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Phialolunulospora vermispora (Chaetosphaeriaceae, Sordariomycetes), a novel asexual genus and species from freshwater in southern China
expand article infoHua Zheng, Yake Wan, Jie Li, Rafael F. Castañeda-Ruiz§, Zefen Yu
‡ Yunnan University, Kunming, China
§ Instituto de Investigaciones Fundamentales en Agricultura Tropical “Alejandro de Humboldt”, La Habana, Cuba
Open Access

Abstract

The asexual taxon Phialolunulospora vermispora gen. et sp. nov., collected from submerged dicotyledonous leaves in Hainan, China, is described and illustrated herein. Phialolunulospora gen. nov. is characterized by macronematous, semimacronematous, septate and pigmented conidiophores and acrogenous, long lunate, vermiform to sigmoid, hyaline conidia with an eccentric basal appendage. Complete sequences of internal transcribed spacer (ITS) and partial sequences of nuclear large subunits ribosomal DNA (LSU) genes are provided. Phylogenetic analyses of combined ITS and LSU sequences revealed its placement in the Chaetosphaeriaceae. The new fungus is compared with morphologically similar genera.

Keywords

Biodiversity, Chaetosphaeriales, phylogeny, taxonomy

Introduction

China is considered an important Asian reservoir of biodiversity. The southern area of China ranks 34th in biodiversity hotspots (Myers et al. 2000; Williams et al. 2001). Hainan Island, located in the south of China, harbors an incredibly high diversity of fungi. Its humid, subtropical climate, with an average annual temperature of 22 to 27 °C and an average annual precipitation of 1000–2600 mm, favors development of fungi. Our group has conducted investigations of freshwater fungi to increase knowledge of this important ecological group in China (Qiao et al. 2017a, b, 2018a, b, 2019a, b, 2020).

During our present investigation of freshwater fungi in Hainan Island, South China, an interesting species was collected on dead leaves of an unidentified dicotyledonous tree. This species is characterized by unbranched and septate conidiophores, phialidic conidiogenous cells and vermiform to sigmoid and aseptate conidia with an eccentric basal appendage. Based on preliminary analysis of morphological data, we place this unknown fungus in Chaetosphaeriaceae, but a literature search found that it did not belong to any known genus. To further confirm the position of the species, phylogenetic analyses with related taxa within Chaetosphaeriaceae were carried out based on complete sequences of internal transcribed spacer (ITS) and partial sequences of nuclear large subunits ribosomal DNA (LSU) genes.

Materials and methods

Isolation and morphological study

Submerged dicotyledonous leaves were collected from Limu Mountain Nature Reserve in Hainan Province. Samples were preserved in zip-lock plastic bags, labelled, and transported to the laboratory. The decomposed leaves were cut into several 2–4 × 2–4 cm sized fragments and then spread on to the surface of corn meal agar (CMA, 20 g cornmeal, 18 g agar, 40 mg streptomycin, 30 mg ampicillin, 1000 ml distilled water) medium for 10 days; single conidium was isolated with a sterilized needle and transferred to CMA plates while viewing with an Olympus BX51 microscope. The pure strain was further transferred to potato dextrose agar (PDA, 200 g potato, 20 g dextrose, 18 g agar, 40 mg streptomycin, 30 mg ampicillin, 1000 ml distilled water) medium. Colony morphology and microscopic characteristics were examined, and photographs were taken with an Olympus BX51 microscope connected to a DP controller digital camera. Measurement data were based on 30 random conidia and 10 conidiophores.

Pure cultures were deposited in the Herbarium of the Laboratory for Conservation and Utilization of Bio resources, Yunnan University, Kunming, Yunnan, China (YMF, formerly Key Laboratory of Industrial Microbiology and Fermentation Technology of Yunnan) and at the China General Microbiological Culture Collection Center (CGMCC).

DNA extraction, PCR amplification, and sequencing

Pure cultures were grown on PDA medium for 5 days at 25 °C. Actively growing mycelium was scraped off from the surface of the culture and transferred to 2 ml Eppendorf micro-centrifuge tubes. Total genomic DNA was extracted according to the procedures in Turner et al. (1997). Primers used for PCR amplification and sequencing of the nuclear large subunits ribosomal DNA (LSU) and the internal transcribed spacer (ITS) were LROR-LR7 and ITS1-ITS4, respectively (Vilgalys and Hester 1990; White et al. 1990). PCR products were purified and stored at -20 °C until sequencing. The same pairs of primers were used to obtain sequences, which was performed by Macrogen Europe (Macrogen Inc. Amsterdam, The Netherlands). Finally, the sequences were assembled and edited using SeqMan v. 7.0.0 (DNAStar Lasergene, Madison, WI, USA) to obtain the consensus sequences. The newly obtained sequences were submitted to GenBank nucleotide database (Table 1).

