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. 2022 Aug 1;92:27–43. doi: 10.3897/mycokeys.92.86521

A new Arthrinium-like genus of Amphisphaeriales in China

Ning Jiang 1,✉, Hermann Voglmayr 2, Chun-Yan Ma 3, Han Xue 1, Chun-Gen Piao 1, Yong Li 1,✉
PMCID: PMC9849059  PMID: 36761316

Abstract

Species of Arthriniums. l. are usually known as endophytes, pathogens or saprobes occurring on various hosts and substrates and are characterised by globose to subglobose, sometimes irregular, dark brown and smooth-walled or finely verruculose conidia, always with a truncate basal scar. Currently, Arthriniums. l. contains two phylogenetically distinct clades, namely, Apiospora and Arthriniums. s. However, Arthriniumtrachycarpi and Ar.urticae have still not been properly classified. With new isolates from diseased leaves of Lithocarpusglaber collected in China, we propose the new Arthrinium-like genus Neoarthrinium in Amphisphaeriales. Based on the morphology and phylogeny of multiple loci, the new genus is established with the type species, N.lithocarpicola and three new combinations, N.moseri (syn. Wardomycesmoseri), N.trachycarpi (syn. Ar.trachycarpi) and N.urticae (syn. Ar.urticae) are added to this genus.

Keywords: Apiospora , Arthrinium , Neoarthrinium , phylogeny, taxonomy

Introduction

Apiosporaceae, including Arthrinium-like taxa, was proposed to accommodate genera with apiosporous hyaline ascospores and a basauxic, Arthrinium-like conidiogenesis (Hyde et al. 1998). In a recent outline of Sordariomycetes, Hyde et al. (2020) accepted five genera viz.Appendicospora, Arthrinium, Dictyoarthrinium, Endocalyx and Nigrospora in family Apiosporaceae. Soon thereafter, Dictyoarthrinium was transferred to Didymosphaeriaceae, based on a multigene phylogeny (Samarakoon et al. 2020). Subsequently, Pintos and Alvarado (2021) separated Apiospora from Arthrinium, based on the study of the type species of both genera and on multigene phylogeny. Recently, Konta et al. (2021) transferred Endocalyx toCainiaceae, based on morphological and phylogenetic evidence and Samarakoon et al. (2022) described the new family Appendicosporaceae forAppendicospora. Therefore, Apiosporaceae currently contains three genera, viz. Apiospora, Arthrinium and Nigrospora.

Until the study of Pintos and Alvarado (2021), the genera Apiospora and Arthrinium were considered synonymous, the first being used for the sexual morph and the second for the asexual morph in dual nomenclature (Réblová et al. 2016). Following the abandonment of dual nomenclature, the older name Arthrinium was recommended for use in unitary nomenclature (Réblová et al. 2016). The genus Arthrinium was proposed by Kunze and Schmidt (1817) and validated by Fries (1832) with Ar.caricicola as the generic type. Apiospora, the type genus of Apiosporaceae, was typified with Ap.montagnei, a new name for Sphaeriaapiospora (Saccardo 1875). However, the phylogenetic identity of Ap.montagnei has been confused because multiple names in Arthrinium have similar sexual morphs that have been referred to as Apiosporamontagnei (Hudson et al. 1976; Pintos et al. 2019; Pintos and Alvarado 2021). New collections from the original region and hosts (Arundo, Piptatherum) of Ap.montagnei have been isolated in pure culture and sequenced (Crous and Groenewald 2013; Pintos et al. 2019). Five species, previously placed in Arthrinium, are classified in Apiospora. Two of these phylogenetically distinct species, Ap.marii and Ap.phragmitis, are morphologically similar to Ap.montagnei (Pintos and Alvarado 2021), but due to a lack of sequence data from the type, it cannot be determined which of these two species should become a synonym of Ap.montagnei. Irrespective of these taxonomic uncertainties in species concept, recent multigene phylogenies revealed that Arthrinium and Apiospora represent two well-supported, distinct lineages close to Nigrospora in Apiosporaceae (Pintos and Alvarado 2021; Samarakoon et al. 2022). However, two Arthrinium species resembling Apiospora in conidial morphology, viz. Ar.trachycarpi and Ar.urticae, were not considered in these studies.

