6,10].
The genus Amylosporus was introduced in 1973, initially typified with Amylosporus graminicola (Murrill) Ryvarden [11]. Later on, Amylosporus graminicola was synonymized with A. campbellii (Berk.) Ryvarden, the latter which became the type species of the genus [12]. Initially, the genus was placed in Wrightoporiaceae Jülich [13], but recently it was treated under Bondarzewiaceae [7,8,9]. Morphologically, the genus is distinguished by annual to perennial basidiomata, which may pileate, effused-reflexed, or resupinate; the pileate form may be stipitate or sessile; cap surface buff to ochraceous or pinkish, darker at the center; pore surface whitish to pale pinkish or lilac to vinaceous; and pores 2–10 per mm, rounded to angular. Microscopically, the genus has a dimitic hyphal system; generative hyphae that are thin-walled, rarely branched, with simple septa; and clamp connections may be present or absent; skeletal hyphae are usually thick-walled, frequently branched, dextrinoid, or IKI−; gloeoplerous hyphae may be present or absent; clamp connections are absent in hymenium; cystidia are absent; basidia are usually four-spored rarely eight-spored; and basidiospores are mostly thin-walled, finely asperulate, IKI+, CB+, or CB− [13,14,15].
Currently, there are 13 species of Amylosporus, distributed in the Americas, Europe, Africa, and Asia; however, no member of the genus has been reported from Australia [15,16,17,18]. Although, several records of the genus from Australia are available on the GBIF website (https://www.gbif.org/species/, accessed 17 July 2024). Sequence data (ITS and 28S) are available only for eight species, which could be the reason that the species of this genus are not yet classified into sections. However, basidiomata form (resupinate/pileate) and the presence or absence of clamps in generative hyphae could be employed for the infrageneric classification of Amylosporus.
Species of Amylosporus are parasitic or saprotrophic in nature, associated with broad-leaved trees or found on the forest floor under grasses, probably associated with underground angiosperm wood [13,17]. The parasitic species are causing white rot in a number of angiosperm plants [19].
In this study, we presented a robust phylogeny and time divergence estimation of Bondarzewiaceae, representing all the genera of the family except the monotypic genus Amylaria himalayensis Corner, for which the sequence data are not available. For the first time, infrageneric classification of the genus Amylosporus with two proposed sections is provided. We also described a new species in Amylosporus, and a taxonomic key to known taxa of the genus is presented. Ecology and species distribution of the genera in the family are further discussed.

2. Materials and Methods

2.1. Study Sites, Sampling and Morphological Examination

The study area, the Dhofar region (Figure 1), located in the south of Oman, experiences monsoon rains from mid-June to mid-September each year [20]. The sea-facing sides of mountains and plains of Dhofar changes into a lush-green region in the summer, with the highest plant biodiversity in the entire Arabian Peninsula [21]. During the summer season, a number of mushroom-forming fungi appeared on the forest floor, on logs, tree trunks, on termite mounds, etc. Mushroom exploration expeditions are recently initiated in the region in which several new species have been described [22,23,24,25,26], including a polypore Fuscoporia dhofarensis Al-Sadi and S. Hussain [27].
Basidiomata were collected in the months of August-September during the years 2022 and 2023, from Dhofar Governorate, Oman. The specimens were found on the forest floor, under grasses. This mushroom is very common in the region during the monsoon season. Morphological characteristics, such as basidiomata size, shape, color, texture, etc., were noted in the field based on fresh collections. Basidiomata were photographed in the natural habitat, tagged, dried in a fruit dehydrator (45 °C temperature), and kept in zipper bags. The dried basidiomata were subjected to a low-temperature treatment at −80 °C for two weeks to kill all the insect’s eggs/larvae. Small, hand-made sections were prepared from the upper surface of the pileus, subiculum, tubes, and stipe for microscopic investigations. The sections were mounted in 5% aqueous KOH solution (w/v), rehydrated in 1% aqueous Congo red (w/v). Microscopic structures, such as basidiospores, basidia, generative hyphae, skeletal hyphae, etc., were examined under a compound microscope (ECLIPSE Ni-U, Nikon Co., Ltd., Minato City, Japan). The studied materials are deposited at Mawarid Center, AlKhoud, Muscat, Oman.

2.2. Molecular Identification

DNA extraction was achieved using the X-AMP DNA extraction kit (Dubuque, IA, USA), according to the manufacturer’s protocol. Three DNA regions were amplified, which included the internal transcribed spacer region (ITS1-5.8S-ITS2 = ITS), the D1/D2 domain of the large subunit of nuc rDNA (28S), and a portion of the translation elongation factor 1 alpha (Tef1-α) gene. The following primers were used: ITS1F/ITS4 for ITS [28,29], LR0R/LR5 for 28S [30], and EF1-983/EF1-1567R for Tef1-α [31], respectively. The PCR reactions and conditions were according to Chen et al. [32]. Purification and sequencing of the PCR products was performed at Macrogen Inc. © (Seoul, Republic of Korea).

2.3. Phylogenetic Analyses

Only ITS and 28S sequence data are available (in GenBank) for most species in Bondarzewiaceae; therefore, we employed the sequences of these two regions to address the phylogeny of the family. A combined ITS-28S dataset was constructed from 52 specimens including Amylonotus labyrinthinus (Yuan 1475) as the outgroup taxon. The dataset represents 51 specimens of Bondarzewiaceae, including 24 samples of Amylosporus, 12 of Wrightoporia, three specimens of each Bondarzewia and Heterobasidion, and two specimens of each Gloiodon P. Karst., Laurilia Pouzar, Lauriliella S.H. He and Nakasone, Stecchericium D.A. Reid. Only Amylaria was not included because no sequence of the genus is available in GenBank. The dataset was aligned using the online version of the multiple sequence alignment tools (MAFFT v. 7 [33]), applying the L-INS-I strategy, and then manually adjusted in BioEdit v. 7.0.9.0 [34]. Details of the specimens included in the phylogenetic analyses are given in Table 1.
Two methods of phylogenetic analyses were used: maximum likelihood (ML) and Bayesian inference (BI). The ML analyses were executed with RAxML-HPC BlackBox (https://www.phylo.org/portal2/; [35]), using the CIPRES Science Gateway platform (https://www.phylo.org/portal2/; accessed on 25 July 2024 [36]). The best model was (TPM2u+F+I+G4) selected using jModelTest2 [37]. Branch support for the ML phylogeny was calculated using 1000 bootstrap replicates. Similarly, for BI analyses, BEAST v. 1.8.2 [38] was used. Initially, the FASTA file was converted to a nexus datafile using ClustlX v. 2.1 [39]. The nexus datafile was converted to an XML file using BEAUti v. 1.8.2 [38]. The model of speciation chosen was the Birth-Death Incomplete Sampling model [40]. Four separate runs were performed with BEAST on the XSEDE tool (v. 1.8.2) on the CIPRES Science Gateway [36]. The log files were traced in Tracer v. 1.6 [41] to check the effective sample size (ESS) values for all parameters. The ESS value for each parameter was well over 200. The tree files were combined in LogCombiner v. 1.8.2 [42]. A maximum clade credibility (MCC) tree was obtained using the TreeAnnotator v. 1.8.2 [42]. Values were considered significant when the ML bootstrap (BT) percentage was ≥70 and BI posterior probabilities (PPs) was ≥0.95. FigTree 1.4.2 [43] was used for tree visualization, and the tree was annotated using Adobe Illustrator CC2019.

