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Article

Bambusicolous Fungi in Pleosporales: Introducing Four Novel Taxa and a New Habitat Record for Anastomitrabeculia didymospora

by
Rungtiwa Phookamsak
1,2,3,4,5,
Hongbo Jiang
1,3,4,6,
Nakarin Suwannarach
7,8,
Saisamorn Lumyong
7,8,9,
Jianchu Xu
2,3,4,5,
Sheng Xu
3,4,5,8,
Chun-Fang Liao
1,10 and
Putarak Chomnunti
1,*
1
School of Science, Mae Fah Luang University, Chiang Rai 57100, Thailand
2
Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China
3
Honghe Center for Mountain Futures, Kunming Institute of Botany, Chinese Academy of Sciences, Honghe 654400, China
4
East and Central Asia Regional Office, World Agroforestry Centre (ICRAF), Kunming 650201, China
5
Centre for Mountain Futures (CMF), Kunming Institute of Botany, Kunming 650201, China
6
Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai 57100, Thailand
7
Research Center of Microbial Diversity and Sustainable Utilization, Faculty of Sciences, Chiang Mai University, Chiang Mai 50200, Thailand
8
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
9
Academy of Science, The Royal Society of Thailand, Bangkok 10300, Thailand
10
Innovative Institute of Plant Health, Zhongkai University of Agriculture and Engineering, Haizhu, Guangzhou 510225, China
*
Author to whom correspondence should be addressed.
J. Fungi 2022, 8(6), 630; https://doi.org/10.3390/jof8060630
Submission received: 19 May 2022 / Revised: 6 June 2022 / Accepted: 7 June 2022 / Published: 13 June 2022
(This article belongs to the Special Issue Ascomycota: Diversity, Taxonomy and Phylogeny)
Browse Figures
Review Reports Versions Notes

Abstract

:
While conducting a survey of bambusicolous fungi in northern Thailand and southwestern China, several saprobic fungi were collected from dead branches, culms and twigs of bamboos, which were preliminarily identified as species belonging to Pleosporales (Dothideomycetes) based on a morphological approach. Multigene phylogenetic analyses based on ITS, LSU, SSU, rpb2, tef1-α and tub2 demonstrated four novel taxa belonging to the families Parabambusicolaceae, Pyrenochaetopsidaceae and Tetraploasphaeriaceae. Hence, Paramultiseptospora bambusae sp. et gen. nov., Pyrenochaetopsis yunnanensis sp. nov. and Tetraploa bambusae sp. nov. are introduced. In addition, Anastomitrabeculia didymospora found on bamboo twigs in terrestrial habitats is reported for the first time. Detailed morphological descriptions and updated phylogenetic trees of each family are provided herein.

1. Introduction

Bamboo is one of the most useful perennial woody grasses that contains the highest amount of living biomass [1]. It belongs to the subfamily Bambusoideae, family Poaceae, comprising about 127 genera, with approximately 1680 species, covering around 25 million hectares in tropical, subtropical, and mild temperate regions of Africa, America, Asia and Oceania, but it is rarely found in Europe [1,2,3,4,5]. Bamboo is important for ecological and socioeconomic sustainability throughout the world. Bamboo forests are crucial for the environmental benefits and climate change mitigation; they are sustainable in soil erosion control, carbon sequestration, soil and water conservation, windbreaks and shelterbelts, land rehabilitation, as well as releasing negative oxygen ions [4,6,7,8,9]. Bamboo has also been utilized for traditional Chinese medicine, food sources, furniture and building construction, musical instruments, paper and textile industries, reinforcing fibers, as well as feedstock for bioethanol and biomethane productions [1,4,7,9,10]. Bamboo is considered to be an eco-friendly plant, but there are also potential problems associated with bamboo’s cultivations such as decreasing biodiversity and soil fertility, soil and water loss, and surface water pollution [7].
Bamboo are highly diverse, distributed worldwide, contain high biomass and are a sustainable carbon source; hence, they host a high diversity of fungi [3,8,11,12,13]. Study into bambusicolous fungi has been carried out since the 18th century, which was first started by Léveillé [14]. Subsequently, many mycologists have described an increasing number of fungi on bamboo, especially ascomycetes [3,11,12,13,15,16,17,18,19]. Recently, more than 1300 fungi have been reported on bamboo, including 150 basidiomycetes and 800 ascomycetes, of which 350 species are reported as asexual morphs [13]. However, many bambusicolous fungi remain poorly clarified in taxonomic classification due to the lack of molecular–phylogenetic approaches [3,12].
Over the last two decades, taxonomic studies of bambusicolous fungi have become an interesting research topic for many Asian mycologists [3,12,13,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54]. The taxonomic classification of bambusicolous fungi based on molecular phylogeny was initially carried out by Tanaka et al. [12], who introduced a novel family Tetraplosphaeriaceae to accommodate tetraploa-like taxa in Pleosporales. Noteworthily, major studies of bambusicolous ascomycetes with modern taxonomic treatments have been carried out by Dai et al. [3], Liu et al. [31,32], Phookamsak et al. [39], and Tanaka et al. [27]. Up to now, more than 175 bambusicolous ascomycetes have been described based on morphological and phylogenetic evidence [13,42,43,44,45,46,47,48,49,50,51,52,53,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70]. However, there have been few thorough studies into the phylogeny-based taxonomy of bambusicolous fungi preceding 2002 [11], causing more than 80% of bambusicolous fungi to lack molecular data that could clarify their phylogenetic placement.
Many families in Pleosporales were initially introduced to accommodate bambusicolous fungi mainly such as Anastomitrabeculiaceae [71], Astrosphaeriellaceae [39], Bambusicolaceae [72], Occultibambusaceae [3], Parabambusicolaceae [27], Pseudoastrosphaeriellaceae [39], Roussoellaceae [32], Shiraiaceae [73] and Tetraploasphaeriaceae [12]. Furthermore, bambusicolous fungi are also distributed among many families in Pleosporales such as Aigialaceae, Dictyosporiaceae, Didymosphaeriaceae, Halotthiaceae, Lentitheciaceae, Ligninsphaeriaceae, Longipedicellataceae, Lophiotremataceae, Periconiaceae, Phaeosphaeriaceae, and Pleosporaceae [27,31,41,49,52,74,75,76,77,78,79,80,81], suggesting that bambusicolous fungi are diverse in Pleosporales. In this study, we also found the bambusicolous fungi in Pleosporales with the intention of providing a better understanding of their taxonomy placement. The aim of this study is to introduce four novel taxa of bambusicolous fungi in Pleosporales based on the morpho-molecular approach.

2. Materials and Methods

2.1. Collection, Examination, Isolation, and Preservation

Samples were collected from the dead branches, culms, and twigs of bamboo in Chiang Mai and Chiang Rai Provinces of Thailand in 2011 and Yunnan Province of China in 2021. The samples were stored in paper bags and brought to the laboratory for observation and examination. Fungal fruiting bodies on host substrates were observed under an Olympus SZ61 series stereo microscope, and a centrum was mounted in sterilized distilled water on a clean slide for examination and captured under a Nikon ECLIPSE Ni compound microscope connected to a Nikon DS-Ri2 camera. Cotton blue was added to observe the fungal centrum, and Indian ink was used to check the mucilaginous sheath covering the ascospores. Morphological features were measured using Tarosoft (R) Image FrameWork version 0.9.7. Photographic plates were edited and combined in Adobe Photoshop CS6 software (Adobe Systems Inc., San Jose, CA, USA). The permanent slides were prepared by adding lacto-glycerol and sealed by nail polish and deposited with herbarium specimens at the Herbarium of Cryptogams Kunming Institute of Botany Academia Sinica (KUN-HKAS), China and the herbarium of Mae Fah Luang University, Chiang Rai, Thailand (MFLU).
Pure cultures were obtained from single-spore isolation based on a spore suspension technique [82]. Germinated ascospores were aseptically transferred to potato dextrose agar (PDA) and cultivated under normal light at 20–25 °C. Fungal colonies were observed and recorded after one week and four weeks. The asexual morph that sporulated in vitro was observed and examined after two months. Axenic living cultures were deposited in the Mae Fah Luang University Culture Collection (MFLUCC) and the Culture Collection of Kunming Institute of Botany (KUMCC). The newly described taxa were registered in Index Fungorum (http://www.indexfungorum.org/names/IndexFungorumRegister.htm; accessed on 13 May 2022).

2.2. DNA Extraction, Amplification, and Sequencing

Fresh mycelia were scraped from fungal colonies growing on PDA for a month and stored in a 1.5 mL sterilized microcentrifuge tube in an aseptic condition. Fungal genomic DNA was extracted by using Biospin Fungus Genomic DNA Extraction Kit (BioFlux®, Hangzhou, China) following the manufacturer’s instructions (Hangzhou, China). Fungal genomic DNA was also extracted from fruiting bodies directly in case the fungi could not germinate on PDA using a Forensic DNA Kit (Omega®, Norcross, GA, USA). The generated fungal genomic DNA was stored at 4 °C for PCR amplification and duplicated at −20 °C for long-term storage.
Fungal genomic DNA was amplified by polymerase chain reaction (PCR) using informative phylogenetic markers of each family, including the internal transcribed spacers (ITS1-5.8S-ITS2), the 28S large subunit rDNA (LSU), the 18S small subunit rDNA (SSU), the partial RNA polymerase second largest subunit (rpb2), the translation elongation factor 1-alpha (tef1-α) and β-tubulin (tub2). The forward and reverse primer pairs ITS5 and ITS4 [83], LR0R and LR5 [84], NS1 and NS4 [83], fRPB2-5F and fRPB2-7cR [85], EF1-983F and EF1-2218R [86], and T1 and BT2B [87,88] were used to amplify the PCR fragments of these genes, respectively. Components of the PCR reaction mixture and the PCR thermal cycle program for ITS, LSU, SSU, rpb2, and tef1-α genes followed the condition described in Jiang et al. [50]. The PCR thermal cycle program for tub2 was set up initially at 94 °C for 3 min, followed by 35 cycles of denaturation at 94 °C for 30 s, annealing at 52 °C for 40 s, elongation at 72 °C for 1 min, a final extension at 72 °C for 10 min, before being held at 4 °C. PCR products were sent to TsingKe Biological Technology (Beijing) Co., Ltd., Beijing, China for purification and sequencing. The quality of the Sanger DNA sequences and sequence consensus from forward and reverse directions were checked and compiled manually in BioEdit v. 7.2.3 [89].

2.3. Sequence Alignment and Phylogenetic Analyses

The generated ITS sequences of the new isolates were used to search the related fungal group via the nucleotide BLAST search tool in the NCBI website (https://blast.ncbi.nlm.nih.gov/Blast.cgi; accessed on 5 December 2021). The nucleotide BLAST searches of the ITS sequence showed that the newly generated sequences had the closest similarity with species in families Anastomitrabeculiaceae, Parabambusicolaceae, Pyrenochaetopsidaceae and Tetraploasphaeriaceae. Thus, sequences generated from this study were analyzed with representative taxa in Anastomitrabeculiaceae, Parabambusicolaceae, Pyrenochaetopsidaceae and Tetraploasphaeriaceae, which were retrieved from GenBank based on recent publications (Table 1). Individual gene alignments were performed and improved manually where necessary using MEGA 7 [90]. Ambiguous sites were excluded from the alignment. Improved individual gene alignments were prior analyzed by maximum likelihood (ML) analysis using RaxmlGUI version 7.3.0 [91]. After checking the tree topologies of every individual gene alignment for congruence, the combined gene dataset of each family was analyzed based on Bayesian inference (BI), maximum likelihood (ML) and maximum parsimony (MP) analyses.
The evolutionary model of nucleotide substitution analysis was selected independently for each locus using MrModeltest 2.3 [92]. The best-fit model under the Akaike Information Criterion (AIC) of each locus was shown in Table 2. Bayesian inference (BI) was analyzed using MrBayes on XSEDE v. 3.2.7a via the CIPRES Science Gateway v. 3.3 [93]. Posterior probabilities (PP) [94,95] were determined by Markov Chain Monte Carlo sampling (MCMC). Two parallel runs with six simultaneous Markov chains were run for 1–2 million generations and stopped automatically when the average standard deviation of split frequencies reached below 0.01. Trees were sampled every 100th generation. The MCMC heated chain was set with a “temperature” value of 0.15. All sampled topologies beneath the asymptote (25%) were discarded as part of the burn-in procedure, and the remaining trees were used for calculating posterior probabilities in the majority rule consensus tree. Maximum likelihood (ML) was analyzed in RaxmlGUI version 7.3.0 [91] using the default algorithm of the program from a random starting tree for each run that was adjusted by setting up the GTR + GAMMAI model of nucleotide substitution with 1000 rapid bootstrap replicates. Maximum parsimony was analyzed by PAUP v. 4.0b10 [96] using the heuristic search function with 1000 random stepwise addition replicates and tree bisection-reconnection (TBR) as the branch-swapping algorithm. Maxtrees were set up to 1000, and a zero of maximum branch length was collapsed. All characters were unordered and of equal weight, and gaps were treated as missing data. Significant parsimonious trees were determined by Kishino–Hasegawa tests (KHT) [97]. All equally parsimonious trees were saved. Clade stability was estimated by bootstrap (BS) support values with 1000 replicates, each with 10 replicates of random stepwise addition of taxa [98]. Descriptive tree statistics viz. tree length (TL), consistency index (CI), retention index (RI), relative consistency index (RC) and homoplasy index (HI) were calculated.
Phylograms were visualized on FigTree v. 1.4.0 [99], and layouts of trees were drawn in Microsoft Office PowerPoint 2016 (Microsoft Inc., Redmond, WA, USA). The newly generated sequences in this study are deposited in GenBank (Table 1). The final alignment and tree were submitted in TreeBASE (https://www.treebase.org; accessed on 25 March 2022) under submission ID: 29589 (A1: Anastomitrabeculiaceae), 29590 (A2: Parabambusicolaceae), 29592 (A3: Pyrenochaetopsidaceae), and 29593 (A4: Tetraploasphaeriaceae).