Arthrinium-like species are globally distributed, inhabiting various substrates, mainly associated with plant tissues as endophytes, pathogens and saprobes (Cooke 1954; Minter 1985; Larrondo and Calvo 1992; Senanayake et al. 2020; Feng et al. 2021; Jiang and Tian 2021; Tian et al. 2021). Some species are important plant pathogens; for example, Ap.arundinis causes bamboo brown culm streak, chestnut leaf spot and barley kernel blight (Martínez-Cano et al. 1992; Chen et al. 2014; Jiang et al. 2021), while Ap.sacchari causes damping-off of durum wheat (Mavragani et al. 2007). Another species, Ar.phaeospermum, can cause dermatomycosis in humans (Zhao et al. 1990).

In the present study, new Arthrinium-like isolates were collected and morphologically examined and their phylogenetic affiliation was determined by analyses of a combined matrix of ITS, LSU, tef1 and tub2 sequences. The aim of this study was to determine the phylogenetic placement of Ar.trachycarpi, Ar.urticae and our new isolates within Amphisphaeriales, which resulted in the identification of a new phylogenetic lineage with isolates belonging to neither Arthrinium nor Apiospora. As a result, a new genus is established for these isolates.

Materials and methods

Isolation and morphology

Diseased leaves of Lithocarpusglaber were observed and collected in Guangdong Province of China (39 m elevation; 23°8'52"N, 113°27'18"E), packed in paper bags and transferred to the laboratory for pure culture isolation. The samples were first surface-sterilised for 1 min in 75% ethanol, 3 min in 1.25% sodium hypochlorite and 1 min in 75% ethanol, rinsed for 2 min in distilled water and blotted on dry sterile filter paper. Then, the diseased areas of the leaves were cut into 0.5 × 0.5 cm pieces using an aseptic razor blade, transferred on to the surface of potato dextrose agar plates (PDA; 200 g potatoes, 20 g dextrose, 20 g agar per litre) and incubated at 25 °C to obtain pure cultures. The cultures were deposited in the China Forestry Culture Collection Center (CFCC; http://cfcc.caf.ac.cn/) and the specimen was deposited in the Herbarium of the Chinese Academy of Forestry (CAF; http://museum.caf.ac.cn/).

The morphology of the isolates was studied, based on sporulating axenic cultures grown on PDA in the dark at 25 °C. The conidiomata were observed and photographed under a dissecting microscope (M205 C, Leica, Wetzlar, Germany). The conidiogenous cells and conidia were immersed in tap water and then the microscopic photographs were captured with an Axio Imager 2 microscope (Zeiss, Oberkochen, Germany), equipped with an Axiocam 506 colour camera using differential interference contrast (DIC) illumination. For measurements, 50 conidiogenous cells and conidia were randomly selected. Culture characteristics were recorded from PDA after 10 d of incubation at 25 °C in the dark.

DNA extraction, PCR amplification and phylogenetic analyses

Genomic DNA was extracted from colonies grown on cellophane-covered PDA using a cetyltrimethylammonium bromide (CTAB) method (Doyle and Doyle 1990). DNA was checked by electrophoresis in a 1% agarose gel and the quality and quantity were measured using a NanoDrop 2000 (Thermo Scientific, Waltham, MA, USA). The following primer pairs were used for amplification of the gene regions sequenced in the present study: ITS1/ITS4 for the ITS1-5.8S-ITS2 nrDNA region (ITS) (White et al. 1990); LR0R/LR5 for the 28S nrDNA region (LSU) (Vilgalys and Hester 1990); EF1-728F/EF2 for the translation elongation factor 1-α (tef1) gene (O’Donnell and Cigelnik 1997; Carbone and Kohn 1999); Bt2a/Bt2b for the beta-tubulin (tub2) gene (Glass and Donaldson 1995). The PCR conditions were set as follows: an initial denaturation step of 5 min at 94 °C, followed by 35 cycles of 30 s at 94 °C, 50 s at 52 °C (ITS and LSU) or 54 °C (tef1 and tub2) and 1 min at 72 °C and a final elongation step of 7 min at 72 °C. The PCR products were assayed via electrophoresis in 2% agarose gels. DNA sequencing was performed using an ABI PRISM 3730XL DNA Analyser with a BigDye Terminator Kit v.3.1 (Invitrogen, USA) at the Shanghai Invitrogen Biological Technology Company Limited (Beijing, China).

