One New Species and Two New Host Records of Apiospora from Bamboo and Maize in Northern Thailand with Thirteen New Combinations

Abstract

The genus Apiospora is known as a cosmopolitan genus, found across various substrates. In this study, four Apiospora taxa were obtained from the decaying stems of bamboo and maize in northern Thailand. Apiospora collections were compared with known species based on the morphological characteristics and the DNA sequence data of internal transcribed spacer (ITS), the partial large subunit nuclear rDNA (LSU), the translation elongation factor 1-alpha gene (TEF1-α) and beta-tubulins (TUB2). Apiospora chiangraiense sp. nov. and two new host records (Ap. intestini and Ap. rasikravindra) are introduced here based on the morphological characteristics and multi-locus analyses. Additionally, thirteen species previously identified as Arthrinium are introduced as new combinations in Apiospora, viz., Ap. acutiapica, Ap. bambusicola, Ap. biserialis, Ap. cordylines, Ap. cyclobalanopsidis, Ap. euphorbiae, Ap. gelatinosa, Ap. locuta-pollinis, Ap. minutispora, Ap. pseudorasikravindrae, Ap. septate, Ap. setariae and Ap. sorghi.

1. Introduction

Apiospora was introduced by Saccardo with Ap. montagnei as the type species [1]. The genus was reported in both sexual and asexual morphs. The sexual morphs are characterized by multi-locular perithecial stromata with hyaline ascospores surrounded by a thick gelatinous sheath [2,3,4]. The asexual morph of Apiospora was characterized by basauxic conidiogenesis, with globose to subglobose conidia, which are usually lenticular in the side view, obovoid and pale brown to brown [2,5,6]. Species of Apiospora are similar in morphology, thus it is difficult to distinguish them without molecular phylogenetic data. The size, color and shape of conidia and the morphology of conidiophores (e.g., size, shape and septation) should be used together to better identify them. For example, conidiophores of some species reduce to conidiogenous cells (e.g., Ap. bambusae, Ap. acutiapicum), while some species have semi-micronematous to macronematous conidiophores (e.g., Ap. bambusicola, Ap. intestini).

Apiospora species have a worldwide distribution and can be found from various hosts [3,7,8,9]. Most Apiospora species are associated with plants as endophytes, pathogens or saprobes, especially on bamboo [2,3,10,11]. To date, more than 25 species have been found from bamboo [2,3,10,11]. Apiospora species can cause leaf necrosis and twig dieback in the olive tree (Olea europaea), leaf edge spot of the peach (Prunus persica), blight disease of bamboo (Schizostachyum), leaf spot of rosemary (Salvia rosmarinus), kernel blight of barley (Hordeum vulgare) and brown culm streak of Phyllostachys praecox [11,12,13,14,15,16,17]. Some species have also been isolated from lichens, air, soil and animal tissues, and a few species are human pathogens which can cause cutaneous infections in humans [9,18,19,20,21,22,23].

The morphological relationships between Arthrinium and Apiospora have long been debated after Ellis [24], as the morphological characteristics of these two genera are similar and difficult to distinguish based on morphology alone. Apiospora was synonymized under Arthrinium by Crous et al. [3] as they found that Apiospora is the sexual morph of Arthrinium and phylogenetic analyses showed that the two genera formed a monophyletic clade. Meanwhile, the phylogenic analyses results from Pintos et al. [25] showed Arthrinium forms a monophyletic clade that separates from all other sequences of Apiospora and suggested that Arthrinium s. str. could actually be phylogenetically different from Apiospora, but this is in need of clarification using the phylogeny of additional species before making a conclusive taxonomic decision on the issue. Recently, Pintos and Alvarado [4] showed that Apiospora and Arthrinium present independent lineages, thus they separate well into two genera.

Morphologically, the conidia of Apiospora are more or less rounded in the face view and lenticular in the side view and conidiophores sometimes develop forming acervuli. Whereas the conidia of Arthrinium are variously shaped (angular, curved, fusiform, globose, polygonal, navicular) and the conidiophores of some species have thick blackish septa [14]. Ecologically, Apiospora species are mostly reported on Poaceae, while Arthrinium species commonly occur on Cyperaceae and Juncaceae. Moreover, Apiospora has a worldwide distribution, and species in the genus can be found from tropical and subtropical areas to the Mediterranean, temperate and cold regions, while Arthrinium species are rarely found from tropical and subtropical habitats. Hence, Pintos and Alvarado [4] considered that genetic, morphological and ecological differences are sufficient to support the taxonomic separation of the two genera, and accordingly, 55 Arthrinium species were transferred to Apiospora based on the phylogenetic analyses. Presently, 117 records of Apiospora are listed in the Index Fungorum [26].

The aims of this study are to determine the phylogenetic placement of the genus Apiospora and describe the three taxa that were isolated from maize and bamboo in Chiang Rai province, Thailand. Based on the morphological characteristics and phylogenetic analyses of a combined dataset of the internal transcribed spacer (ITS), the partial large subunit nuclear rDNA (LSU), the translation elongation factor 1-alpha gene (TEF1-α) and beta-tubulins (TUB2), a new species, Ap. chiangraiense, as well as two new host records, Ap. rasikravindrae and Ap. intestini, are introduced. In addition, thirteen species of Arthrinium were synonymized under Apiospora.

2. Materials and Methods

2.1. Sample Collection, Isolation and Morphological Characteristic Examination

Fresh specimens of bamboo and maize culms with fungal fruiting bodies were collected from Chiang Rai, Thailand from September–October 2020. Specimens were brought to the laboratory in plastic Ziploc bags for observation. Senanayake et al. [27] were followed for the morphological observations and single-spore isolation. The morphological characteristics were examined under a stereomicroscope (Motic SMZ-171, Wetzlar, Germany). The conidiomata were observed and photographed using a Nikon ECLIPSE Ni-U compound microscope connected to a Nikon camera series DS-Ri2 (New York, United States). The germinating ascospores were transferred aseptically to fresh potato dextrose agar (PDA) media and incubated at room temperature (25 °C) for 2–4 weeks. The morphological characteristics of cultures were checked and recorded after 30–60 days.

The herbarium specimens have been deposited at the herbarium of Mae Fah Luang University (MFLU) and Kunming Institute of Botany (HKAS), while the living cultures have been deposited at Mae Fah Luang University Culture Collection (MFLUCC). The Faces of Fungi and the Index Fungorum numbers are registered as outlined in Jayasiri et al. [28], and the Index Fungorum [26].

2.2. DNA Extraction, PCR Amplification and Sequencing

The genomic DNA was extracted from living pure cultures using the Biospin Fungus Genomic DNA extraction Kit (BioFlux, P.R. China) following the manufacturer’s protocol. The internal transcribed spacer (ITS) with the primer pair of ITS4/ITS5 [29], the partial large subunit nuclear rDNA (LSU) with the primer pair of LR0R/LR5 [30], the translation elongation factor 1-alpha gene (TEF1-α) with the primers of EF1-728F/EF-2 [31,32] and the TUB2 with primers of bt2a/bt2b [33] were used to amplify the genes ITS, LSU, TEF1-α and TUB2. The polymerase chain reaction (PCR) was carried out under the following protocol: the final volume of 25 μL consisting of 2 μL of DNA template, 1 μL of each forward and reverse primers, 12.5 μL of 2× FastTaq Premix (mixture of Taq DNA polymerase, dNTPs, and a buffer) and 9.5 μL of deionized water. The PCR thermal cycle program was as follows: for ITS and LSU: initial denaturation at 95 °C for 5 min, then 35 cycles of denaturation at 94 °C for 30 s, annealing at 52 °C for 30 s and extension at 72 °C for 1 min and final extension at 72 °C for 10 min; for TEF1-α: initial denaturation at 94 °C for 5 min, then 35 cycles of denaturation at 94 °C for 1 min, annealing at 56 °C for 1 min and extension at 72 °C for 90 s and final extension at 72 °C for 10 min; for TUB2: initial denaturation at 95 °C for 5 min, then 35 cycles of denaturation at 94 °C for 45 s, annealing at 55 °C for 45 s and extension at 72 °C for 1 min and final extension at 72 °C for 10 min. The PCR products were checked in 1% agarose gels and sent to Tsing Ke Biological Technology (Kunming) Co., China for sequencing. The sequence quality was checked, and the sequences were condensed with SeqMan. The sequences derived in this study were deposited in the GenBank, and the accession numbers were obtained (Table 1).

