http://orcid.org/0000-0003-3376-4376
Figures
Abstract
During our studies on asexual fungi colonizing herbaceous litter in northern Thailand, we discovered two new fungal species, viz. Dendryphion hydei and Torula hydei spp. nov. The latter are examined, and their morphological characters are described as well as their DNA sequences from ribosomal and protein coding genes are analysed to infer their phylogenetic relationships with extant fungi. Torula hydei is different from other similar Torula species in having tiny and catenate conidia. Dendryphion hydei can be distinguished from other similar Dendryphion species in having large conidiophores and subhyaline to pale olivaceous brown, 2–4(–5)-septate conidia. Multigene phylogenetic analyses of a combined LSU, SSU, TEF1-α, RPB2 and ITS DNA sequence dataset generated from maximum likelihood and Bayesian inference analyses indicate that T. hydei forms a distinct lineage and basal to T. fici. Dendryphion hydei forms a distinct lineage and basal to D. europaeum, D. comosum, D. aquaticum and D. fluminicola within Torulaceae (Pleosporales, Dothideomycetes).
Citation: Li J, Jeewon R, Mortimer PE, Doilom M, Phookamsak R, Promputtha I (2020) Multigene phylogeny and taxonomy of Dendryphion hydei and Torula hydei spp. nov. from herbaceous litter in northern Thailand. PLoS ONE 15(2): e0228067. https://doi.org/10.1371/journal.pone.0228067
Editor: Tzen-Yuh Chiang, National Cheng Kung University, TAIWAN
Received: September 26, 2019; Accepted: January 6, 2020; Published: February 5, 2020
Copyright: © 2020 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper.
Funding: The authors are grateful the Mushroom Research Foundation, Chiang Mai, Thailand and the Key Research Program of Frontier Sciences of the Chinese Academy of Sciences (grant no. QYZDY-SSW-SMC014) for supporting this research. Rungtiwa Phookamsak thanks CAS President’s International Fellowship Initiative (PIFI) for young staff (grant no. Y9215811Q1) and National Science Foundation of China (NSFC) project code 31850410489 (grant no. Y81I982211) for financial support. Peter E Mortimer would like to thank the National Science Foundation of China and the South East Asian Biodiversity resources Institute, Chinese Academy of Sciences, for financial support under the following grants: 41761144055, 41771063, Y4ZK111B01. Mingkwan Doilom thanks the 5th batch of Postdoctoral Orientation Training Personnel in Yunnan Province and the 64th batch of China Postdoctoral Science Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: NO authors have competing interests.
Introduction
The family Torulaceae Corda was introduced by Sturm [1] and is typified by Torula Pers. Species in Torulaceae are known only by their asexual morphs which are characterized as followed: superficial, effuse, greyish brown to black, powdery colonies; micro- or macronematous conidiophores, with or without apical branches; doliiform to ellipsoid or clavate, brown, smooth to verruculose, mono- to polyblastic conidiogenous cells which often remaining cupulate; subcylindrical, phragmosporous, acrogenous, brown, dry, smooth to verrucose conidia characteristically produced in branched chains [2,3,4,5,6,7]. Crous et al. [8] investigated phylogenetic relationships of this family with the inclusion of Torula species and accepted Dendryphion Wallr., besides Torula within Torulaceae in Pleosporales. Su et al. [6] introduced Neotorula Ariyaw., Z.L. Luo & K.D. Hyde and two new Dendryphion species in Torulaceae based on molecular data. Li et al. [9] established a novel genus, Sporidesmioides Jun F. Li, Phook. & K.D. Hyde. Su et al. [7] examined 21 freshwater taxa and updated phylogenetic relationships of taxa within the family Torulaceae based on ITS, LSU, TEF1-α and RPB2 genes and accommodated Rostriconidium Z.L. Luo, K.D. Hyde & H.Y. Su within Torulaceae. Crous et al. [10] designated the epitype of Rutola J.L. Crane & Schokn. and accepted the genus in Torulaceae based on LSU phylogeny. Currently, there are six accepted genera in Torulaceae viz. Dendryphion, Neotorula, Rostriconidium, Rutola, Sporidesmioides and Torula [10,4,9,6,7].
Torula is typified by T. herbarum Pers. and is morphologically characterized by having terminal or lateral, monoblastic or polyblastic conidiogenous cells with a thickened and heavily melanized wall on the base and thin-walled and frequently collapsing and becoming coronate on the apex [11]. Crane and Schoknecht [12] provided details of conidiogenesis in Torula based on light and transmission electron microscopy. Based on their examination, conidiogenesis has provided good taxonomic insights useful to segregate Torula and these were also observed by Mason [13], Hughes [14], Subramanian [15] and Ellis [16,17]. However, there was little information regarding the phylogenetic relationships of Torula until the studies of Crous et al. [8], Li et al. [5] and Su et al. [6,7]. To date, only 15 species have their DNA sequence data being analysed to reveal their phylogenetic placements in Torulaceae [18,19,9,5,6,7,20].