The quality of the chromatograms obtained was checked and the nucleotide sequences were assembled using SeqMan v.7.1.0, the DNASTAR lasergene core suite software (DNASTAR Inc, Madison, WI, USA). Reference sequences were retrieved from the National Center for Biotechnology Information (NCBI; https://www.ncbi.nlm.nih.gov), based on related publications (Crous and Groenewald 2013; Wang et al. 2018; Liu et al. 2019; Pintos and Alvarado 2021; Samarakoon et al. 2022). Sequences were aligned using MAFFT v. 6 (Katoh and Toh 2010) and corrected manually using MEGA 7.0.21 (Kumar et al. 2016).

The phylogenetic analyses of the combined loci were performed using Maximum Likelihood (ML) and Bayesian Inference (BI) methods. The ML was implemented on the CIPRES Science Gateway portal (https://www.phylo.org) using RAxML-HPC BlackBox 8.2.10 (Stamatakis 2014), employing a GTRGAMMA substitution model with 1000 bootstrap replicates. The Bayesian posterior probabilities (BPP) were determined by Markov Chain Monte Carlo (MCMC) sampling in MrBayes v. 3.2.6 (Ronquist et al. 2012). The six simultaneous Markov chains were run for 1 M generations, starting from random trees and sampling trees every 100th generation and 25% of aging samples were discarded, running until the average standard deviation of the split frequencies dropped below 0.01. The phylogram was visualised in FigTree v.1.3.1 (http://tree.bio.ed.ac.uk/software) and edited in Adobe Illustrator CS5 (Adobe Systems Inc., USA). The newly-generated nucleotide sequences were deposited in GenBank (Table 1).

Table 1.

Isolates and GenBank accession numbers used in the phylogenetic analyses.