3. Results

3.1. Phylogeny

Four phylogenetic analyses were conducted to resolve phylogenetic relationships of taxa in Anastomitrabeculiaceae (Analysis 1), Parabambusicolaceae (Analysis 2), Pyrenochaetopsidaceae (Analysis 3), and Tetraploasphaeriaceae (Analysis 4) as follows:
Analysis 1: Taxa in Anastomitrabeculiaceae were analyzed with related taxa in families Halojulellaceae and Neohendersoniaceae based on a combined LSU, SSU, ITS, and tef1-α DNA sequence dataset. The Data matrix comprised 20 taxa, of which two species in Massarinaceae (Helminthosporium aquaticum MFLUCC 15-0357, and Massarina eburnea CBS 473.643) were selected as the outgroup taxa. The dataset consists of 3471 total characters, including gaps (LSU: 1–870 bp, SSU: 871–1900 bp, ITS: 1901–2499 bp, tef1-α: 2500–3471 bp). The best scoring RAxML tree is presented in Figure 1 with a final ML optimization likelihood value of −10679.529226 (ln). RAxML analysis yielded 750 distinct alignment patterns, and the proportion of gaps and completely undetermined characters in this alignment was 21.29%. The proportion of invariable sites I = 0.402038 and the gamma distribution shape parameter alpha = 0.46716. The Tree-Length = 0.871849 with estimated base frequencies were as follows: A = 0.242670, C = 0.243741, G = 0.268897, T = 0.244693, and substitution rates AC = 1.181725, AG = 2.821009, AT = 1.536446, CG = 0.754762, CT = 7.660341, GT = 1.000000. The maximum parsimonious dataset consisted of 3471 characters, with 2722 characters being constant (proportion = 0.784212), 212 variable characters being parsimony-uninformative and 537 characters being parsimony-informative. The parsimonious analysis yielded six parsimonious trees, of which the first parsimonious tree was selected as the best tree for the Kishino–Hasegawa test (TL = 1178, CI = 0.778, RI = 0.845, RC = 0.657, HI = 0.222). Bayesian analysis yielded 10,001 trees from one million runs, of which 7501 were sampled. Bayesian posterior probabilities (BYPP) from MCMC were evaluated with the final average standard deviation of split frequencies = 0.004119.
The phylogenetic results based on maximum likelihood (ML), maximum parsimony (MP) and Bayesian inference analyses (Figure 1) showed overall similar tree topologies. Two new strains of Anastomitrabeculia didymospora (MFLUCC 11-0197, MFLUCC 11-0200) shared the same branch length with 72% ML support and grouped with the type strains of A. didymospora (MFLUCC 16-0412, MFLUCC 16-0416) with high support (100% ML, 100% MP, 1.00 PP) in Anastomitrabeculiaceae.
Analysis 2: Novel generated taxa in Parabambusicolaceae were analyzed with other representative genera in Parabambusicolaceae and other related families, including Bambusicolaceae, Dictyosporiaceae, Didymosphaeriaceae, Lentitheciaceae, Macrodiplodiopsidaceae, Sulcatisporaceae, and Trematosphaeriaceae based on a combined ITS, LSU, SSU, and tef1-α sequence dataset. The data matrix comprised 65 taxa with Melanomma pulvis-pyrius CBS 124080 (Melanommataceae) being the outgroup taxon. The dataset consists of 3828 total characters, including gaps (ITS: 1–601 bp, LSU: 602–1487 bp, SSU: 1488–2891 bp, tef1-α: 2892–3828 bp). The best scoring RAxML tree is presented in Figure 2 with a final ML optimization likelihood value of −25582.174441 (ln). RAxML analysis yielded 1375 distinct alignment patterns, and the proportion of gaps and completely undetermined characters in this alignment was 27.28%. The gamma distribution shape parameter alpha = 0.193883 and the Tree-Length = 2.813374. Estimated base frequencies were as follows: A = 0.236013, C = 0.254062, G = 0.272236, T = 0.237689, with substitution rates AC = 1.230009, AG = 2.581111, AT = 1.427698, CG = 1.028329, CT = 5.964523, GT = 1.000000. Bayesian analysis yielded 20,001 trees from two million runs, of which 15001 were sampled. Bayesian posterior probabilities (BYPP) from MCMC were evaluated with the final average standard deviation of split frequencies = 0.005045.
The phylogenetic results based on maximum likelihood (ML) and Bayesian inference analyses (Figure 2) showed overall similar tree topologies. A novel genus, Paramultiseptospora formed a stable subclade, clustered with the genera Multiseptospora, Neomultiseptospora, and Scolecohyalosporium with low support. These four genera formed a well-resolved clade (100% ML, 1.00 PP) within Parabambusicolaceae.
Analysis 3: A new species, Pyrenochaetopsis yunnanensis, was analyzed with taxa in Pyrenochaetopsidaceae based on a combined LSU, ITS, rpb2 and tub2 DNA sequence dataset. The data matrix comprised 25 taxa, with Neopyrenochaetopsis hominis CBS 143033 being the outgroup taxon. The dataset consists of 2819 total characters, including gaps (LSU: 1–908 bp, ITS: 909–1468 bp, rpb2: 1469–2437 bp, tub2: 2438–2819 bp). The best scoring RAxML tree is presented in Figure 3 with a final ML optimization likelihood value of -12390.524384 (ln). RAxML analysis yielded 814 distinct alignment patterns, and the proportion of gaps and completely undetermined characters in this alignment was 7.92%. The proportion of invariable sites I = 0.518277 and the gamma distribution shape parameter alpha = 0.456186. The Tree-Length = 2.561446 with estimated base frequencies were as follows: A = 0.244976, C = 0.246101, G = 0.270141, T = 0.238781, and substitution rates AC = 2.182690, AG = 6.088919, AT = 2.687456, CG = 1.526108, CT = 12.069267, GT = 1.000000. The maximum parsimonious dataset consisted of 2819 characters, with 2067 characters being constant (proportion = 0.733239), 267 variable characters being parsimony-uninformative and 485 characters being parsimony-informative. The parsimonious analysis yielded eight parsimonious trees, of which the first parsimonious tree was selected as the best tree for the Kishino–Hasegawa test (TL = 1836, CI = 0.583, RI = 0.594, RC = 0.346, HI = 0.417). Bayesian analysis yielded 10,001 trees from one million runs, of which 7501 were sampled. Bayesian posterior probabilities (BYPP) from MCMC were evaluated with the final average standard deviation of split frequencies = 0.006366.
Phylograms generated from maximum likelihood (ML), maximum parsimony (MP) and Bayesian inference analyses (Figure 3) were overall similar tree topologies. A new species, Pyrenochaetopsis yunnanensis (KUMCC 21-0843), has a close relationship with P. terricola (HGUP 1802) with high support (100% ML, 100% MP, 1.00 PP) and formed a well-resolved clade basal on P. confluens (CBS 142459), P. decipiens (CBS 343.85) and P. indica (CBS 124454) within Pyrenochaetopsidaceae.
Analysis 4: A new species, Tetraploa bambusae, was analyzed with other representative taxa in Tetraploasphaeriaceae based on a combined LSU, ITS, SSU, tub2 and tef1-α DNA sequence dataset. The data matrix comprised 71 taxa, with Muritestudina chiangraiensis (MFLUCC 17-2551) being the outgroup taxon. The dataset consists of 3397 total characters, including gaps (LSU: 1–853 bp, ITS: 854–1427 bp, SSU: 1428–2421 bp, tub2: 2422–3078 bp, tef1-α: 3079–3397 bp). The best scoring RAxML tree is presented in Figure 4 with a final ML optimization likelihood value of −18736.220881 (ln). RAxML analysis yielded 1138 distinct alignment patterns, and the proportion of gaps and completely undetermined characters in this alignment was 27.96%. The proportion of invariable sites I = 0.573772 and the gamma distribution shape parameter alpha = 0.671292. The Tree-Length = 3.408354, and the estimated base frequencies were as follows: A = 0.239956, C = 0.252519, G = 0.274658, T = 0.232866, and substitution rates AC = 2.302918, AG = 3.658670, AT = 1.691247, CG = 1.425389, CT = 8.553285, GT = 1.000000. The maximum parsimonious dataset consisted of 3397 characters, with 2452 characters being constant (proportion = 0.721813), 177 variable characters being parsimony-uninformative and 768 characters being parsimony-informative. The parsimonious analysis yielded 1000 parsimonious trees, of which the first parsimonious tree was selected as the best tree for the Kishino–Hasegawa test (TL = 2787, CI = 0.532, RI = 0.832, RC = 0.443, HI = 0.468). Bayesian analysis yielded 10,001 trees from one million runs, of which 7501 were sampled. Bayesian posterior probabilities (BYPP) from MCMC were evaluated with the final average standard deviation of split frequencies = 0.007021.
Phylograms generated from maximum likelihood (ML), maximum parsimony (MP) and Bayesian inference analyses (Figure 4) were overall similar tree topologies. A new species, Tetraploa bambusae (KUMCC 21-0844) formed a low support subclade (63% ML, 37% MP, 0.83 PP) with Tetraploa sp. (KT 1684) and clustered with T. endophytica (CBS 147114) and T. obpyriformis (KUMCC 21-0011) with high support (99% ML, 98% MP, 1.00 PP).