Dendryphion Wallr. was introduced by Wallroth [21] to accommodate hyphomycetous species, D. comosum Wallr. The genus is commonly known to be saprobic on dead stems of herbaceous plants and decaying wood, and is characterized by having erect, solitary, branched in upper part, polytretic conidiophores, forming septate, pigmented, thick-walled, finely roughened stipe and a distinct conidiogenous apparatus, with dark scars and catenate, in simple or branched chains of brown, septate (didymo- or cheiro) conidia [8,7]. Crous et al. [3] introduced D. europaeum Crous & R.K. Schumacher based on morphological characteristics and molecular data and later Crous et al. [8] accommodated the species in Torulaceae and further accepted Dendryphion in Torulaceae. Su et al. [6] circumscribed genera of Torulaceae from freshwater. Only seven Dendryphion species have DNA sequence data and their phylogenetic affinities to members of the Torulaceae have been investigated.
In this study, a novel Torula species was isolated from herbaceous litters collected from northern Thailand. Among collected samples, Dendryphion hydei is also recovered as another new species from northern Thailand. These species are described and illustrated. In addition, an updated phylogenetic tree with our new taxa for the family Torulaceae is provided in this study.
Material and methods
Isolation and identification
The specimens were collected from herbaceous litters (Chromolaena odorata Linn. and Bidens pilosa Linn.) in northern Thailand during the year 2015 to 2016. Samples were returned to the laboratory (Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai, Thailand) for examination and description of morphological characteristics. The specimens were observed under a Motic SMZ 168 series dissecting stereomicroscope. The conidial structures were picked up by a sterilized surgical needle and transferred into 10% lacto-glycerol on a clean slide and examined under a Nikon Eclipse 80i compound microscope and photo-captured with a Canon 600D digital camera using DIC microscopy. Macro- morphological structures were photographed with a Discovery V.8 stereo microscope fitted with a CARL ZEISS Axio Cam ERc5S microscope camera. Tarosoft® Image Frame Work program v.0.9.0.7 and Adobe Photoshop CS5 Extended version 10.0 software (Adobe Systems Inc., The United States) were used for measurements and drawing photographic plates.
Single conidium isolation was carried out to obtain pure cultures as described in Dai et al. [22]. Germinating conidia were transferred aseptically to potato dextrose agar (PDA) and malt extract agar (MEA) plates and grown at room temperature (16–30°C) in alternating day and night light. Colony characters were observed and recorded after one week and at weekly intervals [23,24].
The type specimens were deposited in the herbarium of Mae Fah Luang University (MFLU), Chiang Rai, Thailand and the Herbarium of Cryptogams Kunming Institute of Botany Academia Sinica (KUN-HKAS), Yunnan, China. Ex-type living cultures were deposited in Mae Fah Luang University Culture Collection (MFLUCC 18–0250 and MFUCC 18–0236) and Kunming Institute of Botany Culture Collection (KUMCC 16–0037 and KUMCC 18–0009). Faces of Fungi and Index Fungorum numbers are registered as outlined in Jayasiri et al. [25] and Index Fungorum [26]. New species are established based on guidelines of Jeewon and Hyde [27].
DNA extraction, PCR amplification and sequencing
Fungal mycelium was scraped off and transferred to a 1.5 ml micro-centrifuge tube using a sterilized lancet for genomic DNA extraction. The Biospin Fungus Genomic DNA Extraction Kit-BSC14S1 (BioFlux®, P.R. China) was used to extract fungal genomic DNA, following the protocols in the manufacturer’s instructions.
DNA amplification was performed by polymerase chain reaction (PCR) using the following genes (ITS, LSU, SSU, RPB2 and TEF1-α). The primers ITS5 and ITS4 primer pairs were used to amplify the ITS and 5.8S regions of the rDNA gene [28]; The primers LR0R and LR5 were used to amplify the partial ribosomal RNA for the 28S nuclear large subunit (LSU) [29]; NS1 and NS4 were used to amplify the partial ribosomal RNA for the 18S nuclear small subunit (SSU) [28]; fRPB2-5F and fRPB2-7cR were used to amplify the partial RNA polymerase second largest subunit (RPB2) [30] and EF1-983F and EF1-2218R were used to amplify the translation elongation factor 1-alpha gene (TEF1-α) [31].