2.4. Estimation of the Stem Age of Amylosporus

To estimate the stem age of diversification of Amylosporus within Bondarzewiaceae, the combined ITS-28S dataset, comprising 52 specimens, was used. This dataset represents all the representative genera of the family except Amylaria, for which no molecular data are available. The time divergence analyses were estimated using BEAST v. 1.8.2 [38]. An XML file was constructed using BEAUti v. 1.8.2 [42], where substitution models were optimized. A Yule speciation model was chosen [44] with HKY+G+I distribution, following ModelFinder [45]. The ulcd.mean parameter was specified with a uniform distribution, where the initial value was 0.033, the higher set was 1.0, and the lower set was 0.0, using a lognormal relaxed molecular clock. For treeModel.rootHeight parameter, a normal distribution with a mean age of 117 was specified (standard deviation 10) following He et al. [7]. Four independent runs of MCMC chains were run, with 20 million generations each, a logging state of 1000 generation, and discarding the first 10% as burn-in. Log files were checked in Tracer v. 1.6 [41]. Using TreeAnnotator v. 1.8.2 [42], the Tree files were merged into a maximum clade credibility (MCC) tree.
The alignment files were submitted to TreeBase (https://www.treebase.org/treebase-web/home.html; http://purl.org/phylo/treebase/phylows/study/TB2:S31306; accessed on 8 June 2024).

3. Results

3.1. Molecular Phylogenetic Analyses

The combined ITS-28S alignment was 2044 characters long, including 1000 constant sites, 795 parsimony informative sites, and 249 uninformative sites. Both ML and BI analyses resulted phylogenetic trees with similar topologies. The phylogeny inferred from ML analyses is presented with values from both BT and PPs (Figure 2). Species within Bondarzewiaceae were recovered in two major clades. Clade-I corresponds to the genus Amylopsorus, Stecchericium, and one species of Wrightoporia, W. austrosinensis, with moderate support in ML analysis (BT 85%) and excellent support in BI analysis (PPs 0.96). Species in Amylosporus are further split into two sister clades, each with strong phylogenetic support (BT).

3.2. Divergence Time Estimation

Species of Bondarzewiaceae were diversified approximately 114 million years ago (mya); the results are presented in Figure 3. Similar to ML and BI phylogenies, genera in the family recovered in two major clades using the time divergence estimation analyses. One major clade consisting of Amylopsorus, Stecchericium, and Wrightoporia austrosinensis. The ancestors of these taxa are supposed to have diversified approximately 94 mya. The stem age of diversification of Amylosporus is estimated to be around 62 mya. The clade of Amylosporus is further split into two sister clades, each with an estimated diversification age around 45 mya. Similarly, the other major clade consisted of Bondarzewia, Heterobasidion, Gloiodon, Laurilia, Lauriliella, and Wrightoporia. The estimated stem age of the clade is approximately 90 mya.

3.3. Taxonomy

3.3.1. Amylosporus Sect. Amylosporus

Type: Amylosporus campbellii (Berk.) Ryvarden, Norw. J Bot. 24: 217 (1977).
Etymology: The epithet of the section “Amylosporus” follows the name of the genus Amylosporus.
Key characteristics of the section: Basidiomata pileate and generative hyphae with clamp connections.
Morphological description: Basidiomata pileate and stipitate, growth habit mostly annual, rarely perennial, pore 2–6 per mm, pore surface whitish-cream to pinkish when fresh, slightly brownish to ochraceous when dry, generative hyphae with single and multiple clamp connections, gloeoplerous hyphae usually present, rarely absent. Ecologically, species of this section are associated with angiosperm wood, may cause wood rot, or are found saprotrophically under grasses.
Known distribution: Species in this section are wide-spread. Amylosporus campbellii is mainly a subtropical species and can be found in tropical and subtropical regions of Africa, southern North America, Central and South America, Southeast Asia [2,46,47,48,49], and temperate Europe [16]. Amylosporus guaraniticus is distributed in humid–subtropical region of Paraguay, South America, and found on buried logs [17]. Amylosporus succulentus, A. sulcatus, and the proposed new species A. wadinaheezicus are found in subtropical regions of Asia [14,18]. Amylosporus deadaliformis G.Y. Zheng and Z.S. Bi is a subtropical species, reported from Guangdong Province, southeast China [50]. Similarly, Amylosporus auxiliadorae Drechsler-Santos and Ryvarden, distributed in the tropical region of northeast Brazil [51]. Similarly, one unnamed species A. sp. (IJ-2014_IJV29-1, IJ-2014_IJV29-2), distributed in East Africa, and another unnamed A. sp. (BAB-5055) in India.
Notes: Currently there are seven named and two unnamed species in A. sect. Amylosporus, viz. A. auxiliadorae, A. campbellii, A. deadaliformis, A. guaraniticus, A. succulentus, A. sulcatus, A. wadinaheezicus, A. sp. (IJ-2014_IJV29-1, IJ-2014_IJV29-2), and A. sp. (BAB-5055). Sequence data (ITS and 28S) are available for all these species except A. auxiliadorae and A. deadaliformis.
Stem age and phylogenetic support: The estimated stem age of the section is approximately around 45 mya, and PPs is 1 in the MCC tree (Figure 3), strong phylogenetic support in both ML and BI analyses (BT 100%, PP 0.99; Figure 2).