Species Strain Host Origin GenBank accession numbers
ITS LSU tub2 tef1
Allelochaetaacuta CPC 16629 Eucalyptusdives Australia MH554086 MH554297 MH554758 MH554519
Allelochaetaneoacuta CBS 115131 Eucalyptussmithii South Africa JN871200 JN871209 MH704627 MH704602
Amphisphaeriamicheliae MFLUCC 20-0121 Micheliaalba China MT756626 MT756620 MT774371 NA
Apiosporaacutiapica KUMCC 20-0209 Bambusabambos China MT946342 MT946338 MT947365 MT947359
Apiosporaacutiapica KUMCC 20-0210 Bambusabambos China MT946343 MT946339 MT947366 MT947360
Apiosporaarundinis CBS 114316 Hordeumvulgare Iran KF144884 KF144928 KF144974 KF145016
Apiosporaaurea CBS 244.83 Air Spain AB220251 KF144935 KF144981 KF145023
Apiosporabalearica CBS 145129 Poaceae Spain MK014869 MK014836 MK017975 NA
Apiosporabiserialis CGMCC 3.20135 Bamboo China MW481708 MW478885 MW522955 MW522938
Apiosporacamelliae-sinensis LC8181 Brassicacampestris China KY494761 KY494837 KY705229 NA
Apiosporacamelliae-sinensis CGMCC 3.18333 Camelliasinensis China KY494704 KY494780 KY705173 KY705103
Apiosporacyclobalanopsidis CGMCC 3.20136 Cyclobalanopsisglauca China MW481713 MW478892 MW522962 MW522945
Apiosporadescalsii CBS 145130 Ampelodesmosmauritanicus Spain MK014870 MK014837 MK017976 NA
Apiosporadichotomanthi LC8175 Dichotomanthestristaniiaecarpa China KY494755 KY494831 KY705223 KY705151
Apiosporadichotomanthi CGMCC 3.18332 Dichotomanthestristaniiaecarpa China KY494697 KY494773 KY705167 KY705096
Apiosporaesporlensis CBS 145136 Phyllostachysaurea Spain MK014878 MK014845 MK017983 NA
Apiosporagelatinosa GZAAS 20-0107 Bamboo China MW481707 MW478889 MW522959 MW522942
Apiosporaguizhouensis LC5318 Air China KY494708 KY494784 KY705177 KY705107
Apiosporaguizhouensis CGMCC 3.18334 Air China KY494709 KY494785 KY705178 KY705108
Apiosporahydei CBS 114990 Bamboo China KF144890 KF144936 KF144982 KF145024
Apiosporaiberica CBS 145137 Arundodonax Portugal MK014879 MK014846 MK017984 NA
Apiosporaintestini CBS 135835 Gut of a grasshopper India KR011352 MH877577 KR011350 NA
Apiosporaitalica CBS 145138 Arundodonax Italy MK014880 MK014847 MK017985 NA
Apiosporajiangxiensis CGMCC 3.18381 Maesa sp. China KY494693 KY494769 KY705163 KY705092
Apiosporakogelbergensis CBS 113332 Cannomoisvirgata South Africa KF144891 KF144937 KF144983 KF145025
Apiosporakogelbergensis CBS 113333 Restionaceae South Africa KF144892 KF144938 KF144984 KF145026
Apiosporamalaysiana CBS 102053 Macarangahullettii Malaysia KF144896 KF144942 KF144988 KF145030
Apiosporamarii CBS 497.90 Air Spain AB220252 KF144947 KF144993 KF145035
Apiosporaneobambusae CGMCC 3.18335 Bamboo China KY494718 KY494794 KY705186 KY806204
Apiosporaneobambusae LC7107 Bamboo China KY494719 KY494795 KY705187 KY705117
Apiosporaobovata CGMCC 3.18331 Lithocarpus sp. China KY494696 KY494772 KY705166 KY705095
Apiosporaobovata LC8177 Lithocarpus sp. China KY494757 KY494833 KY705225 KY705153
Apiosporaovata CBS 115042 Arundinariahindsii China KF144903 KF144950 KF144995 KF145037
Apiosporaphragmitis CBS 135458 Phragmitesaustralis Italy KF144909 KF144956 KF145001 KF145043
Apiosporaphyllostachydis MFLUCC 18-1101 Phyllostachysheteroclada China MK351842 MH368077 MK291949 MK340918
Apiosporapseudoparenchymatica CGMCC 3.18336 Bamboo China KY494743 KY494819 KY705211 KY705139