2.3. Phylogenetic Analyses

The sequences generated in this study were subjected to a basic local alignment search tool (BLAST) search in the GenBank to identify closely related Apiospora taxa to the taxa obtained in this study. The sequences of Apiospora were also obtained from recently published data [4,18,34,35,36,37,38,39]. Consensus sequences were assembled and aligned using BioEdit and MAFFT v.7.110 online program, respectively (http://mafft.cbrc.jp/alignment/server, accessed on 12 August 2021) [40], and manually edited using BioEdit v7.2.3 [41].

The construction of the combined phylogenetic trees was completed using maximum likelihood (ML) and Bayesian inference posterior probabilities (BYPP), with Sporocadus trimorphus (CBS 114203) as the outgroup taxon. The models were selected as GTRGAMMA for maximum likelihood, while the best-fit models were selected as GTR + I + G for ITS, LSU and HKY + I + G for TUB2, and TEF1-α for the Bayesian posterior probability analysis. The maximum likelihood (ML) analysis was performed using RAxML-HPC v.8 [42,43] on the XSEDE TeraGrid of the CIPRES Science Gateway (https://www.phylo.org, accessed on 12 August 2021) [44] with a rapid bootstrap analysis, followed by 1000 bootstrap replicates. The final tree was selected amongst the suboptimal trees from each run by comparing the likelihood scores under the GTRGAMMA substitution model. The Bayesian analyses were performed by MrBayes v. 3.2 [45]. Markov chain Monte Carlo (MCMC) was run for 5,000,000 generations, and the trees were sampled every 100th generation. The first 10% of the trees that represented the burn-in phase were discarded, and only the remaining 90% of the trees were used for calculating the posterior probabilities (PP) for the majority rule consensus tree. Phylogenetic trees were visualized with FigTree v. 1.4.2 [46] and modified in Adobe Illustrator CS5 software (Adobe Systems, USA). The newly obtained sequences in this study were deposited in the GenBank.

3. Results

3.1. Phylogeny

The combined ITS, LSU, TEF1-α and TUB2 dataset comprised 138 strains, including four newly sequenced strains, with Sporocadus trimorphus (CBS 114203) as the outgroup taxon. Multi-locus sequences were concatenated, which comprised 2820 nucleotide characters, including gaps (ITS: 1–637, LSU: 638–1518, TEF1-α: 1519–1971 and TUB2: 1972–2799). The phylogenic tree from the RAxML analysis had similar topology to the Bayesian analysis. The RAxML analysis of the combined dataset yielded the best scoring tree (Figure 1) with a final ML optimization likelihood value of −27840.652840. The matrix had 1446 distinct alignment patterns, with 27.45% undetermined characters or gaps. the estimated base frequencies were as follows: A = 0.238477, C = 0.253732, G = 0.254209, T = 0.253582; substitution rates AC = 1.244445, AG = 3.021293, AT = 1.211434, CG = 1.060781, CT = 4.719948, GT = 1.000000; gamma distribution shape parameter α = 0.298987.

The phylogenetic trees generated by maximum likelihood and Bayesian show the taxonomic placements of our total strains belong to Apiospora. The strains MFLUCC 21-0051 and MFLUCC 21-0054 clustered together with members of Apiospora and grouped with Ap. rasikravindrae (NFCCL 2144 and LC 8179). The strain MFLUCC 21-0052 presented as a distinct lineage and sister to Ap. intestine (CBS 135835) with significant statistical support (ML/BI = 100/1.00). The strain MFLUCC 21-0053 clustered with Ap. intestine (CBS 135835), but in a distinct clade with high support (ML/BI = 100/1.00).

3.2. Taxon Treatment

• Apiospora chiangraiense X.G. Tian and Tibpromma S., sp. nov. (Figure 2).

Index Fungorum number: IF558492; Faces of Fungi number: FoF 09905.

Etymology: Referring to Chiang Rai Province, Thailand, where the fungus was collected.

Saprobic on dead culms of bamboo. Sexual morph: undetermined. Asexual morph: Colonies on natural substrate are dry, dark brown to black, velvety, dull, consisting of a sterile mycelial outer zone and a round, glistening, abundantly sporulating center, with conidia readily liberated when disturbed. Mycelium is superficial, branched, hyaline to dark brown, septate, smooth-walled and hyphae. Conidiophores are reduced to conidiogenous cells, grouped together to form sporodochia. Conidiogenous cells are 4–7.5 µm high × 3–4 µm diam. ($\stackrel{-}{\mathrm{x}}$ = 6 × 3.5 µm², n = 30), monoblastic or polyblastic, aggregated in clusters on hyphae, hyaline to light brown, smooth and cylindrical to subcylindrical. Conidia are aseptate, pale brown to dark brown, in the surface view 6.5–8 × 6–8 μm² ($\stackrel{-}{\mathrm{x}}$ = 7.5 × 7 μm², n = 50), in the lateral view 6–7.5 × 4–5.5 μm² ($\stackrel{-}{\mathrm{x}}$ = 7 × 5 μm², n = 50), with a central scar, globose in the surface view, a lenticular inside view, with straight germ slit spore length.

Culture characteristics: Conidia germinating on PDA within 24 h at room temperature (25 °C). On the PDA, the colonies’ surfaces are white, lightly yellow, wooly, flat, spreading, filiform, with abundant aerial mycelia and reverse off-white to yellow.

Material examined: THAILAND, Chiang Rai Province, Muang District, on dead culms of bamboo, 23 October 2020, X.G. Tian, bb-4-5, (MFLU 21-0046, holotype); ex-type culture, MFLUCC 21-0053.

Notes: In the phylogenetic analyses, Apiospora chiangraiense formed a distinct clade sister to Ap. intestini with strong bootstrap support values (ML/BI = 100/1.00). Morphologically, Ap. chiangraiense is distinct from Ap. intestine by conidiogenous cells, conidiophores and conidia. The conidiophores of Ap. intestini are usually hyaline, macronematous, mononematous and transversely septate, while Ap. chiangraiense has reduced conidiophores and conidiogenous cells grouped together to form sporodochia. Additionally, Ap. chiangraiense has larger conidia compared to Ap. intestini (surface view 6.5–8 × 6–8 μm², lateral view 6–7.5 × 4–5.5 μm versus surface view (4.5–) 5.5 (–6) μm diam, side view (2–) 4 (–6) μm diam). Based on pairwise nucleotide comparisons, Ap. chiangraiense is different from Ap. intestini (CBS 135835) in 27/583 bp (4.63/) of the ITS, 9/814 (1.1%) of the LSU and 61/696 bp (8.76%) of TUB2, but we were unable to compare TEF-α pairwise nucleotides as the amplification of TEF-α was not successful for this species. However, both the phylogenetic analyses and morphological characteristics supported our species as a distinct new species.