3.3.2. Amylosporus Sect. Resupinati S. Hussain, Al-Sadi, Al-Yahya’ei and R. Velazhahan, Sect. Nov.

MycoBank No: 853625
Type: Amylosporus annosus Y.C. Dai, P. Du, and X.H. Ji, Phytotaxa 424: 295 (2019).
Etymology: The epithet “Resupinati” refers to the resupinate type of basidiomata, which is a common character in the species of this section.
Key characteristics of the section: Basidiomata resupinate to effused-reflexed, and generative hyphae without clamp connections (except Amylosporus bracei).
Morphological description: Basidiomata resupinate or effused-reflexed, growth habit perennial or annual, pores 3–10 per mm, pore surface whitish-cream to yellowish, generative hyphae simple septate, multiple clamp connections only present in A. bracei, gloeoplerous hyphae usually present, rarely absent, basidia regularly four-spored, rarely eight-spored, basidiospores subglobse to ellipsoid. Ecologically, species of this section are associated with angiosperm trees, causing white rot; some species are wood decomposers.
Known distribution: Species in this section are distributed in tropical regions. Amylosporus annosus reported from tropical Southeast Asia, only known from its type of location, Malaysia [15]). Amylosporus casuarinicola is a subtropical species, reported from the southwest coastal region of Beihai, Guangxi, China [52]. Amylosporus bracei is a tropical species, distributed in different parts of the world, viz. Belize, Martinique Island, Central America; Sao Paulo, Brazil, South America; Florida, North America [13]. This is the only species in the section with clamped generative hyphae. Amylosporus efibulatus (I. Lindblad and Ryvarden) Y.C. Dai, Jia J. Chen, and B.K. Cui found in tropical Central America [13]. Amylosporus rubellus has been reported from Beijing, China, with a monsoon-influenced humid continental climate [13]. Similarly, A. ryvardenii Stalpers is another tropical species, reported from East Africa [53].
Notes: Currently there are six named species in the A. sect.: Resupinati, viz. A. annosus, A. bracei, A. casuarinicola, A. rubellus, A. efibulatus, and A. ryvardenii, and two unnamed species: A. sp. (JV-1809-4) from the USA [13] and A. sp. (Dai 22165) from China [52]. Sequence data (ITS and 28S) are available for the first four named species and the two unnamed species.
Stem age and phylogenetic support: The estimated stem age of the section is approximately 45 mya, with PPs of one in the MCC tree (Figure 3), and excellent phylogenetic support in both ML and BI analyses (BT 100%, PP 0.99; Figure 2).

3.3.3. Amylosporus wadinaheezicus S. Hussain, Al-Sadi, Al-Yahya’ei, Al-Kharousi, and A. Al-Owaisi, sp. Nov. Figure 4 and Figure 5