The final volume of the PCR reaction was 25 μl, containing 1 μl of DNA template, 1 μl of each forward and reward primer, 12.5 μl of 2×Easy Taq PCR SuperMix (mixture of EasyTaqTM DNA Polymerase, dNTPs, and optimized buffer, Beijing TransGen Biotech Co., Ltd., Beijing, P.R. China) and 9.5 μl of ddH2O. The PCR thermal cycling conditions of ITS, LSU, SSU and TEF1-α were as follows: 94°C for 3 minutes, followed by 35 cycles of denaturation at 94°C for 30 seconds, annealing at 55°C for 50 seconds, elongation at 72°C for 1 minute, and a final extension at 72°C for 10 minutes. The PCR thermal cycle program for RPB2 was as follows: initial denaturation at 95°C for 5 minutes, followed by 40 cycles of denaturation at 95°C for 1 minute, annealing at 52°C for 2 minutes, elongation at 72°C for 90 seconds, and final extension at 72°C for 10 minutes. Purification and sequencing of PCR fragments with PCR primers mentioned above were carried out at Shanghai Majorbio Biopharm Technology Co., Ltd, China.
Sequence alignment and phylogenetic analyses
Phylogenetic analyses were performed from single gene (LSU dataset) as well as based on a combined LSU, SSU, TEF1-α, RPB2 and ITS sequence dataset. Sequences generated from this study were analyzed with other similar sequences obtained from GenBank and those derived from recent publications [32,10,19,9,5,6,7] (Table 1). The single gene alignment was performed by using MAFFT v. 7 [33] (http://mafft.cbrc.jp/alignment/server/) and manually aligned wherever necessary in MEGA version 7.0 [34]. Further analyses for the combined dataset were analyzed by maximum likelihood (ML) implemented in RAxMLGUI v.0.9b2 [35,36,37,38] and Bayesian Inference (BI) criteria [39,40] following the methodology in Li et al. [5].
The newly generated sequences are indicated in blue bold font, while the type strains are in black bold font.
The phylogram was represented in Treeview [57] and drawn in Microsoft PowerPoint and converted to jpeg file in Adobe Photoshop version CS5 (Adobe Systems Inc., the United States). The new sequences were submitted in GenBank (Table 1). The alignment was deposited in TreeBASE [58] under the accession number 25462.
Nomenclature
The electronic version of this article in Portable Document Format (PDF) in a work with an ISSN or ISBN will represent a published work according to the International Code of Nomenclature for algae, fungi, and plants, and hence the new names contained in the electronic publication of a PLOS ONE article are effectively published under that Code from the electronic edition alone, so there is no longer any need to provide printed copies.
In addition, new names contained in this work have been submitted to Index Fungorum from where they will be made available to the Global Names Index. The unique Index Fungorum number can be resolved and the associated information viewed through any standard web browser by appending the Index Fungorum number contained in this publication to the prefix www.indexfungorum.org/. The online version of this work is archived and available from the following digital repositories: PubMed Central and LOCKSS.
Results
Phylogenetic analyses
The combined LSU, SSU, TEF1-α, RPB2 and ITS sequence dataset comprises 71 taxa with Occultibambusa bambusae (MFLUCC 13–0855) and Neooccultibambusa chiangraiensis (MFLUCC 12–0559) as the outgroup taxa. Bayesian Inference (BI) and maximum likelihood (ML) analyses of the combined dataset were performed to determine the placement of our new taxa and infer relationships at the intrageneric level as well as resolving the phylogenetic relationships of the core families in Pleosporales. The phylogenetic trees obtained from BI and ML analyses resulted in trees with largely similar topologies and also similar to those generated from previous studies based on maximum likelihood analysis [18,5,7]. The best scoring RAxML tree is shown in Fig 1, with the final ML optimization likelihood value of -32357.090382 (ln). The dataset consists of 4053 total characters including gaps (LSU: 1–840 bp, SSU: 841–1776 bp, TEF1-α: 1777–2566 bp, RPB2: 2567–3418 bp, ITS: 3419–4053). RAxML analysis yielded 1585 distinct alignment patterns and 33.97% of undetermined characters or gaps. Estimated base frequencies were as follows: A = 0.246366, C = 0.258260, G = 0.271248, T = 0.224126, with substitution rates AC = 1.424215, AG = 3.485957, AT = 1.457990, CG = 0.955364, CT = 6.607514, GT = 1.000000. The proportion of invariable sites I = 0, the gamma distribution shape parameter alpha = 0.180234 and the Tree-Length = 3.299994. Bayesian posterior probabilities (BYPP) from MCMC were evaluated with final average standard deviation of split frequencies = 0.008574.
Bootstrap support values for maximum likelihood (ML) equal to or greater than 50% and Bayesian posterior probabilities (PP) equal to or greater than 0.95 are shown as “ML/PP” above the nodes. The tree is rooted to Occultibambusa bambusae (MFLUCC 13–0855) and Neooccultibambusa chiangraiensis (MFLUCC 12–0559). The type strains are in black bold and the newly generated sequences are indicated in blue bold.