• Apiospora intestini (Kajale, Sonawane and Rohit Sharma) Pintos and P. Alvarado, Fungal Systematics and Evolution 7: 206 (2021) (Figure 3).

Index Fungorum number: IF 837744.

Saprobic on dead culms of bamboo. Sexual morph: undetermined. Asexual morph: Colonies are on natural substrate surface, gregarious, powdery, dark brown to black, dull with conidia readily liberated when disturbed. Conidiophores are 1.5–2 µm wide ($\stackrel{-}{\mathrm{x}}$ = 2 µm, n = 40) hyaline, macronematous, mononematous, transversely septate, thick-walled, brown. Conidiogenous cells are 6–9.5 × 1.5–2 µm² ($\stackrel{-}{\mathrm{x}}$ = 7.5 × 2 µm², n = 30), intercalary, cylindrical, hyaline. Conidia are 6.5–5 × 6–10 µm² ($\stackrel{-}{\mathrm{x}}$ = 7 × 5.5 µm², n = 50), borne as bunches on conidiophores, lateral, pale brown to brown, smooth-walled, globose to subglobose or irregularly round, aseptate, with a central scar and without germ slit.

Culture characteristics: Conidia germinating on PDA within 24 h at room temperature. The colonies’ surfaces are white, cottony, flat, spreading, filiform, mycelia not tightly attached to the surface and the reverse lightly pigmented.

Material examined: THAILAND, Chiang Rai Province, Muang District, on dead culms of bamboo, 23 October 2020, X. G. Tian bb-4-2 (MFLU 21-0045), living culture, MFLUCC 21-0052.

Notes: Apiospora intestini was introduced by Crous et al. [19] based on the morphology of asexual morph and the phylogenetic analyses. In this paper, our new isolate (MFLUCC 21-0052) clustered with the ex-type strain of Ap. intestini with relatively high support (ML/BI = 100/1.00). Morphologically, the conidia of the new isolate (MFLUCC 21-0052) are similar to the holotype Ap. intestini (CBS 135835) in having similar size of conidiophores that are borne as bunches, intercalary and terminal, brown, smooth, aseptate and globose to subglobose. Based on nucleotide comparisons, Ap. intestini (MFLUCC 21-0052) is slightly different from Ap. intestini in 12/580 bp (2.07%) of the ITS, 2/814 (0.24%) of the LSU, 2/684 bp (0.29%) of TUB2 and 2/610 bp (0.32%) of TEF1-α. Based on both phylogeny and morphology, the new isolate (MFLUCC 21-0052) is identified as Ap. intestini. This is the first report of Ap. intestini (MFLUCC 21-0052) isolated from dead culms of bamboo in Thailand, which was originally isolated from a grasshopper’s gut in India.

• Apiospora rasikravindrae (Shiv M. Singh, L.S. Yadav, P.N. Singh, Rahul Sharma and S.K. Singh) Pintos and P. Alvarado, Fungal Systematics and Evolution 7: 207 (2021) (Figure 4).

Index Fungorum number: IF 837716; Faces of Fungi number: FoF 01994.

Saprobic on dead culms of bamboo. Colonies appear as spotty patches on natural substrate surface. Conidiomata are immersed, pycnidial, scattered, globose to slightly conical, ostiolate, black, coriaceous. Conidiophores are 9–26 × 1–2.5 μm² ($\stackrel{-}{\mathrm{x}}$ = 17.5 × 2 μm², n = 15), arising mostly from swollen basal cells, micro to semi-macronematous, mononematous, unbranched, straight or flexuous, smooth and thin-walled, hyaline. Conidiogenous cells are basauxic, discrete, hyaline, smooth-walled. Conidia in surface view are 9–11 × 9–10.5 μm² ($\stackrel{-}{\mathrm{x}}$ = 10 × 10 μm², n = 50), in lateral view 10–11 × 6.5–8 μm² ($\stackrel{-}{\mathrm{x}}$ = 10.5 × 7.5 μm², n = 20), lenticular, globose to ovoid, occasionally elongated to ellipsoidal, brown to dark brown, smooth-walled, with a longitudinal, thin-walled, with a pale equatorial slit.

Material examined: THAILAND, Chiang Rai Province, Muang District, isolated as Saprobic on dead culms of bamboo, 23 October 2020, X. G. Tian, bb-4-1 (MFLU 21-0044), living culture, MFLUCC 21-0051; ibid decaying maize culms, 11 November 2020, X. G. Tian, corn-1-1 (HKAS 115764), living culture, MFLUCC 21-0054

Notes: The National Center for Biotechnology Information (NCBI) BLAST results of ITS, LSU, TUB2 and TEF1-α sequences of our new isolate (MFLUCC 21-0054) showed high similarities with Apiospora rasikravindrae (LC 8179) (100%, 100%, 98.90% and 98.97%, respectively), while the new isolate (MFLUCC 21-0051) also showed high similarities with Apiospora rasikravindrae (LC 8179) (99.83%, 100%, 99.61% and 99.51%, respectively). Our phylogenetic analyses showed that the two new isolates clustered with the ex-type strain of Ap. rasikravindrae (NFCCI 2144) and Ap. rasikravindrae (LC 8179). Morphologically, our new isolate is closely related to the holotype of Ap. rasikravindrae in having lenticular, globose to ovoid, occasionally elongated to ellipsoidal, brown to dark brown, smooth-walled, germ-slit conidia and micro-semi-macronematous, mononematous, unbranched, straight or flexuous, smooth and thin-walled and hyaline conidiophores. Hence, the two new isolates are identified as Ap. rasikravindrae.

Apiospora rasikravindrae was originally isolated from soil in Norway [47]. Apiospora rasikravindrae occurred on Capsicum, Kappaphycus alvarezii, Pinus, Platanus acerifolia, rice, Sargassum thunbergia and Triticum aestivum from Brazil, China, India, Japan, Netherlands, Svalbard and Thailand [3,48]. Dai et al. [3] describe and illustrate both sexual and asexual morphs for Ap. rasikravindrae and it was collected on the stems of bamboo. In this study, the isolate MFLUCC 21-0051 was newly collected from bamboo, while the isolate MFLUCC 21-0054 was newly recorded from maize.

3.3. New Combinations

• Apiospora acutiapica (Senan. and Cheew) X.G. Tian and Tibpromma S., comb. nov.

Index Fungorum number: IF558499.

Basionym: Arthrinium acutiapicum Senan. and Cheew, Frontiers in Microbiology 11. 2020.

Notes: Arthrinium acutiapicum was introduced by Senanayake et al. [34] and was collected on dead twigs of Bambusa bambos in China. Senanayake et al. [34] mentioned that this species is distinct from Ar. pseudorasikravindrae, which is a sister to Ar. acutiapicum, by the reduction of conidiophores to conidiogenous cells, cylindrical to ampulliform, pale brown conidiogenous cells with pointed, hyaline apex and brown to dark brown and smooth-walled conidia with a dark equatorial slit [34].

In our phylogenetic analysis based on combined LSU, ITS, TEF1-α and TUB2 sequence data, Arthrinium acutiapicum clustered with Apiospora pseudorasikravindrae (=Ar. pseudorasikravindrae) with high support (ML/BI = 95/-). Thus, we propose the transfer of Ar. acutiapicum under the new combination Ap. acutiapica, based on the morphological and phylogenetic analyses.

• Apiospora bambusicola (X. Tang, K.D. Hyde and J.C. Kang) X.G. Tian and Tibpromma S., comb. nov.

Index Fungorum number: IF558493; Faces of Fungi number: FoF 09162.