MycoBank No: 853624
Holotype: Sultanate of Oman: Dhofar: Wadi Naheez, on soil probably on underground wood, below Anogeissus dhofarica trees, 7 August 2022, S. Hussain, A. Al-Owaisi, Al-Yahya’ei, and Al-Sadi, NHZ-22-004 (Holotype Mawarid-NHZ-22-004), GenBank accessions: ITS = PP681308, 28S = PP681313, Tef1-α = PP683472.
Etymology: The specific epithet ‘wadinaheezicus’ refers to the holotype location Wadi Naheez, located in the south of the Sultanate of Oman.
Description: Basidiomata annual, pileate, centrally stipitate, laterally fused pielei, solitary, moist and juicy when fresh, in some specimens with a release of pinkish, juicy droplets, becoming corky and light in weight upon drying. The pileus is circular to semicircular, projecting up to 5 cm long, 15 cm wide, 3 cm thick at the base, with a depressed center, thinner towards the margins, margin undulating, obtuse. The pileus surface is creamy-whitish to pinkish, at the center dark pinkish to pale brownish, becoming pale yellowish on drying, cottony. The pore surface creamy to white when fresh, pale yellowish on drying, pores circular to angular, 2–4 per mm; sterile margin thin, indistinct, and up to 1 mm wide; dissepiment up to 150 µm thick, with lacerate mouth. The context is creamy to light pinkish, fleshy and moist in fresh conditions, pale brownish and corky when dry, and up to 2 cm thick. The tubes are whitish when dry, becoming pale brownish upon drying, and up to 1 cm long. Stipe 1–5 × 2–2.5 cm, stout, thick, pinkish to pale brownish when fresh, becoming brownish on drying, moist.
Smell pleasant when fresh, pungent when dried.
Hyphal system dimitic. Tramal generative hyphae simple septate, rarely branched, with single clamp connection, skeletal hyphae thick-walled, dextrinoid, CB+; contextual generative hyphae simple septate with multiple clam connections, skeletal hyphae frequently branched, think-walled, inflated in KOH. Context generative hyphae dominant, hyaline, with multiple clamp connections, thin-walled, frequently branched, 8.5–15.5 µm in diam; skeletal hyphae frequent, thick-walled with a narrow to wide lumen, branched, flexuous, hyaline, 3–9 µm in diam; gloeoplerous hyphae frequent, rarely branched, hyaline, thin-walled, simple septate, with multiple clamp connections, with granular or oily internal contents, 6–11 µm in diam. Tubes generative hyphae dominant, hyaline, thin-walled, rarely branched, with single clamp connection, 3–5 µm in diam; skeletal hyphae, hyaline, rarely branched, thick-walled, with wide lumen, 3–4.5 µm in diam; gloeoplerous hyphae absent; cystidia and cystidioles absent; basidia 40–58 × 7–9 µm, clavate, with a basal simple septum and four sterigmata, hyaline, smooth. Basidiospores oblong to ellipsoid, hyaline, thin-walled, finely asperulate, CB+, IKI+; (4.0) 4.5–5.0 (6.0) × (2.5) 3.0–3.5 (4.0) µm, Q = 1.4–1.7, av. Q = 1.5, average length × width = 5 × 3.3 µm (n = 90/4).
Habit, habitat, and distribution: Saprotrophic, solitary, under the trees (probably with the roots) of Anogeissus dhofarica A.J. Scott (family Combretaceae). Fruiting bodies of the fungus occurring during monsoon season, from July to September, widespread in Southern Oman.
Jof 10 00625 g004
Figure 4. Basidiomata of Amylosporus wadinaheezicus, (A,B); Mature basidiomata NHZ-22-004 (holotype), (C,D); HOD-23-012, (E); and DRB-23-009, (F–H). Pore surface under stereo microscope (NHZ-22-004).
Figure 4. Basidiomata of Amylosporus wadinaheezicus, (A,B); Mature basidiomata NHZ-22-004 (holotype), (C,D); HOD-23-012, (E); and DRB-23-009, (F–H). Pore surface under stereo microscope (NHZ-22-004).
Jof 10 00625 g004
Additional specimens examined: SULTANATE of OMAN: Dhofar, Salalah, Wadi Naheez, below Anogeissus dhofarica trees, 7 August 2022, S. Hussain, A. Al-Owaisi, Al-Yahya’ei and Al-Sadi, NHZ-22-004a (Mawarid-NHZ-22-004a), GenBank accession: ITS = PP681309; Wadi Jahaneen, below Anogeissus dhofarica trees, 8 August 2022, S. Hussain, A. Al-Owaisi, Al-Yahya’ei and Al-Sadi, JHN-22-009 (Mawarid-JHN-22-009), GenBank accessions: ITS = PP681311, 28S = PP681314, Tef1-α = PP683473; same area and same date, S. Hussain, A. Al-Owaisi, Al-Yahya’ei and Al-Sadi, JHN-22-006 (Mawarid-JHN-22-006), GenBank accessions: ITS = PP681310, 28S = PP681316, Tef1-α = PP683475; Attin, below Anogeissus dhofarica trees, 6 September 2022, A. Al-Owaisi, SALALAH-002 (Mawarid-SALALAH-002); GenBank accessions: ITS = PP697985; 28S = PP681315, Tef1-α = PP683474; Wadi Darbat, below Anogeissus dhofarica trees, 26 August 2023, S. Hussain and M. Al-Jahwari, DRB-23-009 (Mawarid-DRB-23-009); Mirbat, on soil, under grasses, 21 August 2023, S. Hussain and M. Al-Jahwari, MRT-23-001 (Mawarid-MRT-23-001; Anghetat (the place of Prophet Hood’s tomb Peace Be Upon Him), on soil, with mosses, 27 August 2023, S. Hussain and M. Al-Jahwari, HOD-23-012 (Mawarid-HOD-23-012), GenBank accession: ITS = PP681312.
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Figure 5. Illustration of anatomical characters of Amylosporus wadinaheezicus (holotype NHZ-22-004). (A) Basidia, (B) Basidiospores, (C) Contextual generative hyphae, (D) Gloeoplerous hyphae, (E) Contextaul skeletal hyphae, and (F) Tube generative hyphae. Scale bars: (A) = 10 µm, (B) = 5 µm, and (C–F) = 7 µm.
Figure 5. Illustration of anatomical characters of Amylosporus wadinaheezicus (holotype NHZ-22-004). (A) Basidia, (B) Basidiospores, (C) Contextual generative hyphae, (D) Gloeoplerous hyphae, (E) Contextaul skeletal hyphae, and (F) Tube generative hyphae. Scale bars: (A) = 10 µm, (B) = 5 µm, and (C–F) = 7 µm.
Jof 10 00625 g005
Notes: The new species is distinguished by a pileate stipitate basidiomata, fleshy and soft, pinkish cap surface with pale brownish to dark pinkish center, creamy to pinkish pore surface, simple septate and multi-clamped generative hyphae. The new species Amylosporus wadinaheezicus is widespread in Dhofar region, southern Oman, where it was found as saprotrophic on forest floor under grasses, open fields, pastures, simply everywhere in the area which is impacted by the monsoon season. Most probably, the species is associated with underground wood, or it only grows on roots of Anogeissus dhofarica, perhaps it could be an endemic species to this region. Using ML and BI analyses, Amylosporus wadinaheezicus fall in the clade consisting of the proposed A. sect. Amylosporus. Species in A. sect. Amylosporus share plileate basidiomata with creamy pinkish to pale brownish pileus surface, whitish to pale brownish pore surface, and clamped generative hyphae. Amylosporus auxiliadorae associated with angiosperm wood, with pale brownish pileus surface, pore surface pale yellowish, contextual skeletal hyphae shorter in diam (up to 7 µm), absence of gloeoplerous hyphae in context, basidiospores ellipsoid to ovoid, finely asperulate, measuring 4.0–5.0 × 2.5–4.0 µm [51]. This species is only known from type locality, northeast Brazil, and sequence data are not available for this species [51]. Amylosporus succulentus shares the pileate basidiomata and whitish pore surface with A. wadinaheezicus. Amylosporus succulentus with centrally or laterally stipitate basidiomata, smaller stipe (up to 1 cm in length), smaller basidia (10.0–15.0 × 5.0–8.5 µm), and presence of gloeoplerous hyphae in tube tissues in contrast to the new species [14]. Amylosporus campbellii and A. wadinaheezicus share the terrestrial growth habit and basidiomata color. Both species were found under grasses, with more or less circular pileus [46]. Amylosporus campbellii is discernible from the new species by its (i) gloeoplerous hyphae present in both context and tube tissues, and (ii) substantially smaller basidia, measuring 10.0–20.0 × 7.0–8.5 µm. Amylosporus sulcatus with annual to perennial basidiomata associated with dead trunk of angiosperms, pileus surface snow white, pale pinkish cinnamon to pale brownish, pore surface snow white to pale brownish, gloeoplerous hyphae present in both contextual and stipe tissues, basidia 27.0–80.0 × 6.0–12.0 µm, 4-spored, clavate, with basal simple septum, basidiospores ellipsoid to ovoid, hyaline, measuring 3.6–5.7 × 2.7–3.6 µm [18]. Amylosporus guaraniticus has pileate sessile basidiomata, associated with underground log, with semicircular pileus, cap surface whitish to pale brownish or dark brown, pore surface creamy to light brown, gloeoplerous hyphae present in contextual tissues, basidia clavate, 4-spored, hyaline, smaller, measuring 10.0–25.0 × 5.0–8.0 µm, basidiospores ellipsoid, hyaline, finely asperulate, 4.0–5.5 × 3.0–4.0 µm [17]. Amylosporus daedaliformis with characteristic daedaliform shaped pores, gloeoplerous hyphae only present in tramal tissues, unbranched skeletal hyphae, basidiospores ellipsoid, smooth, measuring 5.0–6.0 × 2.5–3.5 µm [50].