Most of the core genera of Torulaceae and other representative genera in Nigrogranaceae, Ohleriaceae, Roussoellaceae and Thyridariaceae are included in our phylogenetic analysis (Fig 1). Torulaceae formed a well-resolved clade (100% ML and 1.00 PP) with a close relationship to Roussoellaceae and Thyridariaceae. Species of different genera currently accommodated in Torulaceae formed well-resolved subclades except for Sporidesmioides which is recovered as basal to other genera with significant Bayesian support (1.00 PP) but with low support in ML analysis (56% ML). Torula is recovered as a strongly monophyletic genus in Torulaceae. Torula hydei is sister to T. fici with high support (100% ML and 1.00 PP). Dendryphion hydei forms a distinct lineage and related to D. europaeum, D. comosum, D. aquaticum, D. fluminicola and D. submersum with significant support in BI analysis (1.00 PP).
Taxonomy
Dendryphion hydei J.F. Li, Phookamsak & Jeewon, sp. nov. Fig 2
Dendryphion hydei (HKAS 97479, holotype) a Colonies on branch of Bidens pilosa. b, c Apex of conidiophores with conidial structures. d, e Conidiophores. f–i Conidiogenous cells. j–q Conidia. Scale bars: a = 100 μm, d, e = 50 μm, b, f–i = 20 μm, b, c, f–q = 10 μm.
[urn:lsid:indexfungorum.org:names:556746]
Facesoffungi number: FoF04574
Etymology–Named in honour of Kevin D. Hyde for his excellent contribution to mycology and on his 65th birthday celebration.
Holotype–KUN-HKAS 97502
Saprobic on a branch litter of Bidens pilosa Linn. (Asteraceae). Sexual morph: Undetermined. Asexual morph: Colonies on the substratum superficial, effuse, gregarious, hairy, brown to dark brown. Mycelium composed of branched, septate, pale brown to brown hyphae. Conidiophores 260–380 μm long × 7–14 μm diam. (13–17 μm diam. at the base) ( = 356.7 × 9.9 μm, n = 10) macronematous, mononematous, septate, verrucose, thick-walled, branching simple or penicillate at the tip of primary branches, brown, flexuous. Conidiogenous cells 6–10 μm long × 3–5 μm diam. (
= 8 × 3.8 μm, n = 20) terminal, integrated, pale brown, polytretic. Conidia (17–)20–30(–35) μm long × 4–7 μm diam. (
= 26.5 μ 5.6 μm, n = 30) single, subhyaline to pale olivaceous brown, slightly paler at the end cells, dry, verrucose, monilioid, 2–4(–5)-septate, constricted at the septa. Conidial secession schizolytic.
Cultural characteristics: Conidia germinating on PDA within 14 hours and germ tubes produced from the apex. Colonies growing on PDA, reaching 5 cm in 21 days at 16–30°C, mycelium partly superficial, partly immersed, slightly effuse, hairy, vertical, with regular edge, white to grayish-brown, not produced pigmentation on media agar.
Material examined: THAILAND, Chiang Mai Province, Mae Taeng District, Mushroom Research Centre, on a branch litter of Bidens pilosa Linn., 12 July 2016, J.F. Li, FHP3 (HKAS 97502, holotype), ex-type living culture, MFLUCC 18–0236, KUMCC 18–0009.
Notes–Dendryphion hydei is unique in having large conidiophores and subhyaline to pale olivaceous brown, 2–4(–5)-septate conidia to compare with other related species in Dendryphion. Dendryphion hydei resembles D. aquaticum and D. europaeum in morphology. However, these species can be distinguished based on the size of the conidiophores, conidiogenous cells and conidia, as well as conidial septation and habitats (see Table 2). Dendryphion hydei has 2–4(–5)-septate conidia and inhabit in a terrestrial environment, similar to D. europaeum. However, D. europaeum has smaller conidiophores and conidia, and the conidia of D. europaeum are (2–)3(–5)-septate while D. aquaticum inhabits in a freshwater environment and has 3–6-septate conidia [3,7]. In the phylogenetic tree, D. hydei forms a separate lineage and clustered with D. europaeum, D. comosum, D. aquaticum and D. fluminicola with significant support in Bayesian inference analysis (1.00 PP). A comparison of TEF1-α nucleotides shows that D. hydei differs from D. fluminicola in 20/852 bp (2.3% difference, no gap) and from D. submersum in 30/902 bp (3.3% difference, no gap). A comparison of ITS nucleotides shows that D. hydei differs from D. europaeum in 19/553 bp (3.4% difference, no gap) and differs from D. aquaticum in 6/398 bp (1.5% difference, no gap). Phylogenetic analyses support D. hydei as a new species in Dendryphion. These tally with recommendations outlined by Jeewon and Hyde [27] to establish our new species. In this study, we collected D. hydei from Bidens pilosa, which is a new host record for this species. A morphometric comparison of the new taxon with other similar taxa of Dendryphion provide in Table 2.
Torula hydei J.F. Li, Phookamsak & Jeewon, sp. nov. Fig 3
a Colonies on dead branch of Chromolaena odorata. b–e Conidiophores with conidiogenous cell. f–j Budding on conidia. k, l Conidia in chain. m–t Conidia. Scale bars: a = 100 μm, b, k–l = 5 μm, c, f–j, q–t = 2 μm, d, e, m–p = 1 μm.