3.2. Taxonomy

Anastomitrabeculiaceae Bhunjun, Phukhams. and K.D. Hyde
Bhunjun et al. [71] introduced the novel family Anastomitrabeculiaceae to accommodate a monotypic genus Anastomitrabeculia based on morphological characteristics and phylogenetic analyses of a combined LSU, SSU and tef1-a dataset coupled with divergence time estimates using molecular clock methodologies. The novel taxa were isolated from bamboo culms submerged in freshwater in southern Thailand. The genus is characterized by gregarious, uni-loculate, globose to subglobose, coriaceous ascomata, immersed under a clypeus to semi-immersed, with short, carbonaceous ostiolar neck, bitunicate, fissitunicate, cylindric-clavate asci, embedded in a hyaline, trabeculate pseudoparaphyses, and hyaline, fusiform, septate ascospores with longitudinally striate wall ornamentation, surrounded by a distinct, mucilaginous sheath [71]. According to Bhunjun et al. [71], Anastomitrabeculiaceae has a close phylogenetic relationship with Halojulellaceae. However, Halojulellaceae can be distinguished from Anastomitrabeculiaceae in having cellular pseudoparaphyses and pigmented ascospores. In this study, we collected Anastomitrabeculia didymospora from bamboo branches in terrestrial habitats in northern Thailand reported for the first time.
Anastomitrabeculia didymospora Bhunjun, Phukhams. and K.D. Hyde, in Bhunjun, Phukhamsakda, Jeewon, Promputtha and Hyde, Journal of Fungi 7(2, no. 94): 12 (2021)
Index Fungorum number: IF 556559, Figure 5
Holotype information: Thailand, Krabi Province (8.1° N, 98.9° E), on dead bamboo culms submerged in freshwater, 15 December 2015, C. Phukhamsakda, KR001 (MFLU 20-0694), ex-type living culture = MFLUCC 16-0412.
Saprobic on dead branches of bamboo, visible as raised, black spots, with spike-like on the host surface. Sexual morph: Ascomata 200–320 μm high, 580–730 μm diam (excluding neck), gregarious, scattered to clustered, immersed under the clypeus to erumpent through host tissue by an ostiolar neck, ampulliform to subconical or hemispherical, uni-loculate, dark brown to black. Ostiolar neck 70–170 μm high, 130–200 μm diam, black, short, central, carbonaceous, papillate, protruding through host tissue. Peridium 30–100 μm wide at the sides, 6–15 μm wide at the base, unequally thick, poorly developed at the base, composed of fungal tissues intermixed with host tissues, of dark brown to black pseudoparenchymatous cells, arranged in a textura angularis. Hamathecium 1–2 μm wide, composed of dense, septate, branched, anastomosed, trabeculate pseudoparaphyses, embedded in a gelatinous matrix. Asci (100–)120–140(–170) × 16–20(–24) μm ( x ¯ = 131.6 × 19.2 μm, n = 20), eight-spored, bitunicate, fissitunicate, cylindric-clavate, with a short pedicel, apically rounded with an ocular chamber. Ascospores (22–)25–30 × (6–)8–10 μm ( x ¯ = 27.1 × 8.2 μm, n = 20), overlapping 1–2-seriate, hyaline, fusiform, straight to curved, 1(–3)-septate, wider in the upper part, rough-walled, with longitudinal furrows on the surface, surrounded by a distinct mucilaginous sheath. Asexual morph: Undetermined.
Culture characteristics: Ascospores germinated on PDA within 12 h. Colonies on PDA reaching 29–33 mm diam after 2 weeks at room temperature (30–35 °C). Colonies medium dense, irregular in shape, flat to slightly raised, surface smooth with an undulate edge, floccose to fluffy; colonies from above white at the margin, pale gray at the middle, with white hyphal turfs at the center; from below white to cream at the margin, yellowish-brown at the middle, dark greenish-gray to black at the center, slightly radiating inwards colony; not producing pigmentation on PDA.
Material examined: Thailand, Chiang Rai Province, Phan District, Mae Yen Subdistrict, Pu Khang Waterfall, on dead branches of bamboo, 13 January 2011, N.N. Wijayawardene, RP0113 (MFLU 11-0233), living culture: MFLUCC 11-0197; Chiang Mai Province, Mae Rim District, Mae Sa Waterfall, on dead branches of bamboo, 12 March 2011, R. Phookamsak, RP0116 (MFLU11-0236), living culture: MFLUCC 11-0200.
Known distribution: Krabi Province, southern Thailand [71], Chiang Mai and Chiang Rai Provinces, northern Thailand (this study).
Known host and habitats: saprobic on bamboo in freshwater [71] and terrestrial environments (this study).
Notes: The nucleotide BLAST search of ITS, LSU and tef1-α sequences resulted in the two newly generated strains (MFLUCC 11-0197 and MFLUCC 11-0200) being similar to Anastomitrabeculia didymospora MFLU 20-0694 (100% similarity). A nucleotide pairwise comparison of ITS, LSU and tef1-α sequences also indicated that strains MFLUCC 11-0197 and MFLUCC 11-0200 are consistent (less than 1.5% different base pair) with A. didymospora MFLU 20-0694 (type strain). We, therefore, identified our strains as A. didymospora. Morphologically, the new collection (MFLU 11-0233) is slightly larger in ascomata, asci, and ascospores than those of the type of A. didymospora [71]. The differences in the size range may be affected by environmental factors. Bhunjun et al. [71] mentioned that A. didymospora (MFLU 20-0694) has one-septate ascospores; however, we found that the species has 1(–3)-septate ascospores in this study. The host preference of A. didymospora is currently restricted to bamboo. However, the species is reported from terrestrial habitats for the first time.
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Figure 5. Anastomitrabeculia didymospora (MFLU 11-0233). (a) The appearance of ascomata on the host surface; (b) Vertical section of ascoma with ostiolar neck; (c,d) Peridium; (e) Pseudoparaphyses stained in cotton blue; (f–h) Asci; (i–l) Ascospores; (m) Germinating ascospore; (n,o) Culture characteristics on PDA after two weeks ((n) = from above, (o) = from below). Scale bars: (b) = 100 μm, (c–h) = 20 μm, (i–m) = 10 μm.
Figure 5. Anastomitrabeculia didymospora (MFLU 11-0233). (a) The appearance of ascomata on the host surface; (b) Vertical section of ascoma with ostiolar neck; (c,d) Peridium; (e) Pseudoparaphyses stained in cotton blue; (f–h) Asci; (i–l) Ascospores; (m) Germinating ascospore; (n,o) Culture characteristics on PDA after two weeks ((n) = from above, (o) = from below). Scale bars: (b) = 100 μm, (c–h) = 20 μm, (i–m) = 10 μm.
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Parabambusicolaceae Kaz. Tanaka and K. Hiray.
Parabambusicolaceae was introduced by Tanaka et al. [27] to accommodate the genera Aquastroma, Multiseptospora, Parabambusicola, and the other two “Monodictys sp.”. Later, a monotypic genus Multilocularia was included in this family by Li et al. [100], while Wanasinghe et al. [101] and Phukhamsakda et al. [102] addressed both sexual and coelomycetous asexual species of Neoaquastroma in this family. Phukhamsakda et al. [102] also included Pseudomonodictys in Parabambusicolaceae. Subsequently, many genera were introduced in this family, including Lonicericola, Neomultiseptospora, Paramonodictys, Paratrimmatostroma, and Scolecohyalosporium [63,103,104]. Presently, 11 genera are accepted in this family based solely on the morpho-molecular approach. We follow the latest treatment of Xie et al. [104] and introduce the new genus Paramultiseptospora to accommodate a single species P. bambusae sp. nov. in this study.
Paramultiseptospora Phookamsak, H.B. Jiang and Chomnunti, gen. nov.
Index Fungorum number: IF 554966
Etymology: Referring to relations with phylogenetically close genus Multiseptospora. Saprobic on dead stems of bamboo. Sexual morph: Ascomata gregarious, scattered to clustered, immersed in dark brown longitudinal clypeus, visible as raised, becoming superficial, lying along the host surface, uni-loculate, hemispherical to flattened ellipsoidal, or quadrilateral, glabrous, with apapillate ostiole. Peridium thin- to thick-walled, slightly thick at the sides, thinner at the apex, poorly developed at the base, composed of several layers of brown to dark brown, pseudoparenchymatous cells, paler brown to hyaline toward the inner layers, arranged in a textura angularis, outer layers intermixed with host tissues. Hamathecium composed of dense, branched, septate cellular pseudoparaphyses, anastomosed above the asci, embedded in a hyaline gelatinous matrix. Asci eight-spored, bitunicate, fissitunicate, cylindric-clavate to clavate, shortly pedicellate, apically rounded, with a well-developed ocular chamber. Ascospores overlapping one to three-seriate, hyaline, fusiform to oblong, with rounded ends, septate, constricted at the septa, smooth-walled, surrounded by a thick, mucilaginous sheath, with small guttules. Asexual morph: Undetermined.
Type species: Paramultiseptospora bambusae Phookamsak and H.B. Jiang, sp. nov.
Notes: A monotypic genus Paramultiseptospora is introduced herein due to the differences in morphological characteristics with the other related genera (viz. Multiseptospora, Neomultiseptospora and Scolecohyalosporium), although the phylogenetic affinity of the genus does not support in this study. Paramultiseptospora formed a stable clade, closely related to Multiseptospora and Scolecohyalosporium in both BI and ML analyses and clustered with Neomultiseptospora. These four genera formed a well-resolved clade (100% ML, 1.00 PP; Figure 2) within Parabambusicolaceae. Paramultiseptospora can be easily distinguished from Multiseptospora and Scolecohyalosporium in having hemispherical to flattened ellipsoidal, glabrous, ascomata, immersed in longitudinal clypeus, visible as raised, lying along the host surface, cylindric-clavate to clavate asci with short pedicel and fusiform to oblong ascospores, with rounded ends. Meanwhile, Multiseptospora has globose to subglobose ascomata, immersed in the host, covered by dark, hair-like hyphae, broadly cylindrical, subsessile asci, and fusiform to vermiform ascospore, with acute ends [33]. Scolecohyalosporium is different in having conical to ovoid, black, rough-walled ascomata, erumpent to superficial on the host, long cylindrical asci, with short pedicel and filiform ascospores [104]. Paramultiseptospora morphologically resembles Neomultiseptospora in having hemispherical to subconical, glabrous ascomata, immersed in the host, with apapillate ostiole, clavate asci, with short pedicel and fusiform or oblong, septate ascospores, surrounded by a thick mucilaginous sheath. However, these two genera are slightly different in the characteristics of ascomata on the host. Paramultiseptospora formed gregarious, scattered to clustered ascomata, immersed in dark brown longitudinal clypeus, lying along the host surface whereas Neomultiseptospora formed solitary, scattered, immersed, visible as raised, black dome-shaped on the host surface [104]. Phylogenetically, Paramultiseptospora always formed a separate branch from Neomultiseptospora. Therefore, we consider Paramultiseptospora as a distinct genus with Neomultiseptospora based on morphology coupled with the phylogenetic relationship.
Paramultiseptospora bambusae Phookamsak and H.B. Jiang, sp. nov.
Index Fungorum number: IF 554968, Figure 6
Etymology: Referring to the host, bamboo, of on which the species was collected.
Holotype: KUN-HKAS 122241
Saprobic on a dead stem of bamboo. Sexual morph: Ascomata 115–150 μm high, 340–470 μm diam, gregarious, scattered to clustered, immersed in dark brown longitudinal clypeus, visible as raised, becoming superficial, lying along the host surface, uni-loculate, hemispherical to flattened ellipsoidal, or quadrilateral, glabrous, indistinct apapillate ostiole. Peridium 30–90 μm wide at the sides toward the apex, 10–25 μm wide at the base, thin- to thick-walled, slightly thick at the sides, thinner at the apex, poorly developed at the base, composed of several layers of brown to dark brown, pseudoparenchymatous cells, paler brown to hyaline toward the inner layers, arranged in a textura angularis, outer layers intermixed with host tissues. Hamathecium composed of dense, 1–2.5 μm wide, branched, septate cellular pseudoparaphyses, anastomosed above the asci, embedded in a hyaline gelatinous matrix. Asci (70–)75–90(–95) × 16–20(–22) μm ( x ¯ = 83.3 × 19.6 μm, n = 30), eight-spored, bitunicate, fissitunicate, cylindric-clavate to clavate, shortly pedicellate, apically rounded, with a well-developed ocular chamber. Ascospores (23–)25–28(–29) × 5–8 μm ( x ¯ = 25.8 × 6.6 μm, n = 30), overlapping one to three-seriate, hyaline, fusiform to oblong, with rounded ends, narrower toward the end cells, enlarged at the third cell from above, slightly curved, six-septate, constricted at the septa, smooth-walled, surrounded by a thick, mucilaginous sheath, with small guttules. Asexual morph: Undetermined
Material examined: China, Yunnan Province, Honghe Autonomous Prefecture, Honghe County, Honghe Hani Rice Terraces (23°5′35″ N, 102°46′47″ E, 1432 + 6 msl), on dead stem of bamboo, 26 January 2021, R. Phookamsak, BN09F (KUN-HKAS 122241, holotype), ex-type strain: KUN-HKAS 122241A. Notes: DNA was extracted from fruit bodies.
Known distribution: Yunnan Province, China.
Known host and habitats: saprobic on a stem of bamboo in a terrestrial environment.
Notes: The nucleotide BLAST search of ITS sequence indicated that Paramultiseptospora bambusae (KUN-HKAS 122241A) has the closest similarity with Multiseptospora thailandica strain MFLUCC 11-0183 (ex-type strain) with 95.58% similarity (Identities = 432/452, with no gap), strains MFLUCC 11-0204 and MFLUCC 12-0006 with 95.48% similarity (Identities = 444/465, with no gap) and is similar to “Pleosporales sp. strain 1192” (95.54% similarity, Identities = 407/426, with no gap). Paramultiseptospora bambusae (KUN-HKAS 122241A) also matches with Neomultiseptospora yunnanensis strain KUMCC 21-0411 (ex-type strain) with 92.84% similarity (Identities = 428/461, with no gap) and Scolecohyalosporium submersum strain KUMCC 21-0412 (ex-type strain) with 92.57% similarity (Identities = 436/471, with two gaps). The nucleotide BLAST search of LSU sequence indicated that P. bambusae (KUN-HKAS 122241A) is similar to S. submersum strains KUMCC 21-0412, KUMCC 21-0413 and KUN-HKAS 122242 with 98.57% similarity (Identities = 830/842, with two gaps), similar to M. thailandica strain MFLUCC 12-0006 (98.56% similarity, Identities = 830/843, with four gaps) and strain MFLUCC 11-0204 (98.46% similarity, Identities = 821/833, with three gaps), and is similar to N. yunnanensis strain KUMCC 21-0411 (97.59% similarity, Identities = 811/831, with one gap) and strain KUN-HKAS 122240 (97.23% similarity, Identities = 808/831, with one gap).
Based on a nucleotide pairwise comparison, Paramultiseptospora bambusae (KUN-HKAS 122241A) differs from Multiseptospora thailandica (MFLUCC 11-0183, ex-type strain) in 88/570 bp of ITS (15.44%), 13/765 bp of LSU (1.7%), and 28/645 bp of tef1-α (4.34%). Paramultiseptospora bambusae (KUN-HKAS 122241A) differs from Scolecohyalosporium submersum (KUMCC 21-0412) in 85/595 bp of ITS (14.28%), 12/842 bp of LSU (1.42%), and 39/921 bp of tef1-α (4.23%). The species is also different from Neomultiseptospora yunnanensis strain KUMCC 21-0411 (ex-type strain) in 102/606 bp of ITS (16.83%), 21/832 bp of LSU (2.52%), and 52/979 bp of tef1-α (5.31%). Paramultiseptospora bambusae is morphologically similar to N. yunnanensis but differs in having fusiform to oblong, six-septate ascospores with rounded ends, narrower toward the end cells, and constricted at the septa, whereas N. yunnanensis has fusiform to ellipsoidal, or oblong, (four to) five-septate ascospores, with rounded ends, slightly constricted at the central septum, which are less constricted at the other septa [104].
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Figure 6. Paramultiseptospora bambusae (KUN-HKAS 122241, holotype). (a) The appearance of ascomata on host substrate; (b) Vertical section of ascoma; (c) Peridium; (d) Asci embedded in cellular pseudoparaphyses; (e) Ascus; (f) Ascospores stained with Indian ink showing a thick mucilaginous sheath surrounded ascospores; (g–j) Ascospores. Scale bars: (b) = 100 μm, (c) = 50 μm, (d–f) = 20 μm, (g–j) = 10 μm.