3.3.4. Key to the Known Species of Amylosporus

A taxonomic key to the known species of Amylosporus is presented below. This key is based on the growth habit of basidiomata (pileate or resupinate) and the presence or absence of clamp connections in generative hyphae. These are the two main morphological characters for the recognition of the proposed sections in the genus.
  • Growth habit of basidiomata pileate, and presence of clamps in generative hyphae—Amylosporus sect. Amylosporus. 2
    -
    Growth habit of basidiomata resupinate or effused-reflexed—Amylosporus sect. Resupinati. 7
2.
Basidiomata annual or perennial, gloeoplerous hyphae present in both contextual and stipe tissues with large basidia measuring 27.0–80.0 × 6.0–12.0 µm. A. sulcatus
-
Basidiomata only annual. 3
3.
Basidiomata eccentrically stipitate, pore surface buff clay, no. of pore 3–6 per mm, will smallest basidia in the genus measuring 10.0–15.0 × 6.0–8.0 µm. A. auxiliadorae
-
Basidiomata pileate stipitate or sessile, pore surface creamy-white to brownish. 4
4.
Basidiomata laterally stipitate, circular to semicircular, appearing in lawn, stipe up to 1 cm in length, pores 2–4/mm, basidiomata watery. A. succulentus
-
Basidiomata sessile. 5
5.
Basidiomata sessile, imbricate to semicircular, brownish pore surface, associated with buried logs. A. guaraniticus
-
Basidiomata stipitate. 6
6.
Basidiomata sessile or stipitate, pores daedaliform shape at maturity, basidiospores smooth, measuring 5.0–6.0 × 2.5–3.5 µm. A. daedaliformis
-
Basidiomata centrally stipitate, gloeoplerous hyphae only present in context, absent in tube tissues, basidia larger, measuring 40–58 × 7–9 µm. A. wadinaheezicus
7.
Generative hyphae septate and with multiple clamp connections. A. bracei
-
Generative simple septate and without clamp connection. 8
8.
Basidiomata thin, less than 5 mm thick. A. efibulatus
-
Basidiomata thick, greater than 5 mm thick. 9
9.
Basidiomata perennial, basidia eight-spored. A. annosus
-
Basidiomata annual, basidia four-spored. 10
10.
Basidiospores up to 4 µm long, 3.5–4.0 × 2.7–3.2 µm. A. casuarinicola
-
Basidiospores > 4 µm long. 11
11.
Basidiospores 4.0–6.0 × 3.0–4.2 µm, Q values 1.33 to 1.42. A. rubellus
-
Basidiospores 4.0–5.0 × 2.5–3.0 µm, Q value 1.6. A. ryvardenii

4. Discussion

Bondarzewiaceae is an ecologically diverse family in Russulales; some of the members are forest tree pathogens, while the majority of the species are wood-rotting fungi [2,3,4,5,6,7]. Currently, the family comprises nine genera and approximately 90 species, where most of these genera are associated with gymnosperm wood; however, genera like Amylosporus and Stecchericium are exclusively associated with angiosperm wood [2,3,4,5,6,13].
In the current taxonomy, Bondarzewiaceae consisted of Amylaria, Amylosporus, Bondarzewia, Heterobasidion, Gloiodon, Laurilia, Lauriliella, and Wrightoporia [8]. Among these genera, the systematic position of Amylosporus and Wrightopori has been in flux. Because Wrightopori was a polyphyletic genus, and both Amylosporus and Wrightoporia have been treated as unclassified genera in Russulales [2]. Some studies classified both the genera in Wrightoporiaceae [6,13,14,15], while some studies placed Wrightoporia in Wrightoporiaceae and Amylosporus as an unassigned genus in Russulales [54]. In the current study, the phylogenetic analyses of the family were evaluated based on combined ITS-28S sequence data of all genera of the family (except Amylaria, for which sequence data are unavailable). Two major clades were revealed using ML, BI, and time divergence estimation. One major clade consisting of Amylosporus, Stecchericium, and Wrightoporia austrosinensis with moderate support in ML analysis (BT 85%) and excellent support in BI analysis (PPs 0.96). Species in this major clade are associated with conifers, except Wrightoporia austrosinensis. The other major clade consisted of Bondarzewia, Heterobasidion, Gloiodon, Laurilia, Lauriliella, and Wrightoporia. The monotypic genus Laurilia sulcata, three species of Gloidon such as G. nigrescens (Petch) Maas Geest., G. stratosus (Berk.) Banker, G. strigosus (Sw.) P. Karst., and some species of Bondarzewia are associated with angiosperm wood [55,56]. However, the majority of the species in other genera of the family are exclusively associated with conifers [6,13,57].

4.1. Ecology and Distribution of Species of the Genera of Bondarzewiaceae

4.1.1. Amylaria Corner

Amylaria is a monotypic, clavorioid genus with a single species, A. himalayensis Corner. The taxon is only known from Bhutan and Nepal [58]. The samples were found on the forest floor, around 2800 m in Nepal and 3000 m in Bhutan, among moss or on rotting buried wood at the base of a conifer tree [59]. The genus has been placed in Bondarzewiaceae according to the recent systematics reports [7]. Since no sequence data are unavailable and no report of the genus has been made after the original description, we think the systematic position of the taxon in Bondarzewiaceae is questionable [59].

4.1.2. Amylosporus Ryvarden

There are 13 known species and one proposed new species in the genus Amylosporus. There are two main morphological characters: (i) the growth habit of basidiomata (pileate or resupinate) and (ii) the presence or absence of clamp connections in generative hyphae. Both these characters were employed for recognition of the proposed sections in the genus. The distribution and ecological association of each species in the genus are already discussed in the Taxonomy section. One species in section Resupinati, Amylosporus bracei, has clamp connections in generative hyphae, indicating that this character evolved twice during the course of the evolution of Amylosporus. The new species Amylosporys wadinaheezicus is most probably associated with underground wood, or it only grows on roots of Anogeissus dhofarica; perhaps it could be an endemic species to this region of the Arabian Peninsula.

4.1.3. Bondarzewia Singer

In Bondarzewia, there are 16 species according to Index Fungorum (https://www.indexfungorum.org/names/Names.asp; accessed on 22 July 2024). The genus is characterized by pileate stipitate to substipitate basidiomata, and a dimitic hyphal system, the presence of lactiferous hyphae, with ornamented and amyloid basidiospores [60]. Some species in the genus are edible and have medicinal potential, such as Bondarzewia mesenterica (Schaeff.) Kreisel, according to the list of World’s Edible Mushroom [61]. Species in the genus are mostly associated with conifers; however, some are hosted by angiosperm trees. Bondarzewia mesenterica is the type species of genus. The species that are associated with flowering trees include Bondarzewia berkeleyi (Fr.) Bondartsev and Singer, distributed in temperate areas of eastern North America and Europe, associated with Fagaceae as tree pathogens [6], B. dickinsii (Berk.) Jia J. Chen, B.K. Cui, and Y.C. Dai has been reported from Japan to eastern China, associated with the fallen wood of Quercus species and the roots of Castanea species [62]; B. guaitecasensis (Henn.) J.E. Wright is a South American species associated with Nothofagus [63,64], B. kirkii J.A. Cooper, Jia J. Chen, and B.K. Cui reported from New Zealand, associated with the roots of Fuscopora fusca [62]. Other species, such as, B. occidentalis Jia J. Chen, B.K. Cui, and Y.C. Dai; B. podocarpi Y.C. Dai and B.K. Cui; B. propria (Lloyd) J.A. Cooper; B. retipora (Cooke) M.D. Barrett; B. submesenterica Jia J. Chen, B.K. Cui, and Y.C. Dai; B. tibetica B.K. Cui, J. Song, and Jia J. Chen; and B. zonata K. Das, A. Parihar and Hembrom are associated with gymnosperms [60,62,65,66]. Some species, such as B. mesofila R. Valenz., Baut.-Hern. and Raymundo are recently described species from tropical Mexico, which grow in the soil as saprotrophic mushrooms [67].