Basioym: Arthrinium bambusicola X. Tang, K.D. Hyde and J.C. Kang, Biodiversity Data Journal 8 (e58755): 11 2020.

Notes: Arthrinium bambusicola was introduced by Tang et al. [18] and was collected on dead culms of Schizostachyum brachycladum in Thailand. Tang et al. [18] mentioned that Ar. bambusicola were retrieved as a sister taxon of Ar. gutiae with high support (ML/BI = 83/0.99), but differs from Ar. gutiae in having larger conidia and irregularly rounded, guttulate to roughened conidia. Pintos and Alvarado [4] transferred Ar. gutiae to Apiospora based on the phylogenetic analyses and morphological characters.

In our phylogenetic analyses based on combined LSU, ITS, TEF1-α and TUB2 sequence data, Arthrinium bambusicola is a sister to the newly introduced species Ap. chiangraiense with high support (ML/BI = 80/0.99). Thus, we propose the transfer of Ar. bambusicola under the new combination Ap. bambusicola, based on the morphological and phylogenetic analyses.

• Apiospora biserialis (Y. Feng and Z.Y. Liu) X.G. Tian and Tibpromma S., comb. nov.

Index Fungorum number: IF558502; Faces of Fungi number: FoF 09569.

Basioym: Arthrinium biseriale Y. Feng, J.K. Liu, C.G. Lin, Y.Y. Chen, M.M. Xiang and Z.Y. Liu, Frontiers in Microbiology 12. 2021.

Notes: Arthrinium biseriale was introduced by Feng et al. [49] from dead culms of bamboo in China. The phylogenetic analysis of Feng et al. [49] showed that Ar. biseriale is closely related to Ar. gelatinosum, but they are phylogenetically distinct and can be recognized as two different species. Morphologically, Ar. biseriale has smaller stromata and the spores of Ar. biseriale are more curved than those of Ar. gelatinosum [49].

In our phylogenetic analyses based on combined LSU, ITS, TEF1-α and TUB2 sequence data, Arthrinium biseriale clustered with Apiospora gelatinosa with high support (ML/BI = 90/0.99). Thus, we propose the transfer of Ar. biseriale under the new combination Ap. biserialis, based on the morphological and phylogenetic analyses.

• Apiospora cordylines (T.Z. Chen, Yong Wang bis and K.D. Hyde) X.G. Tian and Tibpromma S., comb. nov.

Index Fungorum number: IF558494.

Basionym: Arthrinium cordylines T.Z. Chen, Yong Wang bis and K.D. Hyde, Mycotaxon 136(1): 189 2021.

Notes: Arthrinium cordylines was introduced by Chen et al. [39] from the leaves of Cordyline fruticosa in China. Chen et al. [39] mentioned that Ar. cordylinae formed a well-supported branch with type strains of Ar. aureum (CBS 244.83) and Ar. hydei (CBS 114990). Meanwhile, a base difference comparison also confirmed Ar. cordylinae is a distinct species.

In our phylogenetic analyses, Arthrinium cordylines is a sister to Ap. hydei with high support (ML/BI = 96/0.99). Thus, we propose the transfer of Ar. cordylines under the new combination Ap. cordylines.

• Apiospora cyclobalanopsidis (Y. Feng and Z.Y. Liu) X.G. Tian and Tibpromma S., comb. nov.

Index Fungorum number: IF558503; Faces of Fungi number: FoF 09572.

Basioym: Arthrinium cyclobalanopsidis Y. Feng, J.K. Liu, C.G. Lin, Y.Y. Chen, M.M. Xiang and Z.Y. Liu, Frontiers in Microbiology 12. 2021.

Notes: Arthrinium cyclobalanopsidis was introduced by Feng et al. [49] from a leaf of Cyclobalanopsidis glauca Oerst in China. Feng et al. [49] showed that Ar. cyclobalanopsidis clustered with Ar. camelliae-sinensis, but can be distinguished from Ar. camelliae-sinensis by conidiogenous cells. Pintos and Alvarado [4] transferred Ar. camelliae-sinensis to Apiospora camelliae-sinensis, based on the phylogenetic analyses and morphological characteristics.

In our phylogenetic analyses based on combined LSU, ITS, TEF1-α and TUB2 sequence data, Arthrinium cyclobalanopsidis clustered with Ap. camelliae-sinensis with high support (ML/BI = 78/1.00). Thus, we propose the transfer of Ar. cyclobalanopsidis under the new combination Ap. cyclobalanopsidis, based on the morphological and phylogenetic analyses.

• Apiospora euphorbiae (M.B. Ellis) X.G. Tian and Tibpromma S., comb. nov.

Index Fungorum number: IF558495.

Basioym: Arthrinium euphorbiae M.B. Ellis, Mycol. Pap. 103: 6 1965.

Notes: Arthrinium euphorbiae was introduced by Ellis et al. [24] from the dead stems of Euphorbia in Zambia. Tang et al. [18] showed that Ar. euphorbiae is phylogenetically closely related to Ar. malaysianum, Ar. vietnamensis, and Ar. chromolaenae [4,18].

In our phylogenetic analyses, Ar. euphorbiae is a sister to Ap. malaysiana (=Ar. malaysianum) with strong bootstrap support values (ML/PP = 94/0.99). Thus, we propose the transfer of Ar. euphorbiae under the new combination Ap. euphorbiae.

• Apiospora gelatinosa (Y. Feng and Z.Y. Liu) X.G. Tian and Tibpromma S., comb. nov.

Index Fungorum number: IF558504; Faces of Fungi number: FoF 09570.

Basioym: Arthrinium gelatinosum Y. Feng, J.K. Liu, C.G. Lin, Y.Y. Chen, M.M. Xiang and Z.Y. Liu, Frontiers in Microbiology 12. 2021.

Notes: Arthrinium gelatinosum was introduced by Feng et al. [49] from dead culms of bamboo in China. Feng et al. [49] mentioned that Ar. gelatinosum is a sister to Ar. biseriale with a well-supported lineage (ML/MP/BI = 93/98/1.00) [49].

In our phylogenetic analyses, Arthrinium gelatinosum clustered with Apiospora biserialis with high support (ML/BI = 90/0.99). Thus, we propose the transfer of Ar. gelatinosum under the new combination Ap. gelatinosa.

• Apiospora locuta-pollinis (F. Liu and L. Cai) Pintos and P. Alvarado), X.G. Tian and Tibpromma S., comb. nov.

Index Fungorum number: 834523; Faces of Fungi number: FoF05221.

Synonyms: Arthrinium pseudomarii T.Z. Chen, Yong Wang bis and K.D. Hyde, Mycotaxon 136(1): 189. 2021.

Basionym: Arthrinium locutum-pollinis F. Liu and L. Cai (as ‘locuta- pollinis’), Mycosphere 9: 1094. 2018.

Notes: Arthrinium pseudomarii was introduced by Chen et al. [39] from the leaves of Aristolochia debilis in China. Chen et al. [39] mentioned that Ar. pseudomarii differs from Ar. hispanicum, Ar. marii and Ar. mediterranei by larger, subglobose to ellipsoid conidia and showed a close relationship with three species with high bootstrap support values (ML/MP = 95/93) [39].

In our phylogenetic analyses, Ar. pseudomarii (GUCC 10228) is a sister to Ap. locuta-pollinis (=Ar. locuta-pollinis) with high support of 95% ML. Based on the nucleotide comparisons, Ar. pseudomarii is slightly different from Ap. locuta-pollinis in 10/582 bp (1.72%) of ITS, but no base pair differences were observed in TUB2 and TEF1-α. Morphologically, the conidia of Ar. pseudomarii are similar to the holotype Ap. locuta-pollinis (LC 11683) in having similar size, brown with a hyaline equatorial rim, smooth, subglobose to ellipsoid condia and hyaline to pale brown, smooth, ampulliform to doliiform conidiogenous cells aggregated into clusters on the hyphae. Thus, we identified that they are the same species, and we synonymize Ar. pseudomarii under the Ap. locuta-pollinis, based on the morphological and phylogenetic analyses.