Figure 6. Paramultiseptospora bambusae (KUN-HKAS 122241, holotype). (a) The appearance of ascomata on host substrate; (b) Vertical section of ascoma; (c) Peridium; (d) Asci embedded in cellular pseudoparaphyses; (e) Ascus; (f) Ascospores stained with Indian ink showing a thick mucilaginous sheath surrounded ascospores; (g–j) Ascospores. Scale bars: (b) = 100 μm, (c) = 50 μm, (d–f) = 20 μm, (g–j) = 10 μm.
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Pyrenochaetopsidaceae Valenzuela-Lopez et al.
Pyrenochaetopsidaceae was introduced by Valenzuela Lopez et al. [105] to accommodate the asexual genera Pyrenochaetopsis (type genus), Neopyrenochaetopsis and Xenopyrenochaetopsis. The family is characterized by pycnidial, pale brown to brown, solitary or confluent, glabrous or setose, subglobose to ovoid conidiomata, with apapillate or papillate ostiole, acropleurogenous conidiophores, phialidic, hyaline, discrete or integrated, septate conidiogenous cells, and aseptate, hyaline, smooth- and thin-walled, ovoid, cylindrical to allantoid ascospores [105]. Mapook et al. [106] introduced a novel species, Pyrenochaetopsis chromolaenae collected on Chromolaena odorata in Thailand and reported the sexual morph of Pyrenochaetopsis for the first time. The sexual morph is characterized by brown to dark brown solitary or scattered, globose ascomata, superficial on the host, with short papillate ostiole, with reddish-brown setae covering the papilla, thin-walled peridium, fissitunicate, cylindric-clavate asci, with a short, bulbous pedicel, and hyaline to pale brown or yellowish-brown, cylindrical to broadly fusiform, three to four-septate ascospores [106]. Species in Pyrenochaetopsidaceae have been isolated from various substrates as saprobes and also opportunistic pathogens on humans as well as on cysts of plant-parasitic nematodes. [81,105,106].
Pyrenochaetopsis was treated as the generic type of Pyrenochaetopsidaceae and is typified by P. leptospora. The genus was introduced by de Gruyter et al. [107] to accommodate phoma-like taxa. Recently, 19 species are accepted in this genus [108]. In this study, we introduce a holomorph species, P. yunnanensis, which occurred on bamboo in Yunnan, China.
Pyrenochaetopsis yunnanensis C.F. Liao, H.B. Jiang and Phookamsak, sp. nov.
Index Fungorum number: IF 554979, Figure 7
Etymology: Referring to the locality, Yunnan Province of China, of which the species was collected.
Holotype: KUN-HKAS 123172
Saprobic on dead stem of bamboo. Sexual morph: Ascomata 190–280 μm high, 270–460 μm diam, gregarious, scattered to clustered, immersed to semi-immersed under the clypeus, visible as raised, black, shiny, rough on host surface, uni- to tri-loculate, subglobose to subconical, or quadrilateral, glabrous, ostiole central with minute papillate, protruding through host tissue. Peridium 30–80 μm wide at sides toward the apex, 10–30 μm wide at the base, unequally thickness, poorly developed at the base, composed of several layers of dark brown pseudoparenchymatous cells, arranged in textura angularis to textura prismatica, outer layers intermixed with host cortex. Hamathecium composed of dense, 1.5–2.5 μm wide, filamentous, branched, septate, cellular pseudoparaphyses, anastomosed above the asci, embedded in a hyaline gelatinous matrix. Asci (58–)70–95(–110) × 11–14(–15.5) μm ( x ¯ = 80.2 × 12.8 μm, n = 30), eight-spored, bitunicate, fissitunicate, clavate, with short pedicel, apically rounded, with a well-developed ocular chamber. Ascospores (18–)20–25(–28) × (4.5–)5–6.5(–8) μm ( x ¯ = 23.4 × 5.8 μm, n = 30), overlapping one to three-seriate, hyaline, fusiform, with acute ends, slightly curved, one to three-septate, slightly constricted at the central septum, not constricted at the other septa, smooth-walled, lacking mucilaginous sheath. Asexual morph: Coelomycetous, sporulated on PDA after two months at room temperature (15–20 °C), visible as black dots, superficial or immersed in PDA. Conidiomata 50–100 μm high, 68–105 μm diam, pycnidial, black, solitary, or in a small group, immersed to superficial, globose to subglobose, uni- to multi-loculate, setose, with dark brown, septate setae (35–75 × 2–4 μm, n = 20), ostiole central, with pore-like opening or pimple-like. Peridial wall 7.5–20 μm wide, equally thin-walled, composed of one to two layers, of brown to dark brown pseudoparenchymatous cells, arranged in textura angularis to textura prismatica, or textura globulosa. Conidiophores reduced to conidiogenous cells. Conidiogenous cells 2–4 × (1.8–)2–3.5 μm ( x ¯ = 3.5 × 2.8 μm, n = 30) phialidic, hyaline, discrete, aseptate, arising from the inner cavity of the pycnidial wall, difficult to distinguish from the pycnidial wall. Conidia (2.8–)3–4 × 1–2(–2.5) μm ( x ¯ = 3.4 × 1.9 μm, n = 50) hyaline, subglobose to oblong, aseptate, with small guttules.
Culture characteristics: Ascospores germinated on PDA within 24 h. Colonies on PDA reach 25–28 mm diam after one week at room temperature (15–20 °C). Colonies medium dense, irregular in shape, flat to slightly raised, surface smooth with a lobate edge, floccose to cottony; colony from above pale gray to white-gray at the margin, white at the middle toward the center, sectored; from below white at the margin, pale yellowish-brown at middle toward the center; not producing pigmentation on PDA. Sporulation on PDA after two months.
Material examined: China, Yunnan Province, Honghe Autonomous Prefecture, Honghe County, Honghe Hani Rice Terraces (23°5′35″ N, 102°46′47″ E, 1432 + 6 msl), on dead stem of bamboo in a terrestrial environment, 26 January 2021, R. Phookamsak, BN09F (KUN-HKAS 123172, holotype), ex-type living culture: KUMCC 21-0843.
Known distribution: Yunnan Province, China.
Known host and habitats: saprobic on a stem of bamboo in a terrestrial environment.
Notes: The nucleotide BLAST search of ITS sequence indicated that Pyrenochaetopsis yunnanensis (KUMCC 21-0843) is similar to Leptosphaeria sp. (isolate NTOU5272 and R10) with 100% similarity (Identities = 521/521 and 490/490, with no gap), it is similar to Pyrenochaetopsis terricola strain HGUP1802 (ex-type strain) with 99.41% similarity (Identities = 506/509, with two gaps), and it is also identical to Dokmaia sp. isolate C126 (99.79% similarity, Identities = 485/486, with one gap). The nucleotide BLAST search of rpb2 sequence indicated that P. yunnanensis (KUMCC 21-0843) is similar to P. terricola strain HGUP1802 with 94.71% similarity (Identities = 948/1001, with no gap), and the nucleotide BLAST search of tub2 sequence also showed that P. yunnanensis (KUMCC 21-0843) is identical to P. terricola strain HGUP1802 with 98.61% similarity (Identities = 354/359, with three gaps) and is identical to P. sinensis strain LC12199 with 92.98% similarity (Identities = 265/285, with six gaps).
Based on a nucleotide pairwise comparison, Pyrenochaetopsis yunnanensis (KUMCC 21-0843) is consistent with P. terricola strain HGUP1802 in LSU nucleotide pairwise comparison but differs from P. terricola in 11/519 bp of ITS (2.12%), 53/1002 bp of rpb2 (5.29%), and 7/363 bp of tub2 (1.93%). Pyrenochaetopsis yunnanensis (KUMCC 21-0843) grouped with P. terricola strain HGUP1802 with high support (100% ML, 100% MP, 1.00 PP; Figure 3) in the present study. Pyrenochaetopsis yunnanensis (KUMCC 21-0843) morphological resembles P. terricola but the conidial size is slightly longer than P. terricola (2–3 × 1–2 μm) [109]. Wang et al. [109] isolated P. terricola from the soil in Guizhou Province, China and determined only the asexual morph sporulated on OA, while our novel species was found as a saprobe on bamboo and both sexual and asexual morph.
Tetraplosphaeriaceae Kaz. Tanaka and K. Hiray.
Tetraplosphaeriaceae was introduced by Tanaka et al. [12] to accommodate genera that mostly occurred on bamboo. Five genera that formed tetraploa-like asexual morph were initially introduced to this family, including Polyplosphaeria, Pseudotetraploa, Quadricrura, Tetraplosphaeria (generic type), and Triplosphaeria [12]. Later, Tetraplosphaeria was treated as a synonym of Tetraploa [72,110]. Recently, nine genera were accepted in this family viz. Aquatisphaeria, Byssolophis, Ernakulamia, Polyplosphaeria, Pseudotetraploa, Quadricrura, Shrungabeeja, Tetraploa (= Tetraplosphaeria), and Triplosphaeria [41,81,111,112,113,114]. Most species in Tetraplosphaeriaceae were reported as saprobes on bamboo, but some species were isolated from soil and water [81].
Tetraploa (= Tetraplosphaeria), generic type of Tetraplosphaeriaceae, was introduced by Berkeley and Broome [115] with T. aristata as the type species. The asexual morph of Tetraploa is characterized by lacking conidiophores, monoblastic conidiogenous cells, and brown, short-cylindrical, verrucose conidia, composed of four columns with four setose appendages at the apex [12,81]. The sexual morph is characterized by scattered to gregarious, immersed to erumpent, globose to subglobose, glabrous ascomata, with short-papillate to cylindrical ostiole, fissitunicate, cylindrical to clavate, short-pedicellate asci, and hyaline, narrowly fusiform, septate, smooth-walled ascospores, surrounded by a mucilaginous appendage-like sheath [12,81]. Species in Tetraploa mostly occurred on bamboos and other herbaceous plants or rotten wood as well as isolated from soil or raindrops [81]. In this study, the novel species, T. bambusae, isolated from bamboo in Yunnan, China is introduced based on morphological characteristics and multigene phylogenetic analyses.
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Figure 7. Pyrenochaetopsis yunnanensis (KUN-HKAS 123172, holotype). (a) The appearance of ascomata on host substrate; (b) Vertical section of ascomata; (c) Peridium; (d) Pseudoparaphyses; (e) Asci; (f–h) Ascospores; (i) Ascospore stained with Indian ink; (j) Germinated ascospore; (k) Colony sporulated on PDA after two months; (l) Conidiomata immersed or superficial on PDA; (m) Squash mount of conidioma in water; (n) Section through pycnidial wall; (o) Vertical section of conidiomata; (p,q) Conidiogenous cells; (r) Conidia. Scale bars: (b) = 200 μm, (c,m) = 50 μm, (d,e,n,o) = 20 μm, (f–i,j,r) = 10 μm, (p,q) = 5 μm.
Figure 7. Pyrenochaetopsis yunnanensis (KUN-HKAS 123172, holotype). (a) The appearance of ascomata on host substrate; (b) Vertical section of ascomata; (c) Peridium; (d) Pseudoparaphyses; (e) Asci; (f–h) Ascospores; (i) Ascospore stained with Indian ink; (j) Germinated ascospore; (k) Colony sporulated on PDA after two months; (l) Conidiomata immersed or superficial on PDA; (m) Squash mount of conidioma in water; (n) Section through pycnidial wall; (o) Vertical section of conidiomata; (p,q) Conidiogenous cells; (r) Conidia. Scale bars: (b) = 200 μm, (c,m) = 50 μm, (d,e,n,o) = 20 μm, (f–i,j,r) = 10 μm, (p,q) = 5 μm.
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Tetraploa bambusae Phookamsak and H.B. Jiang, sp. nov.
Index Fungorum number: IF 554987, Figure 8
Etymology: Referring to the host, bamboo, of which the species was collected.
Holotype: KUN-HKAS 123174
Saprobic on dead twigs of bamboo. Sexual morph: Undetermined. Asexual morph: hyphomycetous. Colonies brown to brick orange, effuse to powdery, compact, with patch-like, superficial on the host substrate. Mycelia light brown to brown, branched, septate. Conidiophores up to 40–130 µm long, (1.5–)2–3.5 µm wide, macronematous, inconspicuous, light brown, branched, septate. Conidiogenous cells monoblastic, discrete or integrated, determinate, cylindrical. Conidia (21–)23–30(–33) × (17–)18–23(–26) µm ( x ¯ = 24.1 × 19.8 µm, n = 30), muriform, obovoid to turbinate, with obtuse end, brown to dark brown, composed of four columns of cells, four-septate in each column, coarsely verruculose, with four apical appendages, sometimes, a small piece of the denticle remains attached to the base of the conidium. Appendages 15–40 µm long, 2.5–4.5 µm wide at the base, wider at the base, tapering toward the apex, divergent, brown, one to three-septate, straight or slightly flexuous, smooth-walled.
Culture characteristics: Ascospores germinated on PDA within 24 h. Colonies on PDA reach 22–25 mm diam after two weeks at room temperature (15–20 °C). Colonies dense, irregular in shape, raised to umbonate, surface smooth with an undulate edge, velvety; colony from above white–gray to pale gray at the margin, gray at the middle toward the center; from below white to cream at the margin, orange–brown at the middle, brown to dark brown at the center, slightly radiated outwards colony with concentric rings; not producing pigmentation on PDA.
Material examined: China, Yunnan Province, Kunming City, Kunming Institute of Botany, on dead twigs of bamboo, 31 January 2021, R. Phookamsak, KIB21-005 (KUN-HKAS 123174, holotype), ex-type living culture: KUMCC 21-0844.
Known distribution: Yunnan Province, China.
Known host and habitats: saprobic on twigs of bamboo in a terrestrial environment.
Notes: The nucleotide BLAST search of ITS sequence indicated that Tetraploa bambusae (KUMCC 21-0844) closest matches with “uncultured fungus” clone 035A11084, 109A74706, 036A17775, and 034A2039 with 96.30%, 96.05%, 95.80%, and 95.71% similarities, respectively. The species is similar to Tetraplosphaeria sp. strain WSF14_RG24_2 with 95.62% similarity (Identities = 502/525, with eight gaps), and it is similar to Tetraploa yunnanensis MFLUCC 19-0319 (ex-type strain) with 95.60% similarity (Identities = 521/545, with nine gaps). The nucleotide BLAST search of LSU sequence indicated that T. bambusae (KUMCC 21-0844) closest matches with T. sasicola strain MFLUCC 17-1387 with 99.88% similarity (Identities = 822/823, with no gap) and is similar to Tetraploa obpyriformis KUMCC 21-0011 with 99.64% similarity (Identities = 821/824, with one gap) and Tetraploa sp. KT 1684 with 99.51% similarity (Identities = 816/820, with one gap). The nucleotide BLAST search of tub2 sequence also showed that T. bambusae (KUMCC 21-0844) closest matches with Tetraplosphaeria sasicola KT 563 with 88.51% similarity (Identities = 578/653, with 29 gaps) and is similar to Tetraploa aristata CBS 996.70 with 82.53% similarity (Identities = 529/641, with 27 gaps) and Tetraplosphaeria yakushimensis KT 1906 with 81.58% similarity (Identities = 536/657, with 38 gaps).
Phylogenetic analyses based on a combined LSU-ITS-SSU-tub2-tef1-α sequence dataset demonstrated that Tetraploa bambusae (KUMCC 21-0844) is sister to Tetraploa sp. KT 1684 and clustered with T. endophytica CBS 147114 and T. obpyriformis KUMCC 21-0011 with high support (99% ML, 98% MP, 1.00 PP; Figure 4). Based on a nucleotide pairwise comparison, T. bambusae (KUMCC 21-0844) is consistent with Tetraploa sp. KT 1684 in LSU nucleotide pairwise comparison (differs in 1 bp), but it could not be compared for the other informative gene regions (viz. ITS, tub2, and tef1-α) due to the lack of sequence data of Tetraploa sp. KT 1684. Tanaka et al. [12] included Tetraploa sp. KT 1684 in their analyses when they introduced the new family Tetraplosphaeriaceae; however, the morphological characteristics of Tetraploa sp. KT 1684 were not described. Thus, we could not compare the morphology of the novel species with Tetraploa sp. KT 1684, while T. obpyriformis KUMCC 21-0011 is an unpublished species. Tetraploa endophytica CBS 147114 was isolated from the roots of Microthlaspi perfoliatum (Brassicaceae) as an endophyte. The strain did not sporulate in any of the different culture media [116]. Therefore, the species also could not compare their morphology.
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Figure 8. Tetraploa bambusae (KUN-HKAS 123174, holotype). (a) The appearance of colony on host substrate; (b) Conidial mass; (c,d) Conidia attached with conidiophores; (e,f) Conidia; (g) Germinated conidium; (h) Culture characteristics on PDA after one week. Scale bars: (b) = 50 μm, (c–g) = 20 μm.
Figure 8. Tetraploa bambusae (KUN-HKAS 123174, holotype). (a) The appearance of colony on host substrate; (b) Conidial mass; (c,d) Conidia attached with conidiophores; (e,f) Conidia; (g) Germinated conidium; (h) Culture characteristics on PDA after one week. Scale bars: (b) = 50 μm, (c–g) = 20 μm.
Jof 08 00630 g008