4.1.4. Gloiodon P. Karst

Gloiodon is a small, hydnoid mushroom genus with resupinate or effused-reflexed basidiomata, with four known species. Gloiodon occidentalis Ginns has been reported from Canada, associated with the dead wood of Tsuga heterophylla [55]. The other species, such as G. nigrescens (Petch) Maas Geest., G. stratosus (Berk.) Banker, and G. strigosus (Sw.) P. Karst., are associated with angiosperm wood [55,56].

4.1.5. Heterobasidion Bref.

Heterobasidion is an important white rot pathogenic poroid fungi, characterized by effused-reflexed to sessile basidiomata, dimitic hyphal system with dextrinoid skeletal hyphae, generative hyphae without clamp connections, and finely asperulate and nonamyloid basidiospores, distributed in the Northern and Southern Hemisphere [57]. The genus consisted of 18 species, mainly associated with conifers [57]. Heterobasidion abietinum Niemelä and Korhonen, distributed in Italy, associated with Abies alba and Picea abies; H. amyloideum Y.C. Dai, Jia J. Chen and Korhonen with Abies in Tibet China; H. annosum (Fr.) Bref. from Italy and Russia, associated with different species Pinus; H. araucariae P.K. Buchanan with trees of Araucaria cunninghamii, reported from Australia; H. armandii Y.C. Dai, Jia J. Chen and Yuan Yuan with Pinus armandii, found in China; H. australe Y.C. Dai and Korhonen from China, associated with Pinus species; H. insulare (Murrill) Ryvarden from China in association with Pinus massoniana; H. irregulare Garbel. and Otrosina is a South American species associated with Pinus species; H. linzhiense Y.C. Dai and Korhonen is a Chinese species associated with trees of Abies and Picea species; H. occidentale is pathogenic to various trees of conifers; H. orientale Tokuda, T. Hatt. and Y.C. Dai associated with fallen conifer trunk, reported from China; H. parviporum Niemelä and Korhonen associated with Picea abies, distributed in Europe and Asia; H. subinsulare Y.C. Dai, Jia J. Chen and Yuan Yuan is a recently reported species from China, associated with wood of Pinus species; H. subparviporum Y.C. Dai, Jia J. Chen and Yuan Yuan with wood of Abies and Picea, reported from China; and H. tibeticum Y.C. Dai, Jia J. Chen and Korhonen with Pinus wood from China [57].

4.1.6. Laurilia Pouzar

Laurilia is a monotypic genus with L. sulcata (Burt) Pouzar, characterized by effuse-reflexed basidiomata with smooth to tuberculate hymenophore, trimitic hyphal system [54]. Laurilia sulcata is a widely distributed species in boreal conifer forests in the northern hemisphere [54].

4.1.7. Lauriliella S.H. He and Nakasone

Lauriliella is a perennial genus with effused-reflexed, pileate or umbonate, woody basidiomata, hymenophore smooth to tuberculate, basidia with basal clamp connections, basidiospores broadly ellipsoid to subglobose, hyaline, thick-walled, echinulate, and amyloid [54]. The genus comprises two species, namely, L. taxodii (Lentz and H.H. McKay) S.H. He and Nakasone, and L. taiwanensis S.H. He and Nakasone. Lauriliella taxodii are distributed in USA, causing white stringy rot or brown powdery rot in living Taxodium distichum. Similarly, L. taiwanensis is reported from Taiwan, causing white rot in living Chamaecyparis formosensis [54].

4.1.8. Stecchericium D.A. Reid

Stecchericium with dimitic hyphal system, clamped generative hyphae and skeletal hyphae, variable types of cystidia in the hymenium, and amyloid basidiospores [7]. Species of the genus are wood decaying mushrooms, associated with angiosperms, currently with six species, and typified with Stecchericium seriatum (Lloyd) Maas Geest. [7]. According to MycoBank, this genus belongs to Wrightoporiaceae; however, recent studies [7,8,9] and Index Fungorum classified Stecchericium in Bondarzewiaceae. The known species in the genus are: Stecchericium abditum Maas Geest., found on rotten log in Australia [68], S. acanthophysium T. Hatt. and Ryvarden on hardwood reported from Japan [69], S. isabellinum Corner associated with fallen wood in the Amazon forest [70], and S. rusticum Maas Geest., on dead wood in Singapore [71]. Stecchericium fistulatum (G. Cunn.) D.A. Reid, which was the type species of the genus, is now considered a synonym of S. seriatum (Lloyd) Maas Geest. [72]. Stecchericium dimiticum Douanla-Meli is associated with angiosperm wood, reported from Cameroon [73].

4.1.9. Wrightoporia Pouzar

Wrightoporia is a large and diverse genus of wood decaying tropical polypores and has been shown to be polyphyletic [6]. The systematic position of the genus has been in flux; initially it was placed in Wrightoporiaceae [74], transferred to Hericiaceae [53], and according to Index Fungorum and recent studies, the genus has been placed in Bondarzewiaceae [7,8,9]. However, MycoBank still considered Wrightoporia in Wrightoporiaceae [accessed on 20 July 2024]. The type species of the genus is Wrightoporia lenta (Overh. and J. Lowe) Pouzar [75]. The generic circumscription of the genus has recently been revised [13]. According to the recent definition, Wrightoporia s.str. is distinguished by an annual growth pattern, resupinate to effused-refluxed basidiomata, soft and cottony at fresh condition, membranous to cottony at dry condition, pores rounded to angular, 1–4/mm, margins mostly having rhizomorphs, skeletal hyphae narrow with 0.8–2.5 µm in diam, basidiospores finely asperulate, mostly found on dead logs of gymnosperms, rarely on angiosperms. Currently, there are six species in the genus, distributed in Asia: Wrighoporia austrosinensis Y.C. Dai, W. avellanea (Bres.) Pouzar, W. borealis Y.C. Dai, W. lenta, W. srilankensis Y.C. Dai and Yuan Yuan, and W. subavellanea Jia J. Chen and B.K. Cui [13,76,77]. Cysidia is absent in these species; however, in Wrightoporia austrosinensis, cystidia and cystidiols are present [78]. Interestingly, in a recent phylogenetic analysis, W. austrosinensis formed an independent lineage outside of the genus [77]. A similar phylogenetic position of W. austrosinensis outside of Wrightoporia was observed during this study. This species could not be a member of Wrightoporia; perhaps it could be included either in Amylosporus or may be treated as an independent genus.