Apiosporapseudospegazzinii CBS 102052 Macarangahullettii Malaysia KF144911 KF144958 KF145002 KF145045
Apiosporapterosperma CBS 134000 Machaerinasinclairii Australia KF144913 KF144960 KF145004 KF145046
Apiosporasaccharicola CBS 191.73 Air Netherlands KF144920 KF144966 KF145009 KF145051
Apiosporaseptata CGMCC 3.20134 Bamboo China MW481711 MW478890 MW522960 MW522943
Apiosporaserenensis IMI 326869 NA Spain AB220250 AB220344 AB220297 NA
Apiosporasubrosea LC7291 Bamboo China KY494751 KY494827 KY705219 KY705147
Apiosporasubrosea CGMCC 3.18337 Bamboo China KY494752 KY494828 KY705220 KY705148
Apiosporaxenocordella CBS 595.66 Soil Austria KF144926 KF144971 KF145013 KF145055
Arthriniumcaricicola CBS 145127 Carexericetorum Germany MK014871 MK014838 MK017977 NA
Arthriniumcrenatum CBS 146353 Grass France MW208931 MW208861 MW221923 MW221917
Arthriniumcurvatum CBS 145131 Carex sp. Germany MK014872 MK014839 MK017978 NA
Arthriniumjaponicum IFO 30500 Carexdespalata Japan AB220262 AB220356 AB220309 NA
Arthriniumjaponicum IFO 31098 Carexdespalata Japan AB220264 AB220358 AB220311 NA
Arthriniumluzulae AP7619-3 Luzulasylvatica Spain MW208937 MW208863 MW221925 MW221919
Arthriniummorthieri GZU 345043 Carexdigitata Austria MW208938 MW208864 MW221926 MW221920
Arthriniumpuccinioides CBS 549.86 Lepidospermagladiatum Germany AB220253 AB220347 AB220300 NA
Arthriniumsphaerospermum CBS 146355 Poaceae Norway MW208943 MW208865 NA NA
Arthriniumsporophleum CBS 145154 Juncus sp. Spain MK014898 MK014865 MK018001 NA
Bartaliniabella CBS 125525 Maytenusabbottii South Africa GU291796 MH554214 MH554663 MH554421
Bartaliniapini CBS 143891 Pinuspatula Uganda MH554125 MH554330 MH554797 MH554559
Beltraniapseudorhombica CBS 138003 Pinustabulaeformis China MH554124 KJ869215 NA MH554558
Beltraniarhombica CBS 123.58 Sand near mangrove swamp Mozambique MH553990 MH554209 MH704631 MH704606
Beltraniopsisneolitseae CPC 22168 Neolitseaaustraliensis Australia KJ869126 KJ869183 NA NA
Broomellavitalbae HPC 1154 NA NA MH554173 MH554367 MH554846 MH554608
Castanediellacagnizarii CBS 542.96 Leaf litter Cuba MH862597 MH874222 NA NA
Ciliochorellaphanericola MFLUCC 12-0310 Dead leaves Thailand KF827444 KF827445 KF827478 KF827477
Clypeophysalosporalatitans CBS 141463 Eucalyptus sp. Portugal NR_153929 NG_058958 NA NA
Clypeosphaeriamamillana CBS 140735 Cornusalba France KT949897 MH554225 MH704637 MH704610
Cylindriumelongatum CBS 115974 Fagus sp. The Netherlands KM231853 KM231733 KM232123 KM231989
Diplocerashypericinum CBS 109058 Hypericum sp. New Zealand MH553955 MH554178 MH554614 MH554373
Disaetaarbuti CBS 143903 Acaciapycnantha Australia MH554148 MH554346 MH554821 MH554583
Discosiaartocreas CBS 124848 Fagussylvatica Germany MH553994 MH554213 MH554662 MH554420
Discosiabrasiliensis MFLUCC 12-0429 Dead leaf Thailand KF827432 KF827436 KF827469 KF827465
Distononappendiculatabanksiae CBS 131308 Banksiamarginata Australia JQ044422 JQ044442 MH554670 MH554428
Distononappendiculatacasuarinae CBS 143884 Casuarina sp. Australia MH554093 MH554303 MH554766 MH554527
Diversimediisporahumicola CBS 302.86 Soil USA MH554028 MH554247 MH554705 MH554463
Heterotruncatellaacacigena CBS 143880 Acaciapedina Australia MH554084 MH554295 MH554756 MH554517