• Apiospora minutispora (K. Das, S.Y. Lee and H.Y. Jung) X.G. Tian and Tibpromma S., comb. nov.

Index Fungorum number: IF558497.

Basionym: Arthrinium minutisporum K. Das, S.Y. Lee and H.Y. Jung, Mycobiology 48(6): 453 2020.

Notes: Arthrinium minutisporum was introduced by Das et al. [37] from mountain soil in Korea. Morphologically, Ar. minutisporum is quite similar to Ar. phragmites, Ar. aureum and Ar. Hydei. However, the conidia of Ar. minutisporum are smaller than those of Ar. phragmites, Ar. aureum and Ar. Hydei, and Ar. minutisporum produce smaller conidiogenous cells than Ar. phragmites [39]. Pintos and Alvarado [4] transferred Ar. phragmites, Ar. aureum and Ar. hydei to Apiospora phragmites, Ap. aureum and Ap. hydei, based on the phylogenetic analyses and morphological characteristics. Whereas Ar. minutisporum was maintained in Arthrinium.

In our phylogenetic analyses, Arthrinium minutisporum forms a distinct subclade and is close to Apiospora aurea, Ap. balearica and Ap. descalsii with strong bootstrap support values (ML/PP = 99/1.00) within Apiospora. Thus, we propose the transfer of Ar. minutisporum under the new combination Ap. minutispora.

• Apiospora pseudorasikravindrae (Senan. and Cheew) X.G. Tian and Tibpromma S., comb. nov.

Index Fungorum number: IF 558505.

Basionym: Arthrinium pseudorasikravindrae Senan. and Cheew, Frontiers in Microbiology 11. 2020.

Notes: Arthrinium pseudorasikravindrae was introduced by Senanayake et al. [34] from dead twigs of Bambusa bambos Voss. in China. Arthrinium pseudorasikravindrae is morphologically distinct from Ar. chinense, Ar. paraphaeospermum and Ar. rasikravindrae by its thick-walled, finely roughened conidia with a pale, equatorial slit and ampulliform, cylindrical or doliiform, basauxic conidiogenous cells [34]. Pintos and Alvarado [4] transferred Ar. chinense, Ar. paraphaeospermum and Ar. rasikravindrae to Apiospora and synonymized them under Apiospora chinense, Ap. paraphaeospermum and Ap rasikravindrae, respectively, based on the phylogenetic analyses and morphological characteristics.

Our phylogenetic analyses based on combined LSU, ITS, TEF1-α and TUB2 sequence data show Ar. pseudorasikravindrae is a sister to the new combinations Ap. acutiapica (=Ar. acutiapicum) with high support (ML/BI = 77/0.99). Thus, we propose the transfer of Ar. pseudorasikravindrae under the new combination Ap. pseudorasikravindrae.

• Apiospora septata (Y. Feng and Jian K. Liu) X.G. Tian and Tibpromma S., comb. nov.

Index Fungorum number: IF558506; Faces of Fungi number: FoF 09571.

Basioym: Arthrinium septatum Y. Feng, J.K. Liu, C.G. Lin, Y.Y. Chen, M.M. Xiang and Z.Y. Liu, Frontiers in Microbiology 12. 2021.

Notes: Arthrinium septatum was introduced by Feng et al. [49] from dead bamboo culms in China. Feng et al. [49] showed that Arthrinium septatum forms a well-supported clade and appears to be distinct from other Arthrinium species. Arthrinium septatum resembles Ar. biseriale in having a biseriate, broad fusiform to cylindrical ascospores and cylindrical, clavate asci. However, Ar. septatum differs from Ar. biseriale by having smaller stromata [49].

In our phylogenetic analyses, Arthrinium septatum groups in a well-supported clade with Ap. pseudospegazzinii and Ap. gelatinosa. Thus, we propose the transfer of Ar. septatum under the new combination Ap. septata, based on the morphological and phylogenetic analyses.

• Apiosporasetariae (Jiang, N.; Tian, C.M.) X.G. Tian and Tibpromma S., comb. nov.

Index Fungorum number: IF835609.

Basioym: Arthrinium setariae JIANG, N.; TIAN, C.M. Phytotaxa 483, 149-159. 2021.

Notes: Arthrinium setariae was introduced by Jing et al. [38] from Setaria viridis in China. Jing et al. [38] mentioned that this species has larger conidia and is phylogenetically closely related to Ar. jiangxiense. Pintos and Alvarado [4] transferred Ar. jiangxiense to Apiospora and synonymized Ap. jiangxiens based on the phylogenetic analyses and morphological characteristics.

In our phylogenetic analyses based on combined LSU, ITS, TEF1-α and TUB2 sequence data, Arthrinium setariae clustered with Apiospora jiangxiense with high support (ML/BI = 87/1.00). Thus, we propose the transfer of Ar. setariae under the new combination Ap. setariae, based on the morphological and phylogenetic analyses.

• Apiospora sorghi (J.D.P. Bezerra, C.M Gonçalves and C.M. Souza-Motta) X.G. Tian and Tibpromma S., comb. nov.

Index Fungorum number: IF558498; Faces of Fungi number: FoF 05762.

Basioym: Arthrinium sorghi J.D.P. Bezerra, C.M Gonçalves and C.M. Souza-Motta, Fungal Diversity: 10.1007, 73 2020.

Notes: Arthrinium sorghi was introduced as an endophyte by Bezerra et al. [36] from the leaves of Sorghum bicolor in Brazil. Bezerra et al. [36] mentioned that Ar. sorghi is treated as a unique lineage within Arthrinium based on ITS phylogenetic analysis. Morphologically, Ar. sorghi resembles Ar. pseudosinense, Ar. ovatum and Ar. phaeospermum, but differs from them by the culture characteristics, conidiophores and conidia size [36]. Pintos and Alvarado [4] transferred Ar. pseudosinense, Ar. ovatum and Ar. phaeospermum to Apiospora pseudosinensis, Ap. ovata and Ap. phaeospermum based on the phylogenetic analyses and morphological characteristics.

In our phylogenetic analyses based on combined LSU, ITS, TEF1-α and TUB2 sequence data, Arthrinium sorghi clustered with Apiospora bambusucila with high support (ML/BI = 78/0.99). Thus, we propose the transfer of Ar. sorghi under the new combination Ap. sorghi, based on the morphological and phylogenetic analyses.

4. Discussion

In this study, the new taxon Apiospora chiangraiense and two new host records, viz., Ap. intestini and Ap. rasikravindrae, are introduced based on the morphological and phylogenetic analyses. In addition, thirteen new combinations are proposed based on the phylogenetic analyses.

Apiospora was previously synonymized under Arthrinium, but Pintos et al. [14] re-evaluated the placements of these two genera and transferred 55 species to Apiospora based on a phylogenetic analysis. Currently, 117 species of Apiospora are listed in the Index Fungorum [33]. Among these 117 species, 55 species have been confirmed in Apiospora by phylogenetic analyses [4]; however, the remaining 62 species need to be confirmed, as the sequence data of these species are not available. The morphology of Apiospora and Arthrinium are quite similar, so it is difficult to distinguish Apiospora and Arthrinium based only on morphology.