[urn:lsid:indexfungorum.org:names:556747]
Facesoffungi number: FoF 04573
Etymology–Named in honour of Kevin D. Hyde for his excellent contribution to mycology and on his 65th birthday celebration.
Holotype–HKAS 97478
Saprobic on an aerial dead branch of Chromolaena odorata Linn. Sexual morph: Undetermined. Asexual morph: Colonies discrete on host, black, powdery. Mycelium immersed on the substrate, composed of septate, branched, smooth, light brown hyphae. Conidiophores (1.5–)2–3 μm long × 1.5–2 μm diam. ( = 2.2 × 1.8 μm, n = 10), semi-macronematous, mononematous, solitary, erect, light brown, verruculose, thick-walled, consist of one cell or reduced to conidiogenous cells, without apical branches, subcylindrical to subglobose, arising from prostrate hyphae. Conidiogenous cells 3–5.5 μm long × 4.3–5 μm diam. (
= 3.8 × 4.5 μm, n = 20), polyblastic, terminal, dark brown to black, smooth to minutely verruculose, thick-walled, doliiform to ellipsoid. Conidia (7.5–)8–14 μm long × 2–4 μm diam. (
= 10.4 × 3.4 μm, n = 30), solitary to catenate, acrogenous, simple, phragmosporous, brown to dark brown, minutely verruculose, 2–3-septate, rounded at both ends, composed of subglobose cells, slightly constricted at some septa, chiefly subcylindrical. Conidial secession schizolytic.
Cultural characteristics: Conidia germinating on PDA within 14 hours and germ tubes produced from the apex. Colonies growing on PDA, reaching 5 cm in 10 days at 16–30°C, mycelium partly superficial, partly immersed, slightly effuse, hairy, vertical, with regular edge, light brown to brown, not produced pigmentation on media agar; not sporulated on media agar within 2 months.
Material examined: THAILAND, Chiang Mai Province, Mae Taeng District, on an aerial dead branch of Chromolaena odorata Linn. (Asteraceae), 26 December 2015, J.F. Li, MRC2 (HKAS 97478, holotype), ex-type living culture, MFLUCC 18–0250, KUMCC 16–0037.
Notes–Torula hydei resembles T. herbarum and T. fici in having 2–3-septate, catenated, brown, verruculose conidia, but differs in having smaller conidia [3]. Phylogenetic analyses showed that T. hydei constitutes an independent lineage basal to T. fici (100% ML and 1.00 BYPP). Morphologically T. hydei differs from T. fici in having smaller conidia (T. hydei, (7.5–)8–14 × 2–4 μm versus (12–)13–17(–19) × 5(–6) μm, T. fici) and the conidia are also brown to dark brown, paler at the apex where branching occurs [8]. Whereas, T. fici has brown conidia, with a pale brown apex and the fertile cells in the conidial chain, where branching occurs, are darker brown than other cells [8]. The conidiogenous cells of T. fici are slightly larger than T. hydei and frequently clavate (T. fici, (5–)6(–8) × 5(–7) μm versus 3–5.5 × 4.3–5 μm, T. hydei), whereas, T. hydei has doliiform to ellipsoid conidiogenous cells [8]. We also note distinct nucleotide base pair differences between T. hydei and T. fici (CBS 595.96, type strain) across the ITS gene region (8/479 bp, 1.7% difference, no gap) and TEF1-α gene region analysed (43/760 bp, 5.7% difference, no gap). Based on distinct morphological characteristics and phylogenetic support, T. hydei is introduced as a new species in this study.
Discussion
Taxonomic characterizations of taxa in Torulaceae have been well-studied since Crous et al. [8] who re-classified Torula and Dendryphion in Torulaceae (Pleosporales, Dothideomycetes) based on phylogenetic analyses of LSU sequence data. Subsequent authors introduced new genera and species in this family based on multigene phylogenetic analyses coupled with morphological characteristics (see Table 3) [10,18, 9, 5, 6, 7, 20]. Recently, there are more than 520 epithets in the genus Torula and 85 epithets in Dendryphion listed in Index Fungorum [26]. However, most of the described species lack DNA sequence data to verify their phylogenetic placement and affinities with other related fungi. Nevertheless, many species previously described as Torula and Dendryphion have also been synonymized to many genera in Sordariomycetes [26]. Taxa in these genera need to be clarified based on molecular data.
Torula and Dendryphion have a wide host range in various habitats and are commonly found as saprobes in both terrestrial and aquatic habitats in temperate to tropical regions [10,3,59,18,9, 5,6,7,20]. It is interesting to note that many Torula species have been found to be associated with the host family Asteraceae [59,5]. In this study, our new strains were collected from Asteraceae and Li et al. [5] also reported two novel Torula species, T. chromolaenae and T. mackenziei from Asteraceae, indicating that Asteraceae harbors a diversity of these taxa. Dendryphion hydei was also collected from Bidens pilosa (Asteraceae) and is the first record from northern Thailand.