Table 1.

List of strains analyzed in this study, with GenBank accession numbers.

Species Strain ITS LSU
Adautomilanezia caesalpiniae LAMIC 010212 NR_153560 NG_058594
Anacacumisporium appendiculatum HMAS 245593T KT001555 KT001553
Anacacumisporium appendiculatum HMAS 245602 KT001556 KT001554
Bahusutrabeeja dwaya CBS 261.77T MH861059 MH872829
Brunneodinemasporium brasiliense CBS 112007T JQ889272 JQ889288
Brunneodinemasporium jonesii GZCC 16–0050T KY026058 KY026055
Cacumisporium capitulatum FMR 11339 HF677176 HF677190
Cacumisporium capitulatum SMH 3766 AY017374
Calvolachnella guaviyunis CBS 134695 NR_153892 NG_058879
Chaetosphaeria ciliata CBS 122131T MH863180 MH874726
Chaetosphaeria ciliata ICMP 18253 GU180637
Chloridium chloroconium FMR 11940 KY853435 KY853495
Chloridium sp. HGUP 1806 MK372070 MK372068
Codinaea lambertiae CBS 143419T NR_156389 NG_059053
Codinaea pini CBS 138866T NR_137943 NG_058902
Conicomyces pseudotransvaalensis HHUF 29956T NR_138015 LC001708
Cryptophiale hamulata MFLUCC 180098 MG386756
Cryptophiale udagawae MFLUCC 180422 MH758198 MH758211
Cryptophialoidea fasciculata MFLUCC 172119 MH758195 MH758208
Dendrophoma cytisporoides CBS 223.95T JQ889273 JQ889289
Dictyochaeta ellipsoidea MFLUCC 181574T MK828628 MK835828
Dictyochaeta lignicola DLUCC 0899T MK828630 MK835830
Dictyochaeta assamica CBS 242.66 MH858788 MH870426
Dictyochaetopsis gonytrichoides CBS 593.93 AF178556 AF178556
Dinemasporium morbidum CBS 129.66T JQ889280 JQ889296
Dinemasporium polygonum CBS 516.95T NR_137786 NG_059109
Echinosphaeria canescens SMH 4791 AY436403
Eucalyptostroma eucalypti CBS 142074T NR_154027 NG_059257
Eucalyptostroma eucalyptorum CPC 31800T NR_159834 MH327838
Exserticlava vasiformis TAMA 450 AB753846
Gelasinospora tetrasperma CBS 178.33 NR_077163 DQ470980
Helminthosphaeria clavariarum SMH 4609T AY346283
Infundibulomyces cupulata BCC 11929T EF113976 EF113979
Infundibulomyces oblongisporus BCC 13400T EF113977 EF113980
Kionochaeta castaneae GZCC 18–0025T MN104610 MN104621
Kionochaeta microspora GZCC 18–0036T MN104607 MN104618
Lasiosphaeria ovina SMH 4605 AY587923 AY436413
Lecythothecium duriligni CBS 101317 AF261071
Leptosporella arengae MFLUCC 150330T MG272255 MG272246
Leptosporella gregaria SMH 4290T AY346290
Linocarpon arengae MFLUCC 150331T MG272247
Linocarpon cocois MFLUCC 150812T MG272257 MG272248
Menispora glauca FMR 12089 HF678528 HF678538
Menispora tortuosa DAOM 231154 KT225527 AY544682
Menispora tortuosa CBS 214.56 AF178558 AF178558
Menisporopsis breviseta GZCC 18–0071T MN104612 MN104623
Menisporopsis dushanensis GZCC 18–0084T MN104615 MN104626
Morrisiella indica HKUCC 10827 DQ408578
Multiguttulispora sympodialis MFLUCC 180153T MN104606 MN104617
Nawawia filiformis MFLUCC 160853 MH758206
Nawawia filiformis MFLUCC 172394 MH758196 MH758209
Neonawawia malaysiana CBS 125544T GU229886 GU229887
Paliphora intermedia CBS 896.97T NR_160203 NG_057766
Paliphora intermedia CBS 199.95 EF204500
Phaeostalagmus cyclosporus CBS 663.70 MH859892 MH871680
Phaeostalagmus cyclosporus CBS 312.75 MH872661
Phialolunulospora vermispora YMF 1.04260T MK165444 MK165442
Phialosporostilbe scutiformis MFLUCC 170227T MH758194 MH758207
Phialosporostilbe scutiformis MFLUCC 181288 MH758199 MH758212
Pseudodinemasporium fabiforme MAFF 244361T AB934068 AB934044
Pseudolachnea fraxini CBS 113701T JQ889287 JQ889301
Pseudolachnea hispidula MAFF 244364 AB934071 AB934047
Pseudolachnella longiciliata HHUF 29962 AB934081 AB934057
Pseudolachnella yakushimensis HHUF 29683T AB934087 AB934063
Pseudolachnella pachyderma HHUF 29955 AB934085 AB934061
Pyrigemmula aurantiaca CBS 126743T HM241692 HM241692
Pyrigemmula aurantiaca CBS 126744 HM241693 HM241693
Rattania setulifera GUFCC 15501 GU191794 HM171322
Ruzenia spermoides SMH 4606 AY436422
Sordaria fimicola CBS 508.50 MH856730 MH868251
Sporoschisma hemipsilum SMH 2125 AF466083
Sporoschisma hemipsilum SMH 3251 AF466084
Stanjehughesia vermiculata HKUCC 10840 DQ408570
Striatosphaeria codinaeaphora MR 1230 AF178546 AF178546
Striatosphaeria codinaeaphora SMH 1524 AF466088
Synaptospora plumbea SMH 3962 KF765621
Tainosphaeria jonesii GZCC 16–0053 KY026059 KY026056
Tainosphaeria jonesii GZCC 16–0065 KY026060 KY026057
Tainosphaeria monophialidica MFLUCC 180146T MN104616
Thozetella pandanicola MFLUCC 160253T MH388366 MH376740
Thozetella tocklaiensis CBS 378.58T MH857817 MH869349
Verhulstia trisororum CBS 143234T MG022181 MG022160
Zanclospora iberica CBS 130426T KY853480 KY853544
Zanclospora iberica FMR 12186 KY853481 KY853545