4. Discussion and Conclusions

Bambusicolous fungi are highly diverse and distributed in various families within Pleosporales. Since 2015, over 85 bambusicolous species have been introduced in Pleosporales [3,27,33,39,41,45,46,49,50,52,55,59,63,68,71,74,76,77,78,79,80,100,104,117,118,119,120,121,122,123,124,125,126,127,128,129,130,131,132]. Even though novel taxa have been continuedly introduced in recent years, studies into the diversity of bambusicolous fungi correlating with specific bamboo genera are still limited due to the lack of host species identification. Jiang [133] reported that 48% of pleosporalean taxa were associated with bamboos in Thailand, and 39% were discovered in Yunnan, China. However, documented species were restricted to some parts of Thailand (mainly found in northern) and Yunnan Province (e.g., Honghe, Kunming, and Xishuangbanna) as well as some provinces of China (e.g., Guangdong and Sichuan) and Japan, whereas other regions that show a high species richness of bamboos have received less attention. Hence, we believe that a huge number of novel taxa occurring on bamboo are waiting for discovery in other regions. In this study, we collected the ascomycetes on bamboo in Honghe and Kunming (Yunnan Province, China) and also included the collections from Chiang Mai and Chiang Rai Provinces (Thailand), which were collected in 2011. Based on morphological characteristics and multigene phylogenetic analyses, four novel taxa collected from Yunnan, China are introduced, including Paramultiseptospora bambusae sp. et gen. nov., Pyrenochaetopsis yunnanensis sp. nov., and Tetraploa bambusae sp. nov., whereas collections from Thailand are identified as Anastomitrabeculia didymospora and reported in terrestrial habitats for the first time.
Anastomitrabeculia didymospora is a putative species accommodated in Anastomitrabeculiaceae. Bhunjun et al. [71] reported that the species that occurred on the bamboo host was submerged in freshwater. In this study, we also found the species occurring on a bamboo host in the terrestrial habitat near the waterfall. There are few studies concerning relationships between freshwater and terrestrial fungi [134,135,136,137]. Boonyuen et al. [136] mentioned that fungal species partially overlap between freshwater and terrestrial habitats, of which the submerged samples yielded the most fungal diversity. Boonyuen et al. [136] also suggested that the diversity of wood-inhabiting fungi depended on tree species, geography, and exposure period. There is no clear evidence to prove that terrestrial fungi will continue to thrive when submerged in water [137]. Kodseub et al. [137] attempted to investigate the differences in fungal communities that occurred in Magnolia liliifera wood from freshwater and terrestrial habitats. Kodseub et al. [137] mentioned that dominant fungi in the terrestrial environment were significantly different from fungi submerged in freshwater, and few species have been found in both freshwater and terrestrial habitats, suggesting that most fungi occurring on wood in terrestrial habitats did not thrive in freshwater habitats. According to Kodseub et al. [137], we hypothesized that A. didymospora is one of the few species that can survive in both freshwater and terrestrial habitats. The species may initially occur on a bamboo host in the terrestrial environment and continue to thrive in submerged freshwater.
Parabambusicolaceae shows to be heterogeneous, and it currently contains 12 genera, including the new genus introduced in this study. Even though most genera of Parabambusicolaceae contain a single species, they showed high genetic heterogeneity, which can be interpreted by their phylogenetic relationships. Most genera in Parabambusicolaceae are only represented by their sexual or asexual morph, except for Neoaquastroma. Hence, the morphology of some sexual and asexual genera could not be compared, which led to the generic status becoming questionable. More taxa sampling is required for a better understanding of each genus in Parabambusicolaceae.
Pyrenochaetopsis was introduced to accommodate phoma-like taxa that occurred on various host substrates [81,105,106,138]. The genus was previously treated in Cucurbitariaceae [72,107,139]. Later, Valenzuela-Lopez et al. [105] introduced the new family Pyrenochaetopsidaceae to accommodate this genus together with Neopyrenochaetopsis and Xenopyrenochaetopsis. Mapook et al. [106] determined the sexual morph of Pyrenochaetopsis, P. chromolaenae, for the first time. In the present study, the holomorph of P. yunnanensis sp. nov. is also determined. The sexual morph of P. yunnanensis can be distinguished from P. chromolaenae in having subglobose to subconical, or quadrilateral, glabrous ascomata and hyaline, fusiform, one to three-septate ascospores, whereas P. chromolaenae has globose ascomata with setose papilla and hyaline to pale brown or yellowish-brown, cylindrical to broadly fusiform, three to four-septate ascospores [106]. Pyrenochaetopsis yunnanensis is reported as a saprobe on bamboo host in Yunnan Province, China for the first time. Species of Pyrenochaetopsis are well-studied based on molecular analyses coupled with morphological characteristics of their asexual morph. Nevertheless, the sexual morph of this genus is still rarely detected.
In the present study, multigene phylogenetic analyses demonstrated that taxa in Tetraploa could be separated into two subclades. The main subclade (including the type species) comprises T. aristata (type species), T. bambusae sp. nov., T. dwibahubeeja, T. endophytica, T. obpyriformis, T. pseudoaristata, T. puzheheiensis, T. sasicola, T. thrayabahubeeja, T. yakushimensis, T. yunnanensis, and Tetraploa spp. (CY 112, KT 1684). These species formed a well-resolved subclade within Tetraplosphaeriaceae (Figure 4). The second subclade comprises T. aquatica, T. cylindrica, T. nagasakiensis and Tetraploa sp. (KT 2578). Tetraploa aquatica, T. cylindrica, and T. nagasakiensis formed a well-resolved subclade, clustered with Tetraploa sp. KT 2578 with low support and constituted independently basal to the main subclade. Multigene phylogenetic analyses showed that T. aquatica, T. cylindrica, and T. nagasakiensis may be distinct genera with Tetraploa, but generic clarification insight into the morphology-based taxonomy is needed in the future study. Tetraploa sasicola (KT 563, ex-type strain) also formed a separate branch with T. sasicola (FU31019) in this study and also concurred with Liao et al. [140]. Tetraploa sasicola strain FU31019 may not be conspecific with T. sasicola (KT 563) pending further study.