Acknowledgments
The authors acknowledge the Biology Experimental Center, Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences to provide molecular laboratory facilities for molecular work. Itthayakorn Promputtha grateful to thank Chiang Mai University for partially support of this research work. Rajesh Jeewon would like to thank Mae Fah Luang University for giving him the opportunity as a visiting professor to the Center of Excellence in Fungal Research and University of Mauritius for research support. Mingkwan Doilom would like to thank the 5th batch of Postdoctoral Orientation Training Personnel in Yunnan Province and the 64th batch of China Postdoctoral Science Foundation for research support. We thanks to Emeritus Prof. Kevin D. Hyde, Dr. Shaun Pennycook, Dr. Dhanushka Wanasinghe, Hong-Bo Jiang, Dr. Zonglong Luo for their available suggestions and help.
References
- 1. Sturm J. Deutschlands Flora, Abt. III. Die Pilze Deutschlands. 1829; 2: 1–136.
- 2.
Bhat DJ. Fascinating Microfungi (Hyphomycetes) Of Western Ghats-India. Department of Botany. Goa University. 2017.
- 3. Crous PW, Shivas RG, Quaedvlieg W, van der Bank M., Zhang Y, Summerell BA, et al. Fungal Planet description sheets: 214–280. Persoonia. 2014; 32(1):184–306. http://doi: 10.3767/003158514X682395
- 4. Hyde KD, Hongsanan S, Jeewon R, Bhat DJ, McKenzie EHC, Jones EBG, et al. Fungal diversity notes 367–490: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers. 2016; 80:1–270. https://doi.org/10.1007/s13225-016-0373-x
- 5. Li JF, Phookamsak R, Jeewon R, Bhat DJ, Mapook A, Camporesi E, et al. Molecular taxonomy and morphological characterization reveal new species and new host records of Torula species (Torulaceae, Pleosporales). Mycol Prog. 2017; 16:447–461. https://doi: 10.1007/s11557-017-1292-2
- 6. Su HY, Hyde KD, Maharachchikumbura SSN, Ariyawansa HA, Luo ZL, Promputtha I, et al. The families Distoseptisporaceae fam. nov., Kirschsteiniotheliaceae, Sporormiaceae and Torulaceae, with new species from freshwater in Yunnan Province, China. Fungal Divers. 2016; 80(1):375–409. https://doi:10. 1007/ s13225-016-0362-0
- 7. Su XJ, Luo ZL, Jeewon R, Bhat DJ, Bao DF, Li WL, et al. Morphology and multigene phylogeny reveal new genus and species of Torulaceae from freshwater habitats in northwestern Yunnan, China. Mycol Prog. 2018; 17(5):531–545. https://doi.org/10.1007/s11557-018-1388-3
- 8. Crous PW, Carris LM, Giraldo A, Groenewald JZ, Hawksworth DL, Hernández-Restrepo M, et al. The Genera of Fungi-fixing the application of the type species of generic names–G2: Allantophomopsis, Latorua, Macrodiplodiopsis, Macrohilum, Milospium, Protostegia, Pyricularia, Robillarda, Rotula, Septoriella, Torula, and Wojnowicia. IMA Fungus. 2015; 6(1): 163–198. pmid:26203422
- 9. Li JF, Bhat DJ, Phookamsak R, Mapook A, Lumyong S, Hyde KD. Sporidesmioides thailandica gen. et sp. nov. (Dothideomycetes) from northern Thailand. Mycol Prog. 2016; 15(10–11):1169–1178. https://doi: 10.1007/s11557-016-1238-0
- 10. Crous PW, Schumacher RK, Wood AR, Groenewald JZ. The Genera of Fungi–G5: Arthrinium, Ceratosphaeria, Dimerosporiopsis, Hormodochis, Lecanostictopsis, Lembosina, Neomelanconium, Phragmotrichum, Pseudomelanconium, Rutola, and Trullula. Fungal Systematics and Evolution. 2020; 5: 77–98.
- 11. Crane JL, Miller AN. Studies in genera similar to Torula: Bahusaganda, Bahusandhika, Pseudotorula, and Simmonsiella gen. nov. IMA Fungus. 2016; 7(1): 29–45. pmid:27433439
- 12. Crane JL, Schoknecht JD. Revision of Torula species. Rutola, a new name for Torula graminis. Can J Bot. 1977; 55: 3013–3019. http://doi: 10.1139/b77-339
- 13. Mason EW. Annotated account of fungi received at the Imperial Mycological Institute. List 2. Fasc. 3 (special part). Commonw. Mycol Pap. 1941; 5:1–144.