5. Conclusions

It is concluded from this study that members of Bondarzewiaceae are associated with angiosperm or gymnosperm wood, causing white rot in tree species. Microscopically, the species with dimitic hyphal system except Laurilia with trimitic hyphal system. Wrightoporia austrosinensis is not a species in Wrightoporia; it is suggested that it could be an independent genus or a species in Amylosporus.

Author Contributions

Conceptualization, S.H., M.A.-K. and M.N.A.-Y.; methodology, S.H., A.A.A.-O. and D.A.-M.; software, S.H.; validation, S.H., A.M.A.-S., R.V. and M.N.A.-Y.; formal analysis, S.H. and A.A.A.-O.; investigation, S.H., A.A.A.-O., M.A.-K. and D.A.-M.; resources, M.N.A.-Y. and A.M.A.-S.; data curation, S.H., A.A.A.-O. and M.A.-K.; writing—original draft preparation, S.H.; writing—review and editing, S.H., A.A.A.-O., M.N.A.-Y. and R.V.; visualization, S.H., M.A.-K. and A.A.A.-O.; supervision, A.M.A.-S., R.V. and M.N.A.-Y.; project administration, M.N.A.-Y.; funding acquisition, M.N.A.-Y. and A.M.A.-S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Agriculture and Fisheries Development Fund, Sultanate of Oman (grant number 104/1/1).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding authors.