In the phylogenetic analyses, two Arthrinium species, viz., Arthrinium trachycarpum and Ar. urticae, formed a distinct clade out of Arthrinium, and this result is consistent with previous studies [18]. However, the morphologies of these two species are not significantly different from Arthrinium; thus, more collections are required to clarify the placement of these two species [24,50]. In addition, our phylogenetic analyses showed that Apiospora sorghi, Ap. bambusucila, Ap. chiangraiense and Ap. intesini are not clustered together in Apiospora major clades (Figure 1). We also compared the LSU sequence of these four species with other Apiospora species, but a few base pair differences were found. Moreover, their morphologies fit well within the species concept of Apiospora. Thus, further phylogenetic analyses are necessary to confirm whether Apiospora is a species complex or not.

Author Contributions

Data curation, X.T.; funding acquisition, S.T.; methodology, X.T.; supervision, S.C.K., A.M. and S.T.; writing—original draft, X.T. and D.B.; Writing—review and editing, X.T., S.C.K., A.M., I.P., J.X., D.B. and S.T. All authors have read and agreed to the published version of the manuscript.

Funding

Saowaluck Tibpromma would like to thank the International Postdoctoral Exchange Fellowship Program (number Y9180822S1), CAS President’s International Fellowship Initiative (PIFI) (number 2020PC0009), China Postdoctoral Science Foundation and the Yunnan Human Resources and Social Security Department Foundation for funding her postdoctoral research. Samantha C. Karunarathna thanks CAS President’s International Fellowship Initiative (PIFI) for funding his postdoctoral research (number 2018PC0006) and the National Science Foundation of China (NSFC) for funding this research work under project code 31750110478. Itthayakorn Promputtha is grateful to Chiang Mai University for partial support of this research. Austin Smith at World Agroforestry (ICRAF), Kunming Institute of Botany, China, is thanked for English editing.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures and Table

Figure 1. The best-scoring RAxML tree constructed from a concatenated ITS, LSU, TEF1-α, and TUB2 dataset. The tree is rooted with Sporocadus trimorphus (CBS 114203). Nodes were annotated if bootstrap supported value ≥ 70% maximum likelyhood bootstrap proportion (ML, left) or ≥0.95 Bayesian posterior probability (PP, right). The newly described species are in red and new combination species are in blue.

Figure 1. The best-scoring RAxML tree constructed from a concatenated ITS, LSU, TEF1-α, and TUB2 dataset. The tree is rooted with Sporocadus trimorphus (CBS 114203). Nodes were annotated if bootstrap supported value ≥ 70% maximum likelyhood bootstrap proportion (ML, left) or ≥0.95 Bayesian posterior probability (PP, right). The newly described species are in red and new combination species are in blue.

Figure 2. Apiospora chiangraiense (MFLU 21-0046, holotype). (a–c) Appearance of the fungus on dead culms of bamboo. (d–i) Conidia with conidiophores. (j–l) Conidiogenous cells bearing conidia. (n,o,q) Conidia. (p) Conidia with germ-slit. (m) Germinated conidium. (r,s) Colonies on PDA media (r forward, s reversed). Scale bars: a = 4000 μm, b = 1000 μm, c = 200 μm and d–q = 10 µm.

Figure 3. Apiospora intestini (MFLU 21-0045). (a–c) Appearance of the fungus on dead culms of bamboo. (d–g) Conidia with conidiophores. (h–j,l,m) Conidiogenous cells bearing conidia. (n–s) Conidia. (k) Germinated conidium. (t,u) Colonies on PDA media (t forward, u reversed). Scale bars: a = 4000 μm, b = 1000 μm, c = 200 μm, d–g = 20 µm, h–m = 10 μm and n–s = 5 μm.

Figure 4. Apiospora rasikravindrae (MFLU 21-0045). (a–c) Appearance of the fungus on dead culms of bamboo. (d–i) Conidia with conidiophores. (j,k,t,u) Conidiogenous cells bearing conidia. (l,m) Conidia with germ-slit. (p–r) Conidia. (n) Germinated conidium. (o,s) Colonies on PDA media (o forward, s reversed). Scale bars: a = 4000 μm, b = 2000 μm, c = 200 μm and d–s = 10 μm.

Table 1

Taxa names, strain numbers, host, countries and corresponding GenBank accession numbers of the taxa used in the phylogenetic analyses of this study.