Sequence alignment and phylogenetic analysis

Preliminary BLAST searches with the ITS and LSU sequences of our strain against the GenBank nucleotide database determined the closely related species (Altschul et al. 1990). BLAST search showed that our strain has homology to species in Chaetosphaeriaceae. Based on this information, related sequences of the two marker loci, which include 72 representatives belonging to Chaetosphaeriaceae, 4 representatives of Helminthosphaeriaceae, 2 representatives of Linocarpaceae and 2 representatives of Leptosporellaceae, were downloaded according to recent studies (Yang et al. 2016, 2018; Wei et al. 2018; Lin et al. 2019). Sordaria fimicola (Roberge ex Desm.) Ces. & De Not, Gelasinospora tetrasperma Dowding and Lasiosphaeria ovina (Pers.) Ces. & De Not were used as the outgroup. These, together with the newly generated sequences, were aligned with ClustalX 1.83 (Thompson et al. 1997) with default parameters, and the consensus sequences were manually adjusted and linked through BioEdit v.7.0 (Hall 1999). Manual gap adjustments were done to improve the alignment and ambiguously aligned regions were excluded. Then, the combined alignment was converted to a NEXUS file using the program MEGA6 (Tamura et al. 2013) and a PHY files using the program ClustalX 1.83. The resulting combined sequence matrix included 1475 nucleotide positions (with alignment gaps) from two regions (607 from ITS, 868 from LSU). GenBank accession numbers of downloaded sequences are given in Table 1.

Maximum-likelihood (ML) analysis was computed with RAxML (Stamatakis 2006) with the PHY files generated with CLUSTAL_X version 1.83, using the GTR-GAMMA model. ML bootstrap proportions (MLBPs) were computed with 1000 replicates. Bayesian inference (BI) analysis was conducted with MrBayes version 3.2.2 (Ronquist and Huelsenbeck 2003). The Akaike information criterion (AIC) implemented in jModelTest version 2.0 was used to select the best fit models after likelihood score calculations were done (Posada 2008). The base tree for likelihood calculations was ML-optimized. HKY+I+G was estimated as the best-fit model under the output strategy of the AIC. Metropolis-coupled Markov chain Monte Carlo (MCMCMC) searches were run for 5 000 000 generations, sampling every 500th generation. Two independent analyses with four chains each (one cold and three heated) were run until the average standard deviation of the split frequencies dropped below

0.01. The initial 25% of the generations of MCMC sampling were discarded as burn-in. The refinement of the phylogenetic tree was used for estimating BI posterior probability (BIPP) values. The tree was viewed in FigTree version 1.4 (Rambaut 2012).