Heterotruncatellaaspera CBS 144140 Acaciaglaucoptera Australia MH554156 MH554352 MH554829 MH554591
Hyalotiellaspartii MFLUCC 13-0397 Spartiumjunceum Italy KP757756 KP757752 NA NA
Hyalotiellatransvalensis CBS 303.65 Leaf litter and topsoil of Acaciakarroo community South Africa MH554029 MH554248 MH554706 MH554464
Hymenopleellaaustroafricana CBS 143886 Gleditsiatriacanthos South Africa MH554115 MH554320 MH554788 MH554549
Hymenopleella hippophaëicola CBS 113687 Hippophaë rhamnoides Sweden MH553969 MH554188 MH554628 MH554387
Immersidiscosiaeucalypti NBRC 104195 Quercusmyrsinifolia Japan AB594790 AB593722 NA NA
Lepteutypafuckelii CBS 140409 Tiliacordata Belgium NR_154123 KT949902 MH554677 MH554435
Lepteutypasambuci CBS 131707 Sambucusnigra UK NR_154124 MH554219 MH704632 MH704612
Monochaetiamonochaeta CBS 115004 Quercusrobur Netherlands AY853243 MH554198 MH554639 MH554398
Monochaetiaquercus CBS 144034 Quercuseduardi Mexico MH554171 MH554365 MH554844 MH554606
Moriniaacaciae CBS 137994 Acaciamelanoxylon France MH554002 MH554221 MH554673 MH554431
Moriniacrini CBS 143888 Crinumbulbispermum South Africa MH554118 MH554323 MH554791 MH554552
Neoarthriniumlithocarpicola CFCC 54456 Lithocarpusglaber China ON427580 ON427582 ON456914 NA
Neoarthriniumlithocarpicola CFCC 55883 Lithocarpusglaber China ON427581 ON427583 ON456915 NA
Noarthriniummoseri CBS 164.80 Dead petiole Colombia LN850995 LN851049 LN851154 NA
Neoarthriniumtrachycarpi CFCC 53038 Trachycarpusfortunei China MK301098 NA MK303394 MK303396
Neoarthriniumtrachycarpi CFCC 53039 Trachycarpusfortunei China MK301099 NA MK303395 MK303397
Neoarthriniumurticae IMI 326344 Leaf litter India AB220245 AB220339 NA NA
Neopestalotiopsiscubana CBS 600.96 Leaf litter Cuba KM199347 KM116253 KM199438 KM199521
Neophysalosporaeucalypti CBS 138864 Corymbiahenryi Mozambique KP004462 MH878627 NA NA
Nigrosporaaurantiaca CGMCC 3.18130 Nelumbo sp. China KX986064 KX986098 KY019465 KY019295
Nigrosporacamelliae-sinensis CGMCC 3.18125 Camelliasinensis China KX985986 KX986103 KY019460 KY019293
Nigrosporachinensis CGMCC 3.18127 Machilusbreviflora China KX986023 KX986107 KY019462 KY019422
Nigrosporagorlenkoana CBS 480.73 Vitisvinifera Kazakhstan KX986048 KX986109 KY019456 KY019420
Nigrosporaguilinensis CGMCC 3.18124 Camelliasinensis China KX985983 KX986113 KY019459 KY019292
Nigrosporahainanensis CGMCC 3.18129 Musaparadisiaca China KX986091 KX986112 KY019464 KY019415
Nigrosporalacticolonia CGMCC 3.18123 Camelliasinensis China KX985978 KX986105 KY019458 KY019291
Nigrosporamusae CBS 319.34 Musa sp. Australia MH855545 KX986110 KY019455 KY019419
Nigrosporaoryzae LC2693 Neolitsea sp. China KX985944 KX986101 KY019471 KY019299
Nigrosporaosmanthi CGMCC 3.18126 Osmanthus sp. China KX986010 KX986106 KY019461 KY019421
Nigrosporapyriformis CGMCC 3.18122 Citrussinensis China KX985940 KX986100 KY019457 KY019290
Nigrosporarubi LC2698 Rubus sp. China KX985948 KX986102 KY019475 KY019302
Nigrosporasphaerica LC7298 Nelumbo sp. China KX985937 KX986097 KY019606 KY019401
Nigrosporavesicularis CGMCC 3.18128 Musaparadisiaca China KX986088 KX986099 KY019463 KY019294
Nonappendiculataquercina CBS 116061 Quercussuber Italy MH553982 MH554199 MH554641 MH554400