Author Contributions

Conceptualization, R.P. and P.C.; methodology, R.P.; software, R.P. and H.J.; validation, R.P., S.L. and P.C.; formal analysis, R.P. and H.J.; investigation, R.P. and P.C.; resources, R.P., H.J., C.-F.L. and S.X.; data curation, R.P.; writing—original draft preparation, R.P.; writing—review and editing, R.P., N.S. and P.C.; supervision, S.L, J.X. and P.C.; project administration, R.P.; funding acquisition, P.C., S.L. and J.X. All authors have read and agreed to the published version of the manuscript.

Funding

This research study is supported by the Yunnan Provincial Science and Technology Department, Key Project (Grant No. 202101AS070045) and NSFC-CGIAR Project “Characterization of roots and their associated rhizosphere microbes in agroforestry systems: ecological restoration in high-phosphorus environment” (Grant No. 31861143002).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data availability was mentioned in the manuscript. The novel taxa were registered in Index Fungorum (http://www.indexfungorum.org/Names/Names.asp, accessed on 13 May 2022) including Index Fungorum numbers IF 554966, IF 554968, IF 554979 and IF 554987. Final alignment and phylogenetic tree were deposited in TreeBase (https://www.treebase.org/, accessed on 25 March 2022) with submission ID: 29589, 29590, 29592 and 29593) and the newly generated sequences were deposited in GenBank (https://www.ncbi.nlm.nih.gov/genbank/submit/, accessed on 28 March 2022) followed as ITS: ON077079, ON077080, ON077075, ON077076, ON077077, ON077078; LSU: ON077068, ON077069, ON077064, ON077065, ON077066, ON077067; SSU: ON077074, ON077070, ON077071, ON077072, ON077073; rpb2: ON075067, ON075066; tef1-α: ON075062, ON075063, ON075058, ON075059, ON075060, ON075061; tub2: ON075064, ON075065.