Results

Phylogenetic analyses

The combined dataset comprised 71 taxa (including our strain) representing 52 genera, which include 60 species in the family Chaetosphaeriaceae, 4 species in Helminthosphaeriaceae, 2 species in Linocarpaceae and 2 species in Leptosporellaceae, with Gelasinospora tetrasperma CBS 178.33, Sordaria fimicola CBS 508.50 and Lasiosphaeria ovina SMH 4605 as the outgroup. The final alignment comprised a total of 1475 base pairs, containing the ITS and LSU sequences, and were analyzed by BI and ML method. The topology of the tree is shown in Fig. 1, with the Bayesian posterior probabilities above 95% and ML bootstrap support greater than 70% indicated for respective clades. In this tree, our strain occurred on an isolated clade within Chaetosphaeriaceae, and clustered together with Dictyochaetopsis Aramb. & Cabello, Bahusutrabeeja Subram. & Bhat and Dictyochaeta Speg. with good Bayesian posterior probabilities (100%) and ML bootstrap proportions (100%). Considering distinct morphological characters with these three genera, we propose to describe our unknown isolate as a new genus and species, Phialolunulospora vermispora.

Figure 1. 

Phylogenetic tree derived from Bayesian analysis based on ITS and LSU sequences, depicting the relationships of the new taxon Phialolunulospora vermispora with closely related taxa. The numbers above branches represent BIPP (left) and MLBPs (right). BIPP over 95% and MLBPs greater than 70% are shown on the respective branches, and the bar represents the substitutions per nucleotide position. Gelasinospora tetrasperma CBS 178.33, Sordaria fimicola CBS 508.50 and Lasiosphaeria ovina SMH 4605 were used as outgroup.

Taxonomy

Phialolunulospora Z. F. Yu & R. F. Castaneda, gen. nov.

MycoBank No: 828716

Type species

Phialolunulospora vermispora Z. F, Yu & R. F. Castañeda

Etymology

Phialo-Prefix, Phia. lis N.L fem. S. Phialide referring to the phialidic conidiogenous cells, and lunulospora, (lu.nu.la.tus N.L. adj. mean crescent-shaped + spo.ra N.L. fem. S. spora, referred to the conidia), referring to the genus Lunulospora.

Description

Asexual fungus. Conidiophores macronematous, semimacronematous, mononematous, septate, prostrate or erect, straight or flexuous, pigmented. Conidiogenous cells integrated, terminal, cylindrical to subulate, pale brown to brown, monophialidic or polyphialidic, enteroblastic. Conidial secession schizolytic. Conidia solitary, acrogenous, long lunate, vermiform to sigmoid, unicellular, hyaline, truncate at the conspicuous or inconspicuous basal frill, with a cellular, unbranched, eccentric basal appendage.

Phialolunulospora vermispora Z. F. Yu & R. F. Castaneda, sp. nov.

MycoBank No: 828717
Figures 2, 3, 4

Type

China, Hainan province, Limu Mountain, 19°29'40"N, 107°80'45"E, ca. 350 m alt., from leaves of an unidentified dicotyledonous plant submerged in a stream, Apr 2015, Zefen Yu, YMF 1.04260 – holotype; CGMCC 3.19632 – culture ex-type.

Figure 2. 

Phialolunulospora vermispora (YMF 1.04260) A colony on PDA at day 10 B conidia C–F conidiophores, conidiogenous cells and conidia G conidiogenous cells H, I conidiophores and conidiogenous cells. Scale bars: 10 mm (A); 10 μm (B–I).

Etymology

ver.mi- (from vermiformis), NL fem. adj mean worm-shaped + spo.ra N.L. fem. S. spora, referred to worm-shaped conidia.