- 14. Hughes SJ. Conidiophores, conidia, and classification. Can J Bot. 1953; 31:577–659. https://doi.org/10.1139/b53-046
- 15.
Subramanian CV. Hyphomycetes: An account of Indian species except Cercosporae. New Delhi: Indian Council of Agricultural Research. 1971
- 16.
Ellis MB. Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Kew.1971.
- 17.
Ellis MB. More Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Kew. 1976.
- 18. Hyde KD, Norphanphoun C, Abreu VP, Bazzicalupo A, Chethana KWT, Clericuzio M, et al. Fungal diversity notes 603–708: taxonomic and phylogenetic notes on genera and species. Fungal Divers. 2017; 87:1–235. https://doi.org/10.1007/s13225-017-0391-3
- 19. Hyde KD, Tennakoon DS, Jeewon R, Bhat DJ, Maharachchikumbura SSN, Rossi W, et al. Fungal diversity notes 1036–1150: taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Divers. 2019; 96:1–242. https://doi.org/10.1007/s13225-019-00429-2
- 20. Tibpromma S, Hyde KD, Jeewon R, Maharachchikumbura SSN, Liu JK, Bhat DJ, et al. Fungal diversity notes 491–602: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers. 2017; 83:1–261. https://dio.org/10.1007/s13225-017-0378-0
- 21. Wallroth CFW. Flora Cryptogamica Germaniae. 1833; 2:1–923
- 22. Dai DQ, Phookamsak R, Wijayawardene NN, Li WJ, Bhat DJ, Xu JC, et al. Bambusicolous fungi. Fungal Divers. 2017; 82(1): 1–105.
- 23. Boehm EWA, Mugambi GK, Miller AN, Huhndorf SM, Marincowitz S, Spatafora JW, et al. A molecular phylogenetic reappraisal of the Hysteriaceae, Mytilinidiaceae and Gloniaceae (Pleosporomycetidae, Dothideomycetes) with keys to world species. Stud Mycol. 2009; 64: 49–83. pmid:20169023
- 24. Chomnunti P, Hongsanan S, Aguirre-Hudson B, Tian Q, Peršoh D, Dhami MK, et al. The sooty moulds. Fungal Divers. 2014; 66: 1–36. http://doi:10.1007/s13225-014-0278-5
- 25. Jayasiri SC, Hyde KD, Ariyawansa HA, Bhat DJ, Buyck B, Cai L, et al. The Faces of Fungi database: fungal names linked with morphology, phylogeny and human impacts. Fungal Divers. 2015; 74:3–18. https://doi.org/10.1007/s13225-015-0351-8
- 26.
Index Fungorum. 2019 http://www.indexfungorum.org/names/Names.asp (Accessed 1 February 2019).
- 27. Jeewon R, Hyde KD. Establishing species boundaries and new taxa among fungi: recommendations to resolve taxonomic ambiguities. Mycosphere. 2016; 7(11):1669–1677. https://doi: 10.5943/mycosphere/7/11/4
- 28. White TJ, Bruns T, Lee SJWT, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR—Protocols and Applications. 1990; 18:315–322.
- 29. Vilgalys R, Hester M. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol. 1990; 172:4238–4246. pmid:2376561
- 30. Liu YJ, Whelen S, Hall BD. Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol. 1999; 16:1799−1808. pmid:10605121
- 31. Rehner SA. Primers for Elongation Factor 1-alpha (EF1-alpha). 2001. Available from: http://ocid. NACSE.ORG/research/deephyphae/EF1primer.pdf.
- 32. Ariyawansa HA, Hyde KD, Jayasiri SC, Buyck B, Chethana KWT, Dai DQ, et al. Fungal diversity notes 111–252—Taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers. 2015; 75: 27–274. http://dx.doi.org/10.1007/s13225-015-0355-4
- 33. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30:772–780. pmid:23329690
- 34. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0. Mol Biol Evol. 2016; 33(7):1870–1874. pmid:27004904
- 35. Silvestro D, Michalak I. RAxML GUI: a graphical front–end for RAML http://sourceforge.net/projects/raxmlgui. 2010.
- 36. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006; 22:2688–2690. pmid:16928733
- 37. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014; 30(9):1312–1313. pmid:24451623
- 38. Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology. 2008; 57:758–771. pmid:18853362
- 39. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001; 17:754–755. pmid:11524383
- 40. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. Bayesian inference of phylogeny and its impact on evolutionary biology. Science. 2001; 294:2310–2314. pmid:11743192
- 41. Ahmed SA, van de Sande WWJ, Stevens DA, Fahal A, van Diepeningen AD, Menken SBJ, et al. Revision of agents of black-grain eumycetoma in the order Pleosporales. Persoonia. 2014; 33(1):141–154. 10.3767/003158514X684744
- 42. Wanasinghe DN, Phukhamsakda C, Hyde KD, Jeewon R, Lee HB, Jones EBG, et al. Fungal diversity notes 709–839: taxonomic and phylogenetic contributions to fungal taxa with an emphasis on fungi on Rosaceae. Fungal Divers. 2018; 89:1–236. https://doi.org/10.1007/s13225-017-0378-0
- 43. Vu D, Groenewald M, De Vries M, Gehrmann T, Stielow B, Eberhardt U, et al. Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Studi Mycol. 2019; 92:135–154.