Taxa Names	Strain Numbers	Substrates	Countries	GenBank Accession Numbers
				ITS	LSU	TUB2	TEF 1-α
Apiospora acutiapica	KUMCC 20-0210	Bambusa bambos	China	MT946343	MT946339	MT947366	MT947360
Apiospora aquaticum	S-642	Submerged wood	China	MK828608	MK835806	-	-
Apiospora arundinis	CBS 133509	Aspergillus flavus sclerotium Buried in sandy field	USA	KF144886	KF144930	KF144976	KF145018
Apiospora arundinis	CBS 449.92	Bamboo	Canada	KF144887	KF144931	KF144977	KF145019
Apiospora aurea	CBS 244.83	-	Japan	AB220251	KF144935	KF144981	KF145023
Apiospora balearica	CBS 145129	Undetermined poaceae	Spain	MK014869	MK014836	MK017975	MK017946
Apiospora bambusae	ICPM 6889	Bamboo	New Zealand	MK014874	MK014841	MK017980	MK017951
Apiospora bambusae	CBS 145133	Phyllostachys aurea	Spain	MK014875	MK014842	MK017981	MK017952
Apiospora bambusicola	MFLUCC20-0144	Schizostachyum brachycladum	Thailand	MW173030	MW173087	-	MW183262
Apiospora biserialis	CGMCC 3.20135	Bamboo	China	MW481708	MW478885	MW522955	MW522938
Apiospora biserialis	GZCC 20_0099	Bamboo	China	MW481709	MW478886	MW522956	MW522939
Apiospora biserialis	GZCC 20_0100	Bamboo	China	MW481710	MW478887	MW522957	MW522940
Apiospora camelliae-sinensis	LC 5007	Camellia sinensis	China	KY494704	KY494780	KY705173	KY705103
Apiospora camelliae-sinensis	LC 8181	Brassica rapa	China	KY494761	KY494837	KY705229	KY705157
Apiospora chromolaenae	MFLUCC17-1505	Chromolaena odorata	Thailand	MT214342	MT214436	-	MT235802
Apiospora chiangraiense ▲	MFLUCC21-0053	Dead culms of bamboo	Thailand	MZ542520	MZ542524	MZ546409	-
Apiospora cordylinae	GUCC 10026	Cordyline fruticosa	China	MT040105	-	MT040147	MT040126
Apiospora cyclobalanopsidis	CGMCC 3.20136	Cyclobalanopsidis glauca	China	MW481713	MW478892	MW522962	MW522945
Apiospora cyclobalanopsidis	GZCC 20_0103	Cyclobalanopsidis glauca	China	MW481714	MW478893	MW522963	MW522946
Apiospora descalsii	CBS 145130	Ampelodesmos mauritanicus	Spain	MK014870	MK014837	MK017976	MK017947
Apiospora dichotomanthi	LC 4950	Dichotomanthes tristaniicarpa	China	KY494697	KY494773	KY705167	KY705096
Apiospora dichotomanthi	LC 8175	Dichotomanthes tristaniicarpa	China	KY494755	KY494831	KY705223	KY705151
Apiospora esporlensis	CBS 145136	Phyllostachys aurea	Spain	MK014878	MK014845	MK017983	MK017954
Apiospora euphorbiae	IMI 285638b	Bambusa sp.	Bangladesh	AB220241	AB220335	AB220288	-
Apiospora gaoyouensis	CFCC 52301	Phragmites australis	China	MH197124	-	MH236789	MH236793
Apiospora gaoyouensis	CFCC 52302	Phragmites australis	China	MH197125	-	MH236790	MH236794
Apiospora garethjonesii	KUMCC 16-0202	Dead culms of bamboo	China	KY356086	KY356091	-	-
Apiospora gelatinosa	KHAS 11962	Bamboo	China	MW481706	MW478888	MW522958	MW522941
Apiospora gelatinosa	GZAAS 20-0107	Bamboo	China	MW481707	MW478889	MW522959	MW522942
Apiospora guizhouensis	LC 5318	Air in karst cave	China	KY494708	KY494784	KY705177	KY705107
Apiospora guizhouensis	LC 5322	Air in karst cave	China	KY494709	KY494785	KY705178	KY705108
Apiospora hispanica	IMI 326877	Beach sand	Spain	AB220242	AB220336	AB220289	-
Apiospora hydei	CBS 114990	Bambusa tuldoides	China	KF144890	KF144936	KF144982	KF145024
Apiospora hydei	KUMCC 16-0204	Dead culms of bamboo	China	KY356087	KY356092	-	-
Apiospora hyphopodii	MFLUCC15-0003	Bambusa tuldoides	China	KR069110	-	-	-
Apiospora hyphopodii	KUMCC 16-0201	Culms of bamboo	China	KY356088	KY356093	-	-
Apiospora iberica	CBS 145137	Arundo donax	Portugal	MK014879	MK014846	MK017984	MK017955
Apiospora intestini	CBS 135835	Gut of a grasshopper	India	KR011352	MH877577	KR011350	KR011351
Apiospora intestini ▲	MFLUCC 21-0052	Dead culms of bamboo	Thailand	MZ542521	MZ542525	MZ546410	MZ546406
Apiospora italica	CBS 145138	Arundo donax	Italy	MK014880	MK014847	MK017985	MK017956
Apiospora italica	CBS 145139	Phragmites australis	Spain	MK014881	MK014848	MK017986	-
Apiospora jatrophae	AMH-9557	Jatropha podagrica	India	JQ246355	-	-	-
Apiospora jatrophae	AMH-9556	Jatropha podagrica	India	HE981191	-	-	-
Apiospora jiangxiensis	LC 4494	Phyllostachys sp.	China	KY494690	KY494766	KY705160	KY705089
Apiospora jiangxiensis	LC 4577	Maesa sp.	China	KY494693	KY494769	KY705163	KY705092
Apiospora kogelbergensis	CBS 113332	Cannomois virgata	South Africa	KF144891	KF144937	KF144983	KF145025
Apiospora kogelbergensis	CBS 113333	Dead culms of Restionaceae	South Africa	KF144892	KF144938	KF144984	KF145026
Apiospora locuta -pollinis	LC 11688	Bee bread	China	MF939596	-	MF939623	MF939618
Apiospora locuta -pollinis	LC 11683	Brassica campestris	China	MF939595	-	MF939622	MF939616
Apiospora longistroma	MFLUCC 11-0479	Dead culms of bamboo	Thailand	KU940142	KU863130	-	-
Apiospora longistroma	MFLUCC11-0481	Dead culms of bamboo	Thailand	KU940141	KU863129	-	-
Apiospora malaysiana	CBS 102053	Macaranga hullettii	Malaysia	KF144896	KF144942	KF144988	KF145030
Apiospora marii	CBS 497.90	Beach sands	Spain	AB220252	KF144947	KF144993	KF145035
Apiospora marii	DiSSPA_A1	Oleaeuropaea	Italy	MK602320	-	MK614695	MK645472
Apiospora mediterranea	IMI 326875	Air	Spain	AB220243	AB220337	AB220290	-
Apiospora minutispora	1.70E-41	Mountain soil	Korea	LC517882	-	LC518888	LC518889
Apiospora mytilomorpha	DAOM 214595	Andropogon sp.	India	KY494685	-	-	-
Apiospora neobambusae	LC 7106	Leaves of bamboo	China	KY494718	KY494794	KY705186	KY806204
Apiospora neobambusae	LC 7124	Leaves of bamboo	China	KY494727	KY494803	KY705195	KY806206
Apiospora neochinensis	CFCC 53036	Fargesia qinlingensis	China	MK819291	-	MK818547	MK818545
Apiospora neochinensis	CFCC 53037	Fargesia qinlingensis	China	MK819292	-	MK818548	MK818546
Apiospora neogarethjonesii	DQD 2019a	Bamboo	China	MK070897	MK070898	-	-
Apiospora neosubglobosa	JHB 006	Bamboo	China	KY356089	KY356094	-	-
Apiospora neosubglobosa	KUMCC 16-0203	Bamboo	China	KY356090	KY356095	-	-
Apiospora obovata	LC 4940	Lithocarpus sp.	China	KY494696	KY494772	KY705166	KY705095
Apiospora obovata	LC 8177	Lithocarpus sp.	China	KY494757	KY494833	KY705225	KY705153
Apiospora ovata	CBS 115042	Arundinaria hindsii	China	KF144903	KF144950	KF144995	KF145037
Apiospora paraphaeosperma	MFLUCC13-0644	Dead culms of bamboo	Thailand	KX822128	KX822124	-	-
Apiospora phragmitis	CPC 18900	Phragmites australis	Italy	KF144909	KF144956	KF145001	KF145043
Apiospora phyllostachydis	MFLUCC18-1101	Phyllostachys heteroclada	China	MK351842	MH368077	MK291949	MK340918
Apiospora piptatheri	CBS 145149	Piptatherum miliaceum	Spain	MK014893	MK014860	-	MK017969
Apiospora pseudomarii	GUCC 10228	Aristolochia debilis	China	MT040124	-	MT040166	MT040145
Apiospora pseudoparenchymatica	LC 7234	Leaves of bamboo	China	KY494743	KY494819	KY705211	KY705139
Apiospora pseudoparenchymatica	LC 8173	Leaves of bamboo	China	KY494753	KY494829	KY705221	KY705149
Apiospora pseudorasikravindrae	KUMCC 20-0208	Bambusa dolichoclada	China	MT946344	-	MT947367	MT947361