Description

Mycelium partly superficial and partly immersed, composed of septate, branched, smooth, hyaline, 1–2 μm wide hyphae. Conidiophores solitary, macronematous, semimacronematous, erect or prostrate, straight or flexuous, unbranched, up to 4-septate, cylindrical, up to 150 μm long, 3–4 μm wide, pale brown to brown, smooth, sometimes reduced to conidiogenous cells. Conidiogenous cells integrated, terminal, cylindrical to subulate, sometimes lageniform, determinate, smooth, pale brown to brown, mostly darker than conidiophores, phialidic, after secession leaving an inconspicuous basal frill, 12–47 × 2.6–3 μm. Conidia solitary, acrogenous, long lunate, vermiform to sigmoid, unicellular, guttulate, hyaline, smooth-walled, 31–55 × 2.5–3.5 μm, acute at the apex and narrow truncate at the base bearing minute marginal frills and a cellular, single, unbranched, somewhat attenuated or acuminate, eccentric basal appendage, 1.5–4.6 μm long.

Figure 3. 

Phialolunulospora vermispora conidiogenous cells and conidia.

Culture characteristics

Colonies attain 2.4 cm diameter on PDA and 2.8 cm diameter on CMA after 10 days at 25 °C. On PDA, colonies flat to slightly raised, aerial mycelium abundant, margin entire to undulate, surface white initially, then become buff and grey with age, reverse same color. Colonies on CMA, center with aerial mycelium cottony, periphery with scarce aerial mycelium, olivaceous grey, dark green exudate and soluble pigment produced, reverse same color.

Distribution and ecology

The species occurs on submerged leaves in stream. This species is currently known only from the type locality.

Figure 4. 

Phialolunulospora vermispora conidiogenous cells.

Discussion

The family Chaetosphaeriaceae was firstly introduced by Réblová et al. (1999) to accommodate Chaetosphaeria and its allies. Réblová et al. (1999) also suggested that Chaetosphaeriaceae should be placed in the Sordariales. However, based on the nuclear large subunit ribosomal RNA gene (LSU) sequence, Huhndorf et al. (2004) placed Chaetosphaeriaceae in order Chaetosphaeriales. In a recent review of the family Chaetosphaeriaceae based on morphology and phylogenetic analysis, Lin et al. (2019) accepted 49 genera (including three uncertain genera) within the family, among which 44 were asexual genera.

The asexual morph of the Chaetosphaeriaceae is hyphomycetous taxa. It is characterized by septate, branched or unbranched conidiophores with the conidiogenous cell monophialidic or polyphialidic, holoblastic or enteroblastic, smoothwalled (Réblová et al. 1999, 2011). Our new fungus, Phialolunulospora vermispora, fits the general description of asexual hyphomycetous Chaetosphaeriaceae well. Phialolunulospora is mainly distinguished from other species in the Chaetosphaeriaceae in having vermiform to sigmoid conidia. Conidia of typical members of the family, including Dictyochaeta and Codinaea Maire (Réblová 2000; Whitton et al. 2000; Cruz et al. 2008; Crous et al. 2014), are aseptate or 1-septate; they may be setulose or not. In this study, the phylogenetic analyses combining ITS and LSU sequences showed that P. vermispora is close to three asexual genera in Chaetosphaeriaceae (Fig. 1), Dictyochaetopsis, Bahusutrabeeja and Dictyochaeta. Morphologically, Bahusutrabeeja and Dictyochaeta are superficially similar to P. vermispora in septate and cylindrical conidiophores, but can be distinguished from the new genus in having globose conidia without appendages and long fusiform conidia with long appendage (Subramanian and Bhat 1977; Li et al. 2014; Liu et al. 2016; Lin et al. 2019), respectively. P. vermispora is clearly different from Dictyochaetopsis species in morphology, such as smooth and pale brown or brown conidiophores and long lunate, vermiform to sigmoid conidia (Arambarri and Cabello 1990; Whitton et al. 2000; Castañeda-Ruíz et al. 2008).

Phialolunulospora is morphologically similar to some other genera species of Chaetosphaeriaceae in hyaline conidia with basal eccentric cellular appendages, including Neopseudolachnella A. Hashim. & Kaz. Tanaka, Pseudolachnea Ranoj., Pseudolachnella Teng and Rattania Prabhug. & Bhat. Of these, species of Neopseudolachnella, Pseudolachnea and Pseudolachnella are different from Phialolunulospora in acervular, setose and stromatic conidiomata (Ranojevic 1910; Teng and Ling 1936; Hashimoto et al. 2015). The genus Rattania is distinguished from Phialolunulospora in having seta and smaller septate conidia (Prabhugaonkar and Bhat 2009). In addition, the type species of Lunulospora Ingold, L. curvula Ingold (Sordariomycetes, Sordariales incertae sedis), also has resemblance to Phialolunulospora in conidial shape (Ingold 1942; Seifert et al. 2011), but it has obviously bigger size of conidia, 70–90 × 4–5 μm vs. 12–47 × 2.6–3 μm, in Lunulospora.