- 44. Jaklitsch WM, Voglmayr H. Hidden diversity in Thyridaria and a new circumscription of the Thyridariaceae. Stud Mycol. 2016; 85:35–64. pmid:27872508
- 45. Phookamsak R, Hyde KD, Jeewon R, Bhat DJ, Gareth Jones EB, Maharachchikumbura SSN, et al. Fungal diversity notes 929–1035: taxonomic and phylogenetic contributions on genera and species of fungi. Fungal Divers. 2019; 95(1):1–273. https://doi.org/10.1007/s13225-019-00421-w
- 46. Doilom M, Dissanayake AJ, Wanasinghe DN, Boonmee S, Liu JK, Bhat DJ, et al. Microfungi on Tectona grandis (teak) in northern Thailand. Fungal Divers. 2017; 82(1): 107–182. https://doi.org/10.1007/s13225-016-0368-7
- 47. Liu JK, Phookamsak R, Dai DQ, Tanaka K, Jones EBG, Xu JC, et al. Roussoellaceae, a new pleosporalean family to accommodate the genera Neoroussoella gen. nov., Roussoella and Roussoellopsis. Phytotaxa. 2014; 181(1):1−33. http://dx.doi.org/10.11646/phytotaxa.181.1.1
- 48. Shaw JJ, Spakowicz DJ, Dalal RS, Davis JH, Lehr NA, Strobel SA. Biosynthesis and genomic analysis of medium-chain hydrocarbon production by the endophytic fungal isolate Nigrograna mackinnonii E5202H. Appl. Microbiol. Biotechnol. 2015; 99(8):3715–3728. pmid:25672844
- 49. Suetrong S, Schoch CL, Spatafora JW, Kohlmeyer J, Volkmann-Kohlmeyer B, Sakayaroj J, et al. Molecular systematics of the marine Dothideomycetes. Stud Mycol. 2009; 64:155–173. pmid:20169029
- 50. Tibpromma S., Hyde K.D., McKenzie E.H., Bhat D.J., Phillips A.J., Wanasinghe D.N., et al., 2018. Fungal diversity notes 840–928: micro-fungi associated with Pandanaceae. Fungal diversity, 93(1), pp.1–160.
- 51. Tanaka K, Hirayama K, Yonezawa H, Hatakeyama S, Harada Y, Sano T, et al. Molecular taxonomy of bambusicolous fungi: Tetraplosphaeriaceae, a new Pleosporalean family with Tetraploa-like anamorphs. Stud Mycol. 2009; 64:175−209. pmid:20169030
- 52. Shenoy BD, Jeewon R, Wu WP, Bhat DJ, Hyde KD. Ribosomal and RPB2 DNA sequence analyses suggest that Sporidesmium and morphologically similar genera are polyphyletic. Mycol Res. 2006; 110(8):916–928. https://doi.org/10.1016/j.mycres.2006.06.004
- 53. Devadatha B, Sarma VV, Jeewon R, Wanasinghe DN, Hyde KD, Jones EG. Thyridariella, a novel marine fungal genus from India: morphological characterization and phylogeny inferred from multigene DNA sequence analyses. Mycol Prog. 2018; 1–14. https://doi.org/10.1007/s11557-018-1387-4
- 54. Crous PW, Wingfield MJ, Burgess TI, Hardy GE, Crane C, Barrett S, et al. Fungal Planet description sheets: 469–557. Persoonia. 2016; 37: 218–403. pmid:28232766
- 55. Hyde KD, Dong Y, Phookamsak R, Jeewon R, Bhat DJ, Jones EBG, et al. Fungal diversity notes 1151–1276: taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Divers. 2020 (proof).
- 56. Pratibha J, Prabhugaonkar A. Torula goaensis, a new asexual ascomycetous fungus in Torulaceae. Webbia. 2017; 72(2):171–175. https://doi.org/10.1080/00837792.2017.1349237
- 57. Page RDM. TreeView: an application to display phylogenetic trees on personal computers. CABIOS. 1996; 12:357–358. pmid:8902363
- 58.
TreeBASE. available from: https://treebase.org/ (accessed: January 2019). 2019.
- 59.
Farr DF, Rossman AY. Fungal Databases, U.S. National Fungus Collections, ARS, USDA. Retrieved January 3, 2019; from https://nt.ars-grin.gov/fungaldatabases/
- 60.
Seifert K, Morgan-Jones G, Gams W, Kendrick B. The genera of hyphomycetes. CBS-KNAW Fungal Biodiversity Centre, Utrecht. 2011.