Apiospora pseudosinensis	CPC 21546	Leaves of bamboo	Netherlands	KF144910	KF144957	-	KF145044
Apiospora pseudospegazzinii	CBS 102052	Macaranga hullettii	Malaysia	KF144911	KF144958	KF145002	KF145045
Apiospora pterosperma	CBS 123185	Machaerina sinclairii	New Zealand	KF144912	KF144959	KF145003	-
Apiospora pterosperma	CPC 20193	Lepidosperma gladiatum	Australia	KF144913	KF144960	KF145004	KF145046
Apiospora qinlingensis	CFCC 52303	Fargesiaqinlingensis	China	MH197120	-	MH236791	MH236795
Apiospora qinlingensis	CFCC 52304	Fargesia qinlingensis	China	MH197121	-	MH236792	MH236796
Apiospora rasikravindrae	LC 8179	Brassica rapa	China	KY494759	KY494835	KY705227	KY705155
Apiospora rasikravindrae	NFCCI 2144	Soil	Norway	JF326454	-	-	-
Apiospora rasikravindrae ▲	MFLUCC 21-0051	Dead culms of bamboo	Thailand	MZ542523	MZ542527	MZ546412	MZ546408
Apiospora rasikravindrae ▲	MFLUCC 21-0054	Dead culms of Maize	Thailand	MZ542522	MZ542526	MZ546411	MZ546407
Apiospora sacchari	CBS 372.67	Air	-	KF144918	KF144964	KF145007	KF145049
Apiospora sacchari	CBS 664.74	Soil under Calluna vulgaris	Netherlands	KF144919	KF144965	KF145008	KF145050
Apiospora saccharicola	CBS 191.73	Air	Netherlands	KF144920	KF144966	KF145009	KF145051
Apiospora saccharicola	CBS 831.71	-	Netherlands	KF144922	KF144969	KF145012	KF145054
Apiospora septata	CGMCC 3.20134	bamboo	China	MW481711	MW478890	MW522960	MW522943
Apiospora septata	GZCC 20_0109	bamboo	China	MW481712	MW478891	MW522961	MW522944
Apiospora serenensis	IMI 326869	Food, pharmaceutical excipients, atmosphere and home dust	Spain	AB220250	AB220344	AB220297	-
Apiospora setariae	MT492005	Setaria viridis	China	MT492005	-	MT497467	MW118457
Apiospora setostroma	KUMCC 19-0217	Dead branches of bamboo	China	MN528012	MN528011	-	MN527357
Apiospora sorghi	URM 93000	Sorghum bicolor	Brazil	MK371706	-	MK348526	-
Apiospora subglobosa	MFLUCC11-0397	Dead culms of bamboo	Thailand	KR069112	KR069113	-	-
Apiospora subrosea	LC 7291	Leaves of bamboo	China	KY494751	KY494827	KY705219	KY705147
Apiospora subrosea	LC 7292	Leaves of bamboo	China	KY494752	KY494828	KY705220	KY705148
Apiospora thailandica	MFLUCC 15-0199	Dead culms of bamboo	Thailand	KU940146	KU863134	-	-
Apiospora thailandica	MFLUCC15-0202	Dead culms of bamboo	Thailand	KU940145	KU863133	-	-
Apiospora vietnamensis	IMI 99670	Citrus sinensis	Vietnam	KX986096	KX986111	KY019466	-
Apiospora xenocordella	CBS 478.86	Soil from roadway	Zimbabwe	KF144925	KF144970	KF145013	KF145055
Apiospora xenocordella	CBS 595.66	Soil	Austria	KF144926	KF144971	-	-
Apiospora yunnana	DDQ 00281	Phyllostachys nigra	China	KU940148	KU863136	-	-
Apiospora yunnana	MFLUCC15-1002	Phyllostachys nigra	China	KU940147	KU863135	-	-
Arthrinium austriacum	GZU 345004	Carex pendula	Austria	MW208928	-	-	-
Arthrinium austriacum	GZU 345006	Carex pendula	Austria	MW208929	MW208860	-	-
Arthrinium cf. sporophleoides	GZU 345102	Carex firma	Austria	MW208944	MW208866	-	-
Arthrinium caricicola	CBS 145127	Carex ericetorum	China	MK014871	MK014838	MK017977	MK017948
Arthrinium crenatum	AG 19066	Poaceae, Carex	France	MW208931	MW208861	-	-
Arthrinium curvatum	AP 25418	Leaves of Carex sp.	China	MK014872	MK014839	MK017978	MK017949
Arthrinium japonicum	IFO 30500	-	Japan	AB220262	AB220356	AB220309	-
Arthrinium japonicum	IFO 31098	Leaves of Carex despalata	Japan	AB220264	AB220358	AB220311	-
Arthrinium luzulae	AP7619-3	Luzula sylvatica	Spain	MW208937	MW208863	-	-
Arthrinium morthieri	GZU 345043	Cyperaceae carex	Austria	MW208938	MW208864	-	-
Arthrinium phaeospermum	CBS 114317	Leaves of Hordeum vulgare	Iran	KF144906	KF144953	KF144998	KF145040
Arthrinium phaeospermum	CBS 114318	Leaves of Hordeum vulgare	Iran	KF144907	KF144954	KF144999	KF145041
Arthrinium puccinioides	CBS 549.86	Lepidosperma gladiatum	Germany	AB220253	AB220347	AB220300	-
Arthrinium sphaerospermum	AP25619/CBS 146355	Poaceae	Norway	MW208943	MW208865	-	-
Arthrinium sporophleum	CBS 145154	Dead leaves of Juncus sp.	Spain	MK014898	MK014865	MK018001	MK017973
Arthrinium trachycarpum	CFCC 53038	Trachycarpus fortune	China	MK301098	-	MK303394	MK303396
Arthrinium urticae	IMI 326344	-	-	AB220245	AB220339	AB220292	-
Arthrinium trachycarpum	CFCC 53039	Trachycarpus fortune	China	MK301099	-	MK303395	MK303397
Nigrospora aurantiaca	CGMCC 3.18130	Nelumbo sp.	China	KX986064	KX986098	KY019465	KY019295
Nigrospora camelliae -sinensis	CGMCC 3.18125	Camellia sinensis	China	KX985986	KX986103	KY019460	KY019293
Nigrospora chinensis	CGMCC 3.18127	Machilus breviflora	China	KX986023	KX986107	KY019462	KY019422
Nigrospora gorlenkoana	CBS 480.73	Vitis vinifera	Kazakhstan	KX986048	KX986109	KY019456	KY019420
Nigrospora guilinensis	CGMCC 3.18124	Camellia sinensis	China	KX985983	KX986113	KY019459	KY019292
Nigrospora hainanensis	CGMCC 3.18129	Musa paradisiaca	China	KX986091	KX986112	KY019464	KY019415
Nigrospora lacticolonia	CGMCC 3.18123	Camellia sinensis	China	KX985978	KX986105	KY019458	KY019291
Nigrospora musae	CBS 319.34	Musa sp.	Australia	MH855545	KX986110	KY019455	KY019419
Nigrospora oryzae	LC2693	Neolitsea sp.	China	KX985944	KX986101	KY019471	KY019299
Nigrospora osmanthi	CGMCC 3.18126	Hedera nepalensis	China	KX986010	KX986106	KY019461	KY019421
Nigrospora pyriformis	CGMCC 3.18122	Citrus sinensis	China	KX985940	KX986100	KY019457	KY019290
Nigrospora rubi	LC2698	Rubus sp.	China	KX985948	KX986102	KY019475	KY019302
Nigrospora sphaerica	LC7298	Nelumbo sp.	China	KX985937	KX986097	KY019606	KY019401
Nigrospora vesicularis	CGMCC 3.18128	Musa paradisiaca	China	KX986088	KX986099	KY019463	KY019294
Sporocadus trimorphus	CBS 114203	Rosa canina	Sweden	MH553977	MH554196	MH554636	MH554395

Notes: Newly generated sequences are indicated by ▲ after the species name. Ex-type strains are in bold. - = information not available. Abbreviations: AMH: Ajrekar Mycological Herbarium, Pune, Maharashtra, India; CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, Netherlands; CFCC: China Forestry Culture Collection Center, Beijing, China; CPC: Culture collection of Pedro Crous, housed at the Westerdijk Fungal Biodiversity Institute; DAOM: Canadian Collection of Fungal Cultures, Ottawa, Canada; DDQ: D.Q. Dai; GUCC: Guizhou University Culture Collection, Guizhou, China; ICMP: International Collection of Microorganisms from Plants, New Zealand; IFO: Institute for Fermentation, Osaka, Japan; IMI: Culture collection of CABI Europe UK Centre, Egham, UK; JHB: H.B. Jiang; KUMCC: Culture collection of Kunming Institute of Botany, Yunnan, China; LC: Personal culture collection of Lei Cai, housed in the Institute of Microbiology, Chinese Academy of Sciences, China; MFLUCC: Mae Fah Luang University Culture Collection, Chiang Rai, Thailand; NFCCI: National Fungal Culture Collection of India.

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