Many freshwater species occur in the family Chaetosphaeriaceae. So far, approximately 16 genera in this family have been reported from fresh water, such as Codinaea (Luo et al. 2019). In this study, Phialolunulospora vermispora was also collected from freshwater habitats.

Acknowledgements

This work was financed by the National Natural Science Foundation Program of PR China (31770026, 31970013). We are grateful to two reviewers for critically reviewing the manuscript and for providing helpful suggestions to improve this paper.

References

  • Arambarri AM, Cabello MN (1990) Considerations about Dictyochaeta, Codinaeopsis and a new genus Dictyochaetopsis. Mycotaxon 38: 11–14. https://doi.org/10.1007/BF02277306
  • Castañeda-Ruíz RF, Gusmão LFP, Guarro J, Stchigel AM, Stadler M, Saikawa M, Leão-Ferreira SM (2008) Two new anamorphic fungi from Brazil: Dictyochaetopsis polysetosa and Myrothecium compactum. Mycotaxon 103: 1–8. https://doi.org/10.1007/BF02277306
  • Crous PW, Wingfield MJ, Schumacher RK, Summerell BA, Giraldo A, Gené J, Guarro J, Wanasinghe DN, Hyde KD, Camporesi E, Garethjones EB, Thambugala KM, Malysheva EF, Malysheva VF, Acharya K, Álvarez J, Alvarado P, Assefa A, Barnes CW, Bartlett JS, Blanchette RA, Burgess TI, Carlavilla JR, Coetzee MPA, Damm U, Decock CA, Denbreeÿen A, Devries B, Dutta AK, Holdom DG, Rooney-Latham S, Manjón JL, Marincowitz S, Mirabolfathy M, Moreno G, Nakashima C, Papizadeh M, Shahzadehfazeli SA, Amoozegar MA, Romberg MK, Shivas RG, Stalpers JA, Stielow B, Stukely MJC, Swart WJ, Tan YP, Vanderbank M, Wood AR, Zhang Y, Groenewald JZ (2014) Fungal Planet description sheets: 281–319. Persoonia 33: 212–289. https://doi.org/10.3767/003158514X685680
  • Cruz ACR, Leáo-ferreira SM, Barbosa FR, Gusmão LFP (2008) Conidial fungi from semi-arid Caatinga biome of Brazil. New and interesting Dictyochaeta species. Mycotaxon 106: 15–27.
  • Hashimoto A, Sato G, Matsuda T, Matsumura M, Hatakeyama S, Harada Y, Ikeda H, Tanaka K (2015) Taxonomic revision of Pseudolachnea and Pseudolachnella and establishment of Neopseudolachnella and Pseudodinemasporium gen. nov. Mycologia 107(2): 383–408. https://doi.org/10.3852/14-171
  • Huhndorf SM, Miller AN, Fernandez FA (2004) Molecular systematics of the Sordariales: the order and the family Lasiosphaeriaceae redefined. Mycologia 96: 368–387. https://doi.org/10.2307/3762068
  • Li XX, Xia JW, Ma LG, Castaneda-Ruiz RF, Zhang XG (2014) A new species of Bahusutrabeeja from Guangxi, China. Mycotaxon 126: 227–230. https://doi.org/10.5248/126.227
  • Lin CG, McKenzie EHC, Liu JK, Jones EBG, Hyde KD (2019) Hyaline-spored chaetosphaeriaceous hyphomycetes from Thailand and China, with a review of the family Chaetosphaeriaceae. Mycosphere 10(1): 655–700. https://doi.org/10.5943/mycosphere/10/1/14
  • Liu J, Yang J, Maharachchikumbura SS, Mckenzie EH, Jones EB, Hyde KD, Liu ZY (2016) Novel chaetosphaeriaceous hyphomycetes from aquatic habitats. Mycological Progress 15(10–11): 1157–1167. https://doi.org/10.1007/s11557-016-1237-1
  • Luo Z, Hyde KD, Liu J, Maharachchikumbura SSN, Jeewon R, Bao D-F, Bhat DJ, Lin C-G, Li W-L, Yang J, Liu N-G, Lu Y-Z, Jayawardena RS, Li J-F, Su H-Y (2019) Freshwater Sordariomycetes. Fungal Diversity 99: 451–660. https://doi.org/10.1007/s13225-019-00438-1