Acknowledgments

R.P. thanks the Visiting Scholars for World Class Research Collaboration Reinventing university grant 2021 for providing visiting scholarship. P.C. would like to thank the National Research Council of Thailand (NRCT) grant number N41A640165 for funding. The Biology Experimental Center, Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences is thanked for providing the facilities of the molecular laboratory. Shaun Pennycook at Manaaki Whenua—Landcare Research, New Zealand, is thanked for assistance in naming the novel taxa. Austin G. Smith at World Agroforestry (ICRAF), Kunming Institute of Botany, China, is thanked for editing English grammar. Nalin N. Wijayawardene at the Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food Engineering, Qujing Normal University, China is thanked for sample collection. Reinventing University 2021 is thanked for supporting the research assistant. H.-B.J. would like to thank Mae Fah Luang University, Thailand for his Ph.D. scholarship. Chiang Mai University, Thailand is thanked for partial research financial support.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Phylogram generated from RAxML analysis of a concatenated LSU-SSU-ITS-tef1-α sequence dataset to represent the phylogenetic relationships of taxa in Anastomitrabeculiaceae, Halojulellaceae, and Neohendersoniaceae. Bootstrap support values for ML and MP equal to or greater than 70% and the Bayesian posterior probabilities equal to or higher than 0.95 PP are indicated above the nodes as ML/MP/PP. Support values lower than 70% ML/MP and 0.95 PP are indicated by a hyphen (-). Ex-type strains are in bold and the newly generated sequences are indicated in blue.
Figure 1. Phylogram generated from RAxML analysis of a concatenated LSU-SSU-ITS-tef1-α sequence dataset to represent the phylogenetic relationships of taxa in Anastomitrabeculiaceae, Halojulellaceae, and Neohendersoniaceae. Bootstrap support values for ML and MP equal to or greater than 70% and the Bayesian posterior probabilities equal to or higher than 0.95 PP are indicated above the nodes as ML/MP/PP. Support values lower than 70% ML/MP and 0.95 PP are indicated by a hyphen (-). Ex-type strains are in bold and the newly generated sequences are indicated in blue.
Jof 08 00630 g001
Jof 08 00630 g002 550
Figure 2. Phylogram generated from RAxML analysis of a concatenated ITS-LSU-SSU-tef1-α sequence dataset to represent the phylogenetic relationships of novel taxa in Parabambusicolaceae with other related families in Pleosporales. Bootstrap support values for ML equal to or greater than 70% and the Bayesian posterior probabilities equal to or higher than 0.95 PP are indicated above the nodes as ML/PP. Support values lower than 70% ML and 0.95 PP are indicated by a hyphen (-). Ex-type strains are in bold, and the new species is indicated in blue. The arrow in the figure is indicated the support value at the node.
Figure 2. Phylogram generated from RAxML analysis of a concatenated ITS-LSU-SSU-tef1-α sequence dataset to represent the phylogenetic relationships of novel taxa in Parabambusicolaceae with other related families in Pleosporales. Bootstrap support values for ML equal to or greater than 70% and the Bayesian posterior probabilities equal to or higher than 0.95 PP are indicated above the nodes as ML/PP. Support values lower than 70% ML and 0.95 PP are indicated by a hyphen (-). Ex-type strains are in bold, and the new species is indicated in blue. The arrow in the figure is indicated the support value at the node.
Jof 08 00630 g002
Jof 08 00630 g003 550
Figure 3. Phylogram generated from RAxML analysis of a concatenated LSU-ITS-rpb2-tub2 sequence dataset to represent the phylogenetic relationships of a novel taxon in Pyrenochaetopsidaceae. Bootstrap support values for ML and MP equal to or greater than 70% and the Bayesian posterior probabilities equal to or higher than 0.95 PP are indicated above the nodes as ML/MP/PP. Support values lower than 70% ML/MP and 0.95 PP are indicated by a hyphen (-). Ex-type strains are in bold, and the new species is indicated in blue. The arrow is indicated the support value at the node.
Figure 3. Phylogram generated from RAxML analysis of a concatenated LSU-ITS-rpb2-tub2 sequence dataset to represent the phylogenetic relationships of a novel taxon in Pyrenochaetopsidaceae. Bootstrap support values for ML and MP equal to or greater than 70% and the Bayesian posterior probabilities equal to or higher than 0.95 PP are indicated above the nodes as ML/MP/PP. Support values lower than 70% ML/MP and 0.95 PP are indicated by a hyphen (-). Ex-type strains are in bold, and the new species is indicated in blue. The arrow is indicated the support value at the node.
Jof 08 00630 g003
Jof 08 00630 g004 550
Figure 4. Phylogram generated from RAxML analysis of a concatenated LSU-ITS-SSU-tub2-tef1-α sequence dataset to represent the phylogenetic relationships of the novel taxon in Tetraploasphaeriaceae. Bootstrap support values for ML and MP equal to or greater than 70% and the Bayesian posterior probabilities equal to or higher than 0.95 PP are indicated above the nodes as ML/MP/PP. Support values lower than 70% ML/MP and 0.95 PP are indicated by a hyphen (-). Ex-type strains are in bold, and the new species is indicated in blue.
Figure 4. Phylogram generated from RAxML analysis of a concatenated LSU-ITS-SSU-tub2-tef1-α sequence dataset to represent the phylogenetic relationships of the novel taxon in Tetraploasphaeriaceae. Bootstrap support values for ML and MP equal to or greater than 70% and the Bayesian posterior probabilities equal to or higher than 0.95 PP are indicated above the nodes as ML/MP/PP. Support values lower than 70% ML/MP and 0.95 PP are indicated by a hyphen (-). Ex-type strains are in bold, and the new species is indicated in blue.
Jof 08 00630 g004
Table
Table 1. GenBank accession numbers used in the phylogenetic analyses. The ex-type cultures are indicated with superscript “T”, and the newly generated sequences are indicated in bold.
Table 1. GenBank accession numbers used in the phylogenetic analyses. The ex-type cultures are indicated with superscript “T”, and the newly generated sequences are indicated in bold.
TaxonVoucher/Strain No.Family GenBank Accession Number
ITSLSUSSUrpb2 tub2 tef1-α
Anastomitrabeculia didymosporaMFLUCC 16-0412 TAnastNR_172008MW412978NG_073568n/an/aMW411338
Anastomitrabeculia didymosporaMFLUCC 16-0417AnastMW413897MW413899MW413898n/an/aMW411339
Anastomitrabeculia didymosporaMFLUCC 11-0197AnastON077079ON077068n/an/an/aON075062
Anastomitrabeculia didymosporaMFLUCC 11-0200AnastON077080ON077069ON077074ON075067n/aON075063
Aquastroma magniostiolataKT 2485/HHUF 30122 TParabNR_153583NG_056936NG_061000n/an/aAB808486
Aquatisphaeria thailandicaMFLUCC 21-0025 TTetraMW890969MW890763MW890967n/an/an/a
Aquatisphaeria thailandicaDLUCC B151Tetran/aMW890764MW890968n/an/an/a
Bambusicola loculataMFLUCC 13-0856 TBambuNR_153609NG_069267NG_065061KP761715n/aKP761724
Bambusicola massariniaMFLUCC 11-0389 TBambuNR_121548NG_058658NG_061198KP761716n/aKP761725
Brevicollum hyalosporumMFLUCC 17-0071NeoheMG602204MG602200MG602202n/an/aMG739516
Brevicollum hyalosporumMAFF 243400 TNeoheNR_156334NG_058715NG_065123LC271249n/aLC271245
Brevicollum versicolorHHUF 30591 TNeoheNR_156335NG_058716NG_065124LC271250n/aLC271246
Camarographium koreanumCBS 117159 TMacroJQ044432JQ044451n/an/an/an/a
Crassiparies quadrisporusKH111/HHUF 30409 TNeoheNR_148185NG_059028NG_061267n/an/an/a
Crassiparies quadrisporusKT 2986/HHUF 30590NeoheLC271244LC271241LC271238LC271252n/aLC271248
Dendryphiella fasciculataMFLUCC 17-1074 TDictyoNR_154044NG_059177n/an/an/an/a
Dictyocheirospora aquaticaKUMCC 15-0305 TDictyoNR_154030KY320513n/an/an/an/a
Dictyosporium elegansNBRC 32502DictyoDQ018087DQ018100DQ018079n/an/an/a
Didymocrea sadasivaniiCBS 438.65DidymoMH858658DQ384103DQ384074n/an/an/a
Didymosphaeria rubi-ulmifoliiMFLUCC 14-0023 TDidymon/aKJ436586NG_063557n/aKJ939277n/a
Ernakulamia cochinensisPRC 3992TetraLT964671LT964670n/an/aLT964672n/a
Ernakulamia cochinensisMFLUCC 18-1237TetraMT627670MN913716MT627670n/an/an/a
Ernakulamia krabiensisKUMCC 18-0237 TTetraNR_163341NG_066314NG_065780MK434872n/an/a
Ernakulamia tanakaiiNFCCI 4617TetraMN937228MN937210n/an/aMN938311n/a
Ernakulamia tanakaiiNFCCI 4615 TTetraMN937229MN937211n/an/aMN938312n/a
Ernakulamia tanakaiiNFCCI 4616TetraMN937227MN937209n/an/aMN938310n/a
Ernakulamia xishuangbannaensisKUMCC 17-0187 TTetraMH275080MH260314MH260354n/an/an/a
Falciformispora lignatilisBCC 21117TremaKF432942GU371826GU371834n/an/aGU371819
Halojulella avicenniaeBCC 20173Halojn/aGU371822GU371830GU371786n/aGU371815
Halojulella avicenniaeBCC 18422Halojn/aGU371823GU371831GU371787n/aGU371816
Halojulella avicenniaePUFD542HalojMK028713MK026757MK026754MN532682n/an/a
Helminthosporium aquaticumMFLUCC 15-0357 TMassaNR_155170NG_059656NG_063601n/an/an/a
Katumotoa bambusicolaKT 1517a/HHUF 28661 TLentiNR_154103NG_059386NG_060989AB539095n/aAB539108
Lonicericola fuyuanensisMFLU 19-2850 TParabNR_172419NG_073809NG_070329n/an/aMN938324
Lonicericola hyaloseptisporaKUMCC 18-0149 TParabNR_164294NG_066434NG_067680n/an/an/a
Lonicericola hyaloseptisporaKUMCC 18-0150ParabMK098194MK098200MK098206n/an/aMK098210
Macrodiplodiopsis desmazieriCBS 140062 TMacroNR_132924NG_058182n/an/an/an/a
Magnicamarosporium iriomotenseKT 2822/HHUF 30125 TSulcaNR_153445NG_059389NG_060999n/an/aAB808485
Massarina eburneaCBS 473.64MassaOM337528MH877786GU296170GU371732n/aGU349040
Medicopsis romeroiCBS 252.60TNeoheNR_130697NG_057800NG_061069KF015708n/aKF015678
Medicopsis romeroiCBS 132878NeoheKF015658KF015622KF015648KF015709n/aKF015682
Medicopsis romeroiCBS 122784NeoheKF366447EU754208EU754109KF015707n/aKF015679
Melanomma pulvis-pyriusCBS 124080MelanMH863349MH874873GU456302GU456350n/aGU456265
Monodictys sp.JO 10Parabn/aAB807552AB797262n/an/aAB808528
Monodictys sp.KH 331Parabn/aAB807553AB797263n/an/aAB808529
Multilocularia bambusaeMFLUCC 11-0180 TParabNR_148099NG_059654NG_061229n/an/aKU705656
Multiseptospora thailandicaMFLUCC 11-0183 TParabNR_148080NG_059554KP753955n/an/aKU705657
Multiseptospora thailandicaMFLUCC 11-0204ParabKU693447KU693440KU693444n/an/aKU705659
Multiseptospora thailandicaMFLUCC 12-0006ParabKU693448KU693441KU693445n/an/aKU705660
Multiseptospora thysanolaenaeMFLUCC 11-0202 TParabn/aNG_059655NG_063600n/an/aKU705658
Muritestudina chiangraiensisMFLUCC 17-2551 TTestuMG602247MG602248MG602249MG602250n/aMG602251
Neoaquastroma bauhiniaeMFLUCC 16-0398 TParabNR_165217NG_067814NG_070696MH028251n/aMH028247
Neoaquastroma bauhiniaeMFLUCC 17-2205ParabMH025953MH023320MH023316MH028252n/aMH028248
Neoaquastroma guttulatumMFLUCC 14-0917 TParabKX949739KX949740KX949741n/an/aKX949742
Neoaquastroma krabienseMFLUCC 16-0419 TParabNR_165218NG_067815NG_067670n/an/aMH028249
Neobambusicola strelitziaeCBS 138869 TSulcaNR_137945NG_058125n/an/an/aMG976037
Neohendersonia kickxiiCBS 112403 TNeoheNR_154248NG_058264n/an/an/an/a
Neohendersonia kickxiiCBS 122938NeoheKX820257KX820268n/an/an/an/a
Neohendersonia kickxiiCPC 24865NeoheKX820259KX820270n/an/an/an/a
Neomultiseptospora yunnanensisKUMCC 21-0411 TParabOL898884OL898925OL898890n/an/aOL964282
Neomultiseptospora yunnanensisKUN-HKAS 122240 TParabOL898885OL898886OL898891n/an/aOL964283
Neopyrenochaetopsis hominis CBS 143033 TPyrenLN880536 LN880537 n/aLT593073LN880539n/a
Palmiascoma gregariascomumMFLUCC 11-0175 TBambuNR_154316NG_059557KP753958KP998466n/an/a
Parabambusicola aquaticaMFLUCC 18-1140 TParabNR_171877NG_073791n/an/an/an/a
Parabambusicola bambusinaH 4321/MAFF 239462ParabLC014578AB807536AB797246n/an/aAB808511
Parabambusicola bambusinaKH 139/MAFF 243823ParabLC014579AB807537AB797247n/an/aAB808512
Parabambusicola bambusinaKT 2637/MAFF 243822ParabLC014580AB807538AB797248n/an/aAB808513
Parabambusicola hongheensisKUMCC 21-0410 TParabOL898880OL898921OL898886n/an/an/a
Parabambusicola thysanolaenaeKUMCC 18-0147 TParabNR_164044NG_066435NG_067681n/an/aMK098209
Parabambusicola thysanolaenaeKUMCC 18-0148ParabMK098193MK098198MK098202n/an/aMK098211
Paraconiothyrium estuarinumCBS 109850 TDidymNR_166007MH874432AY642522LT854937JX496355n/a
Paramonodictys hongheensisKUMCC 21-0343 TParabOL436229OL436227OL436232n/an/aOL505582
Paramonodictys hongheensisKUMCC 21-0346ParabOL436235OL436224OL436225n/an/aOL505583
Paramonodictys solitariusGZCC 20-0007 TParabMN901152MN897835MN901118MT023015n/aMT023012
Paramonodictys solitariusMFLUCC 17-2353ParabMT627707MN913703MT864299n/an/aMT954397
Paramonodictys yunnanensisKUMCC 21-0337 TParabOL436231OL436226OL436230n/an/aOL505585
Paramonodictys yunnanensisKUMCC 21-0347ParabOL436233OL436228OL436234n/an/aOL505586
Paramultiseptospora bambusaeKUN-HKAS 122241ATParabON077075ON077064ON077070n/an/aON075058
Paramultiseptospora bambusaeKUN-HKAS 122241BParabON077076ON077065ON077071n/an/aON075059
Paraphaeosphaeria michotiiMFLUCC 13-0349 TDidymNR_155640NG_059522KJ939285KP998465n/an/a
Paratrimmatostroma kunmingensisKUN-HKAS 102224A TParabMK098192MK098196MK098204n/an/aMK098208
Paratrimmatostroma kunmingensisKUN-HKAS 102224B TParabMK098195MK098201MK098207n/an/an/a
Poaceascoma helicoidesMFLUCC 11-0136 TLentiNR_154317NG_059565NG_061205KP998460n/aKP998461
Polyplosphaeria fuscaKT 1043TetraAB524788AB524603AB524462n/aAB524850AB524819
Polyplosphaeria fuscaKT 1640TetraAB524790AB524605AB524464n/aAB524852AB524821
Polyplosphaeria fuscaKT 1616 TTetraAB524789AB524604AB524463n/aAB524851AB524820
Polyplosphaeria fuscaKT 1686Tetran/aAB524606AB524465n/an/an/a
Polyplosphaeria fuscaKT 2124TetraAB524791AB524607AB524466n/aAB524853AB524822
Polyplosphaeria nabanheensisKUMCC 16-0151 TTetraMH275078MH260312MH260352n/aMH412745n/a
Polyplosphaeria pandanicolaKUMCC 17-0180 TTetraMH275079MH260313MH260353n/an/an/a
Polyplosphaeria thailandicaMFLUCC 15-0840 TTetraKU248766KU248767n/an/an/an/a
Pseudochaetosphaeronema larenseCBS 640.73 TMacroNR_132038NG_057978NG_061147KF015706n/aKF015684
Pseudocoleophoma calamagrostidisKT 3284/HHUF 30450 TDictyNR_154375NG_059804NG_061264n/an/aLC014614
Pseudomonodictys tectonaeMFLUCC 12-0552 TParabn/aNG_059590NG_061213KT285572n/aKT285571
Pseudotetraploa curviappendiculataHHUF 28582 TTetraAB524792AB524608AB524467n/aAB524854AB524823
Pseudotetraploa curviappendiculataKT 2558TetraAB524794AB524610AB524469n/aAB524856AB524825
Pseudotetraploa curviappendiculataHHUF 28590TetraAB524793AB524609AB524468n/aAB524855AB524824
Pseudotetraploa javanicaHHUF 28596TetraAB524795AB524611AB524470n/aAB524857AB524826
Pseudotetraploa longissimaHHUF 28580 TTetraAB524796AB524612AB524471n/aAB524858AB524827
Pseudotetraploa rajmachiensisNFCCI 4619TetraMN937222MN937204n/an/aMN938305n/a
Pseudotetraploa rajmachiensisNFCCI 4618 TTetraMN937221MN937203n/an/aMN938304n/a
Pseudotetraploa rajmachiensisNFCCI 4620TetraMN937223MN937205n/an/aMN938306n/a
Pyrenochaetopsis americana FMR 1375 TPyrenLT592912 LN907368 n/aLT593050LT592981n/a
Pyrenochaetopsis yunnanensis KUMCC 21-0843PyrenON077077 ON077066 ON077072ON075066ON075064ON075060
Pyrenochaetopsis botulispora UTHSC:DI 16-289PyrenLT592941 LN907432 n/aLT593080LT593010n/a
Pyrenochaetopsis botulispora UTHSC:DI 16-297PyrenLT592945 LN907440 n/aLT593084LT593014n/a
Pyrenochaetopsis botulispora CBS 142458 TPyrenLT592946 LN907441 n/aLT593085LT593015n/a
Pyrenochaetopsis chromolaenaeMFLUCC: 17-1440 TPyrenMT214378 MT214472 NG_070172MT235827n/aMT235790
Pyrenochaetopsis confluens CBS 142459 TPyrenLT592950 LN907446 n/aLT593089LT593019n/a
Pyrenochaetopsis decipiens CBS 343.85 TPyrenLT623223 GQ387624 NG_065569LT623280LT623240n/a
Pyrenochaetopsis globosa CBS 143034 TPyrenLT592934 LN907418 n/aLT593072LT593003n/a
Pyrenochaetopsis indica CBS 124454 TPyrenLT623224 GQ387626 GQ387565LT623281LT623241n/a
Pyrenochaetopsis kuksensis CBS 146534/MeND-F-57 TPyrenMT371092 MT371397 n/aMT372656MT372662n/a
Pyrenochaetopsis kuksensis MeND-F-58PyrenMT371093 MT371398 n/aMT372657MT372663n/a
Pyrenochaetopsis leptospora CBS 101635 TPyrenJF740262 GQ387627 NG_063097LT623282LT623242MF795881
Pyrenochaetopsis leptospora CBS 122787PyrenLT623225 EU754151 n/aLT623283LT623243n/a
Pyrenochaetopsis microspora CBS 102876 TPyrenLT592899 LN907341 NG_065571LT593037LT592968n/a
Pyrenochaetopsis paucisetosa CBS 142460 TPyrenLT592897 LN907336 n/aLT593035LT592966n/a
Pyrenochaetopsis poae CBS 136769 TPyrenKJ869117 KJ869175 n/aLT623286KJ869243n/a
Pyrenochaetopsis rajhradensis CBS 146846 TPyrenMT853115 MT853182 n/aMT857727MT857726MT857725
Pyrenochaetopsis setosissima CBS 119739 TPyrenLT623227 GQ387632 n/aLT623285LT623245n/a
Pyrenochaetopsis sinensis CGMCC 3.19296 TPyrenMK348586 MK348581 n/aMK355077MK348221n/a
Pyrenochaetopsis tabarestanensis CBS 139506/IBRC: M 30051 TPyrenKF730241 KF803343 NG_065034n/aKX789523n/a
Pyrenochaetopsis terricola HGUP 1802 TPyrenMH697394 MH697393 n/aMH697395MH697392n/a
Pyrenochaetopsis uberiformis CBS 142461/FMR 13769 TPyrenLT592935 LN907420 n/aLT593074LT593004n/a
Quadricrura bicornisCBS 125427 TTetraAB524797AB524613AB524472n/aAB524859AB524828
Quadricrura meridionalisKT 2607 TTetraAB524798AB524614AB524473n/aAB524860AB524829
Quadricrura septentrionalisKT 920TetraAB524801AB524617AB524476n/aAB524863AB524832
Quadricrura septentrionalisCBS 125429TetraAB524799AB524615AB524474n/aAB524861AB524830
Quadricrura septentrionalisCBS 125431TetraAB524802AB524618AB524477n/aAB524864AB524833
Quadricrura septentrionalisCBS 125432TetraAB524803AB524619AB524478n/aAB524865AB524834
Quadricrura septentrionalisCBS 125433TetraAB524804AB524620AB524479n/aAB524866AB524835
Quadricrura septentrionalisCBS 125430 TTetraAB524800AB524616AB524475n/aAB524862AB524831
Scolecohyalosporium submersumKUMCC 21-0412 TParabOL898883OL898924OL898889n/an/aOL964281
Scolecohyalosporium submersumKUMCC 21-0413ParabOL898881OL898922OL898887n/an/aOL964279
Scolecohyalosporium submersumKUN-HKAS 122242ParabOL898882OL898923OL898888n/an/aOL964280
Setoseptoria phragmitisCBS 114802 TLentiKF251249KF251752n/aKF252254KF252732KF253199
Shrungabeeja longiappendiculataBCC 76463 TTetraKT376474KT376472KT376471n/an/an/a
Shrungabeeja longiappendiculataBCC 76464TetraKT376475KT376473n/an/an/an/a
Shrungabeeja vadirajensisMFLUCC 17-2362TetraMT627681MN913685n/an/an/an/a
Spegazzinia tessarthraSH 287Didymn/aAB807584AB797294n/an/aAB808560
Sulcatispora acerinaKT 2982 TSulcaLC014597LC014610LC014605n/an/aLC014615
Sulcatispora berchemiaeKT 1607/ HHUF 29097 TSulcaNR_153444NG_059390NG_064843n/an/aAB808509
Tetraploa aquaticaMFLU 19-0995 TTetraMT530448MT530452n/an/an/an/a
Tetraploa aquaticaMFLU 19-0996TetraMT530449MT530453MT530454n/an/an/a
Tetraploa aristataCBS 996.70TetraAB524805AB524627AB524486n/aAB524867AB524836
Tetraploa bambusaeKUMCC 21-0844TetraON077078ON077067ON077073n/aON075065ON075061
TetraploacylindricaKUMCC 20-0205 TTetraMT893205MT893204MT893203n/aMT899418MT899417
Tetraploa dashaoensisKUMCC 21-0010 TTetraOL473549OL473555OL473556n/aOL505601OL505599
Tetraploa dwibahubeejaNFCCI 4621 TTetraMN937225MN937207n/an/aMN938308n/a
Tetraploa dwibahubeejaNFCCI 4622TetraMN937224MN937206n/an/aMN938307n/a
Tetraploa dwibahubeejaNFCCI 4623TetraMN937226MN937208n/an/aMN938309n/a
Tetraploa endophyticaCBS 147114 TTetran/aMW659165KT270279n/an/aMW659821
Tetraploa nagasakiensisKUMCC 18-0109TetraMK079890MK079891MK079888n/an/an/a
Tetraploa nagasakiensisKT 1682 TTetraAB524806AB524630AB524489n/aAB524868AB524837
Tetraploa obpyriformisKUMCC 21-0011 TTetraOL473558OL473554OL473557n/aOL505600OL505598
Tetraploa pseudoaristataNFCCI 4624 TTetraMN937232MN937214n/an/aMN938315n/a
Tetraploa pseudoaristataNFCCI 4625TetraMN937230MN937212n/an/aMN938313n/a
Tetraploa pseudoaristataNFCCI 4626TetraMN937231MN937213n/an/aMN938314n/a
Tetraploa puzheheiensisMFLUCC 20-0151 TTetraMT627744MT627655n/an/an/an/a
Tetraploa sasicolaFU31019TetraMN937236MN937218n/an/an/an/a
Tetraploa sasicolaKT 563 TTetraAB524807AB524631AB524490n/aAB524869AB524838
Tetraploa sp.KT 1684Tetran/aAB524628AB524487n/an/an/a
Tetraploa sp.KT 2578Tetran/aAB524629AB524488n/an/an/a
Tetraploa sp.CY112TetraHQ607964n/an/an/an/an/a
Tetraploa thrayabahubeejaNFCCI 4627 TTetraMN937235MN937217n/an/aMN938318n/a
Tetraploa thrayabahubeejaNFCCI 4628TetraMN937233MN937215n/an/aMN938316n/a
Tetraploa thrayabahubeejaNFCCI 4629TetraMN937234MN937216n/an/aMN938317n/a
Tetraploa yakushimensisKT 1906/HHUF 29652 TTetraNR_119405NG_042330NG_064836n/aAB524870AB524839
Tetraploa yunnanensisMFLUCC 19-0319 TTetraMT627743MN913735MT864341MT878451n/an/a
Trematosphaeria griseaCBS 332.50 TTremaNR_132039NG_057979NG_062930KF015720n/aKF015698
Trematosphaeria_pertusaCBS 122368 TTremaNR_132040NG_057809n/an/an/an/a
Tingoldiago graminicolaKH 68 TLentiLC014598AB521743AB521726n/an/aAB808561
Triplosphaeria acutaKT 1170 TTetraAB524809AB524633AB524492n/aAB524871AB524840
Triplosphaeria cylindricaKT 1800TetraAB524810AB524635AB524494n/aAB524872AB524841
Triplosphaeria cylindricaKT 2550TetraAB524811AB524636AB524495n/aAB524873AB524842
Triplosphaeria maximaKT 870/HHUF 29390 TTetraAB524812AB524637AB524496n/aAB524874AB524843
Triplosphaeria sp.HHUF 27481TetraAB524815AB524640AB524499n/aAB524877AB524846
Triplosphaeria sp.KT 2546TetraAB524816AB524641AB524500n/aAB524878AB524847
Triplosphaeria yezoensisKT 1715 TTetraAB524813AB524638AB524497n/aAB524875AB524844
Triplosphaeria yezoensisKT 1732TetraAB524814AB524639AB524498n/aAB524876AB524845
Trematosphaeria griseaCBS 332.50 TTremaNR_132039NG_057979NG_062930KF015720n/aKF015698
Trematosphaeria pertusaCBS 122368 TTremaNR_132040NG_057809n/an/an/an/a
Xenopyrenochaetopsis pratorum CBS 445.81/FMR 14878 TPyrenJF740263 GU238136 NG_062792KT389671KT389846n/a
Abbreviations: BCC: BIOTEC Culture Collection, Bangkok, Thailand; BCRC: FU: Bioresource Collection and Research Center Collection, Taiwan; CBS: the Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands; CGMCC: China General Microbiological Culture Collection Center; CPC: Collection of Pedro Crous housed at CBS; DLUCC: Dali University Culture Collection, Yunnan, China; FMR: Facultat de Medicina, Universitat Rovira i Virgili, Reus, Spain; GZCC: Guizhou Culture Collection, Guizhou, China; H: University of Helsinki, Helsinki, Finland; HGUP: Herbarium of Department of Plant Pathology, Guizhou University, Guizhou, China; HHUF: the Herbarium of Hirosaki University Fungi, Aomori, Japan; IBRC: M: Herbarium of the Plant bank, Iranian Biological Resource Center; KH: K. Hirayama; KT: Kazuaki Tanaka, Japan; KUMCC: Kunming Institute of Botany Culture Collection, Yunnan, China; KUN-HKAS: Herbarium of Cryptogams Kunming Institute of Botany Academia Sinica, Yunnan, China; MeND-F: Fungal Collection of Mendeleum—Institute of Genetics, Mendel University, Czech Republic; MAFF: the National Institute of Agrobiological Sciences, Japan; MFLU: the Herbarium of Mae Fah Luang University Chiang Rai, Thailand; MFLUCC: Mae Fah Luang University Culture Collection, Chiang Rai, Thailand; NBRC: Biological Resource Center, National Institute of Technology and Evaluation, Chiba, Japan; NFCCI: National Fungal Culture Collection of India, Maharashtra, India; PRC: the Herbarium of the Charles University, Prague, Czech Republic; PUFU: Culture Collection at Pondicherry University, Puducherry, India; SH: S. Hughes; UTHSC: Fungus Testing Laboratory at the University of Texas Health Science Center, San Antonio, Texas, USA. Abbreviations of families: Anast: Anastomitrabeculiaceae; Bambu: Bambusicolaceae; Dicty: Dictyosporiaceae; Didym: Didymosphaeriaceae; Haloj: Halojulellaceae; Lenti: Lentitheciaceae; Macro: Macrodiplodiopsidaceae; Massa: Massarinaceae; Melan: Melanommataceae; Neohe: Neohendersoniaceae; Parab: Parabambusicolaceae; Pyren: Pyrenochaetopsidaceae; Sulca: Sulcatisporaceae; Testu: Testudinaceae; Tetra: Tetraploasphaeriaceae; Trema: Trematosphaeriaceae.
Table
Table 2. The best nucleotide substitution model for each locus based on the Akaike Information Criterion (AIC) generated by MrModeltest v. 2.3.
Table 2. The best nucleotide substitution model for each locus based on the Akaike Information Criterion (AIC) generated by MrModeltest v. 2.3.
Phylogenetic AnalysesNucleotide Substitution Models
ITSLSUSSUrpb2 tef1-α tub2
A1: AnastomitrabeculiaceaeSYM+GGTR+I+GGTR+In/aGTR+I+Gn/a
A2: ParabambusicolaceaeGTR+I+GGTR+I+GHKY+I+Gn/aGTR+I+Gn/a
A3: PyrenochaetopsidaceaeSYM+GGTR+In/aSYM+I+GGTR+Gn/a
A4: TetraploasphaeriaceaeGTR+I+GGTR+I+GGTR+I+Gn/aHKY+I+GGTR+I+G
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Phookamsak, R.; Jiang, H.; Suwannarach, N.; Lumyong, S.; Xu, J.; Xu, S.; Liao, C.-F.; Chomnunti, P. Bambusicolous Fungi in Pleosporales: Introducing Four Novel Taxa and a New Habitat Record for Anastomitrabeculia didymospora. J. Fungi 2022, 8, 630. https://doi.org/10.3390/jof8060630