Acknowledgments

We express our gratitude to Bader Al Quyudhi, Shamsa Al Balushi, and Maryam Al Hinai for their indispensable assistance during the Dhofar Region sample expedition, which was crucial to our research. Additionally, we are grateful to Mohammed Al Jahwari and Amer Qattan for their leadership and assistance during the project.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Map of the sampling sites, the Dhofar Governorate, located in south of Oman, the region consisting of lush wades and mountains, the photos showing some parts of the study area (Wadi Darbat with GPS coordinates: 17°07′ N, 54°43′ E; Wadi Jarzeez GPS coordinates: 17°13′ N, 54°05′ E; Wadi Rakhyut GPS coordinates: 16°80′ N, 53°42′ E). The pink dots represent sampling sites.
Figure 1. Map of the sampling sites, the Dhofar Governorate, located in south of Oman, the region consisting of lush wades and mountains, the photos showing some parts of the study area (Wadi Darbat with GPS coordinates: 17°07′ N, 54°43′ E; Wadi Jarzeez GPS coordinates: 17°13′ N, 54°05′ E; Wadi Rakhyut GPS coordinates: 16°80′ N, 53°42′ E). The pink dots represent sampling sites.
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Figure 2. Maximum likelihood phylogeny of family Bondarzewiaceae based on combined ITS-28 sequences; values above the nodes are maximum likelihood bootstrap (BT) and Bayesian posterior probabilities (PPs), with Amylonotus labyrinthinus (Yuan 1475) as outgroup. Species within the family were recovered in two clades. Clade-I consists of genus Amylosporus, Stecchericium and a species of Wrightoporia W. austrosinens, with moderate ML (BT 85%) and excellent BI support (PPs 1). Species in Amylosporus are further split into two sister clades: one sister clade with species having pileate basidiomata and clamped generative hyphae, representing the proposed section A. sect. Amylosporus; and the other sister clade with taxa having resupinate to effused-reflexed basidiomata and generative hyphae without clamp connections, making the section A. sect. Resupinati. Clade-II consisted of genera: Bondarzewia, Heterobasidion, Gloiodon, Laurilia, Lauriliella, and Wrightoporia, with excellent phylogenetic support in both analyses (BT 100%, PPs 1). The associated wood type, either angiosperm or gymnosperm are represented with their respective tree icon. Sequences of the new species Amylosporus wadinaheezicus are shown in bold font.
Figure 2. Maximum likelihood phylogeny of family Bondarzewiaceae based on combined ITS-28 sequences; values above the nodes are maximum likelihood bootstrap (BT) and Bayesian posterior probabilities (PPs), with Amylonotus labyrinthinus (Yuan 1475) as outgroup. Species within the family were recovered in two clades. Clade-I consists of genus Amylosporus, Stecchericium and a species of Wrightoporia W. austrosinens, with moderate ML (BT 85%) and excellent BI support (PPs 1). Species in Amylosporus are further split into two sister clades: one sister clade with species having pileate basidiomata and clamped generative hyphae, representing the proposed section A. sect. Amylosporus; and the other sister clade with taxa having resupinate to effused-reflexed basidiomata and generative hyphae without clamp connections, making the section A. sect. Resupinati. Clade-II consisted of genera: Bondarzewia, Heterobasidion, Gloiodon, Laurilia, Lauriliella, and Wrightoporia, with excellent phylogenetic support in both analyses (BT 100%, PPs 1). The associated wood type, either angiosperm or gymnosperm are represented with their respective tree icon. Sequences of the new species Amylosporus wadinaheezicus are shown in bold font.
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Figure 3. Maximum clade credibility (MCC) tree of Bondarzewiaceae obtained from BEAST analysis based on ITS-28S dataset comprises 52 specimens including the outgroup taxon Amylonotus labyrinthinus (Yuan 1475). The dataset represents all the genera which belonging to Bondarzewiaceae according to Index Fungorum and Outlines of Fungi, except Amylaria, for which no sequence data are available. Taxa in the family recovered into two clades, in congruence to ML and BI analyses. One clade with an estimated stem age of diversification of approximately 94 mya, consisting of genus Amylosporus, Stecchericium, and Wrightoporia austrosinens. The horizontal dashed line separate Amylosporus for the rest of the genera of the family. The other clade with estimated stem age of divergence around 90 mya, consisting of Bondarzewia, Heterobasidion, Gloiodon, Laurilia, Lauriliella, and Wrightoporia. The 95% highest posterior density of divergence time estimations is marked by horizontal bars.
Figure 3. Maximum clade credibility (MCC) tree of Bondarzewiaceae obtained from BEAST analysis based on ITS-28S dataset comprises 52 specimens including the outgroup taxon Amylonotus labyrinthinus (Yuan 1475). The dataset represents all the genera which belonging to Bondarzewiaceae according to Index Fungorum and Outlines of Fungi, except Amylaria, for which no sequence data are available. Taxa in the family recovered into two clades, in congruence to ML and BI analyses. One clade with an estimated stem age of diversification of approximately 94 mya, consisting of genus Amylosporus, Stecchericium, and Wrightoporia austrosinens. The horizontal dashed line separate Amylosporus for the rest of the genera of the family. The other clade with estimated stem age of divergence around 90 mya, consisting of Bondarzewia, Heterobasidion, Gloiodon, Laurilia, Lauriliella, and Wrightoporia. The 95% highest posterior density of divergence time estimations is marked by horizontal bars.
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Table 1. Taxa used in phylogenetic analyses, presented here as appeared in Figure 2 and Figure 3, bold fonts represent the new species.
Table 1. Taxa used in phylogenetic analyses, presented here as appeared in Figure 2 and Figure 3, bold fonts represent the new species.
Genus/SectionSpeciesHerbarium VoucherCountry of OriginGenBank Accession
ITS28S
Amylosporus sect. AmylosporusAmylosporus wadinaheezicusJHN-22-006OmanPP681310PP681316
Amylosporus wadinaheezicusSALALAH-002OmanPP697985PP681315
Amylosporus wadinaheezicusJHN-22-009OmanPP681311PP681314
Amylosporus wadinaheezicusNHZ-22-004OmanPP681308PP681313
Amylosporus sulcatusGXU 1084ChinaMG280818MG280819
Amylosporus sulcatusGXU 1095ChinaMG280820MG280821
Amylosporus sp.IJ-2014_IJV29-2TanzaniaKM851314KM593892
Amylosporus sp.IJ-2014_IJV29-1TanzaniaKM851315KM593893
Amylosporus campbellii0806-20aJamaicaJF692200KJ807077
Amylosporus campbelliiGilbertson_14806USAKM107861KM107879
Amylosporus guaraniticusM._Campi_106ParaguayMF377528MF377529
Amylosporus guaraniticusM._Campi_105ParaguayMF377530-
Amylosporus succulentusDai_7802ChinaKM213669KM213671
Amylosporus succulentusDai_7803ChinaKM213668KM213670
Amylosporus sect. ResupinatiAmylosporus annosusBJFC-Dai_18640MalaysiaMH647059MH647055
Amylosporus annosusBJFC-Dai_18638MalaysiaMH647058MH647054
Amylosporus annosusBJFC-Dai_18635MalaysiaMH647057MH647053
Amylosporus annosusBJFC-Dai_18632MalaysiaMH647056MH647052
Amylosporus sp.JV_1809-4USAMN888695MN888696
Amylosporus rubellusDai_9233ChinaKJ807071KJ807084
Amylosporus casuarinicolaDai_6914ChinaKJ807068-
Amylosporus casuarinicolaYuan_1614ChinaKM107862-
Amylosporus bracei1008-77USAKM267724KJ807076
Amylosporus sp.Dai_22165ChinaOL473603OL473616
Wrightoporia s.l.Wrightoporia austrosinensisUC2023009USAKP814178-
Wrightoporia austrosinensisDai 11579ChinaKJ807065KJ807073
StecchericiumStecchericium seriatumCBS:756.81SingaporeMH861476-
Stecchericium seriatumSL1685SingaporeOR527392-
BondarzewiaBondarzewia podocarpiDai 9261ChinaKJ583207KJ583221
Bondarzewia propriaPDD 60293New ZealandKJ583213KJ583227
Bondarzewia occidentalisHHB 14803USAKM243329KM243332
LauriliellaLauriliella taiwanensisFP-101635China: TaiwanKY172891KY172906
Lauriliella taxodiiFP-105464-SpUSAKY172896KY172912
LauriliaLaurilia sulcataHe 20120916-7ChinaKY172894KY172909
Laurilia sulcataKHL 8267RussiaAF506414AF506414
HeterobasidionHeterobasidion amyloideumCui 12656ChinaMT146480MT446029
H. armandiiDai 17605ChinaMT146482MT446031
Heterobasidion abietinum00053/1ItalyKJ651451KJ651509
GloiodonGloiodon nigrescensDesjardin7287BaliAF506450AF506450
Gloiodon strigosusJS26147NorwayAF506449AF506449
Wrightoporia s.str.Wrightoporia srilankensisDai_19621Sri LankaMN688691MN688684
Wrightoporia srilankensisDai_19667Sri LankaMN688692MN688685
Wrightoporia srilankensisDai_19500Sri LankaMN688690MN688683
Wrightoporia srilankensisDai_19668Sri LankaMN688693MN688686
Wrightoporia srilankensisDai_19620Sri LankaMN688694MN688687
Wrightoporia avellaneaLR41710JamaicaAF506488AF506488
Wrightoporia lentaDai 10462ChinaKJ513291KJ807082
Wrightoporia lentaCui_7804ChinaKJ513292KJ807081
Wrightoporia subavellaneaDai_11484ChinaKJ513295KJ807085
Wrightoporia subavellaneaDai_11488ChinaKJ513296KJ807086
Wrightoporia subavellaneaDai_11492ChinaKJ513297KJ807087
OutgroupAmylonotus labyrinthinusYuan 1475ChinaKM107860KM107878
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Hussain, S.; Al-Kharousi, M.; Al-Maqbali, D.; Al-Owaisi, A.A.; Velazhahan, R.; Al-Sadi, A.M.; Al-Yahya’ei, M.N. Notes on the Ecology and Distribution of Species of the Genera of Bondarzewiaceae (Russulales and Basidiomycota) with an Emphasis on Amylosporus. J. Fungi 2024, 10, 625. https://doi.org/10.3390/jof10090625

AMA Style

Hussain S, Al-Kharousi M, Al-Maqbali D, Al-Owaisi AA, Velazhahan R, Al-Sadi AM, Al-Yahya’ei MN. Notes on the Ecology and Distribution of Species of the Genera of Bondarzewiaceae (Russulales and Basidiomycota) with an Emphasis on Amylosporus. Journal of Fungi. 2024; 10(9):625. https://doi.org/10.3390/jof10090625

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Hussain, Shah, Moza Al-Kharousi, Dua’a Al-Maqbali, Arwa A. Al-Owaisi, Rethinasamy Velazhahan, Abdullah M. Al-Sadi, and Mohamed N. Al-Yahya’ei. 2024. "Notes on the Ecology and Distribution of Species of the Genera of Bondarzewiaceae (Russulales and Basidiomycota) with an Emphasis on Amylosporus" Journal of Fungi 10, no. 9: 625. https://doi.org/10.3390/jof10090625

APA Style

Hussain, S., Al-Kharousi, M., Al-Maqbali, D., Al-Owaisi, A. A., Velazhahan, R., Al-Sadi, A. M., & Al-Yahya’ei, M. N. (2024). Notes on the Ecology and Distribution of Species of the Genera of Bondarzewiaceae (Russulales and Basidiomycota) with an Emphasis on Amylosporus. Journal of Fungi, 10(9), 625. https://doi.org/10.3390/jof10090625

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