  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403: 853–858. https://doi.org/10.1038/35002501
  • Prabhugaonkar A, Bhat DJ (2009) Rattania setulifera, an undescribed endophytic hyphomycete on rattans from Western Ghats, India. Mycotaxon 108: 217–222. https://doi.org/10.5248/108.217
  • Qiao M, Du X, Bian ZH, Peng J, Yu ZF (2017a) Ellisembia pseudokaradkensis sp. nov. from Hainan, China. Mycotaxon 132: 813–817. https://doi.org/10.5248/132.813
  • Qiao M, Li WJ, Huang Y, Xu JP, Zhang L, Yu ZF (2018b) Classiculasinensis, a new species of basidiomycetous aquatic hyphomycetes from southwest China. MycoKeys 40: 1–12. https://doi.org/10.3897/mycokeys.40.23828
  • Qiao M, Zheng H, Lv RL, Yu ZF (2020) Neodactylariales, Neodactylariaceae (Dothideomycetes, Ascomycota): new order and family, with a new species from China. MycoKeys 73: 69–85. https://doi.org/10.3897/mycokeys.73.54054
  • Ranojevic N (1910) Zweiter Beitrag zur Pilzflora Serbiens. Annales Mycologici 8: 347–402.
  • Réblová M, Barr ME, Samuels GJ (1999) Chaetosphaeriaceae, a new family for Chaetosphaeria and its relatives. Sydowia 51: 49–70.
  • Réblová M, Gams W, Seifert K (2011) Monilochaetes and allied genera of the Glomerellales, and a reconsideration of families in the Microascales. Studies in Mycology 68: 163–191. https://doi.org/10.3114/sim.2011.68.07
  • Seifert KA, Morgan-Jones G, Gams W, Kendrick B (2011) The genera of Hyphomycetes. CBS Biodiversity Series 9, CBSKNAW Fungal Biodiversity Centre, Utrecht.
  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729. https://doi.org/10.1093/molbev/mst197
  • Teng SC, Ling L (1936) Additional fungi from China IV. Sinensia 7: 752–823.
  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876–4882. https://doi.org/10.1093/nar/25.24.4876
  • Turner D, Kovacs W, Kuhls K, Lieckfeldt E, Peter B, Arisan-Atac I, Strauss J, Samuels GJ, Börner T, Kubicek CP (1997) Biogeography and phenotypic variation in Trichoderma sect. Longibrachiatum and associated Hypocrea species. Mycological Research 101(4): 449–459. https://doi.org/10.1017/S0953756296002845
  • Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238–4246. https://doi.org/10.1128/JB.172.8.4238-4246.1990
  • Wei M, Zhang H, Dong W, Boonmee S, Zhang D (2018) Introducing Dictyochaeta aquatica sp. nov. and two new species of Chloridium (Chaetosphaeriaceae, Sordariomycetes) from aquatic habitats. Phytotaxa 362(2): 187–199. https://doi.org/10.11646/phytotaxa.362.2.5
  • Whitton SR, Mckenzie EHC, Hyde KD (2000) Dictyochaeta and Dictyochaetopsis species from the Pandanaceae. Fungal Diversity 4: 133–158.
  • Williams J, Read C, Norton A, Dovers S, Burgman M, Proctor W, Anderson H (2001) Biodiversity, Australia State of the Environment Report 2001 (Theme Report). CSIRO Publishing on behalf of the Department of the Environment and Heritage, Canberra, 217 pp.
  • Yang J, Liu JK, Hyde KD, Bhat DJ, Jones EBG, Liu Z-Y (2016) New species of Sporoschisma (Chaetosphaeriaceae) from aquatic habitats in Thailand. Phytotaxa 289(2): 147–157. https://doi.org/10.11646/phytotaxa.289.2.4
  • Yang J, Liu NG, Liu J, Hyde KD, Jones EB, Liu ZY (2018) Phylogenetic placement of Cryptophiale, Cryptophialoidea, Nawawia, Neonawawia gen. nov. and Phialosporostilbe. Mycosphere 9(6): 1132–1150. https://doi.org/10.5943/mycosphere/9/6/5