AMA Style

Phookamsak R, Jiang H, Suwannarach N, Lumyong S, Xu J, Xu S, Liao C-F, Chomnunti P. Bambusicolous Fungi in Pleosporales: Introducing Four Novel Taxa and a New Habitat Record for Anastomitrabeculia didymospora. Journal of Fungi. 2022; 8(6):630. https://doi.org/10.3390/jof8060630

Chicago/Turabian Style

Phookamsak, Rungtiwa, Hongbo Jiang, Nakarin Suwannarach, Saisamorn Lumyong, Jianchu Xu, Sheng Xu, Chun-Fang Liao, and Putarak Chomnunti. 2022. "Bambusicolous Fungi in Pleosporales: Introducing Four Novel Taxa and a New Habitat Record for Anastomitrabeculia didymospora" Journal of Fungi 8, no. 6: 630. https://doi.org/10.3390/jof8060630

APA Style

Phookamsak, R., Jiang, H., Suwannarach, N., Lumyong, S., Xu, J., Xu, S., Liao, C. -F., & Chomnunti, P. (2022). Bambusicolous Fungi in Pleosporales: Introducing Four Novel Taxa and a New Habitat Record for Anastomitrabeculia didymospora. Journal of Fungi, 8(6), 630. https://doi.org/10.3390/jof8060630

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