Parabartalinialateralis CBS 399.71 Acaciakarroo South Africa MH554043 MH554256 MH554719 MH554478
Parapleurotheciopsisinaequiseptata MUCL 41089 Rotten leaf Brazil EU040235 EU040235 NA NA
Parapleurotheciopsiscaespitosa CBS 519.93 Syzygiumcordatum South Africa MH862437 NG_066263 NA NA
Pestalotiopsisadusta CBS 263.33 Rhododendronponticum Netherlands KM199316 KM116198 KM199414 KM199489
Pestalotiopsisaustralasiae CBS 114126 Knightia sp. New Zealand KM199297 KM116218 KM199409 KM199499
Phlogicylindriumeucalypti CBS 120080 Eucalyptusglobulus Australia NR_132813 DQ923534 MH704633 MH704607
Phlogicylindriumeucalyptorum CBS 120221 Eucalyptusglobus Australia EU040223 MH554204 MH704635 MH704608
Pseudopestalotiopsisampullacea LC6618 Camelliasinensis China KX895025 KX895039 KX895358 KX895244
Pseudopestalotiopsiscamelliae-sinensis LC3009 Camelliasinensis China KX894935 KX895050 KX895267 KX895152
Pseudosarcostromaosyridicola CBS 103.76 Osyrisalba France MH553954 MH554177 MH554613 MH554372
Pseudosporidesmiumknawiae CBS 123529 NA NA MH863299 MH874823 NA NA
Robillardaafricana CBS 122.75 NA South Africa KR873253 KR873281 MH554656 MH554414
Robillardaterrae CBS 587.71 Soil India KJ710484 KJ710459 MH554734 MH554493
Sarcostromaafricanum CBS 143879 Pelargoniumcucullatum South Africa MH554078 MH554289 MH554752 MH554513
Sarcostromaaustraliense CBS 144160 Daviesialatifolia Australia MH554138 MH554340 MH554811 MH554573
Seimatosporiumgermanicum CBS 437.87 NA Germany MH554047 MH554259 MH554723 MH554482
Seimatosporiumluteosporum CBS 142599 Vitisvinifera USA KY706284 KY706309 KY706259 KY706334
Seiridiumcancrinum CBS 226.55 Cupressusmacrocarpa Kenya LT853089 MH554241 LT853236 LT853186
Seiridiumcupressi CBS 224.55 Cupressusmacrocarpa Kenya LT853083 MH554240 LT853230 LT853180
Sporocadusbiseptatus CBS 110324 NA NA MH553956 MH554179 MH554615 MH554374
Sporocaduscornicola CBS 143889 Cornussanguinea Germany MH554121 MH554326 MH554794 MH554555
Sporocadustrimorphus CBS 114203 Rosacanina Sweden MH553977 MH554196 MH554636 MH554395
Strickeriakochii CBS 140411 Robiniapseudoacacia Austria NR_154423 KT949918 MH554679 MH554437
Subramaniomycesfusisaprophyticus CBS 418.95 Leaf litter Cuba EU040241 EU040241 NA NA
Synnemapestaloidesjuniperi CBS 477.77 Juniperusphoenicea France MH554053 MH554266 MH554729 MH554488
Truncatellaangustata CBS 113.11 Piceaabies Germany MH553966 MH554185 MH554625 MH554384
Xenoseimatosporiumquercinum CBS 129171 Rhododendron sp. Latvia MH553997 MH554216 MH554666 MH554424
Xyladictyochaetalusitanica CBS 143502 Eucalyptus sp. Australia MH107926 MH107972 MH108053 MH108033
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Note: NA, not applicable. Strains in this study are marked in bold.

Results

Phylogenetic analyses

The combined sequence dataset (ITS, LSU, tef1 and tub2) was analysed to infer the phylogenetic placement of our new isolates within Amphisphaeriales. The dataset consisted of 136 sequences, including two outgroup taxa, Clypeosphaeriamamillana (CBS 140735) and Pseudosporidesmiumknawiae (CBS 123529). A total of 3526 characters, including gaps (793 for ITS, 859 for LSU, 762 for tef1 and 1112 for tub2), were included in the phylogenetic analysis. Of these characters, 1543 were constant, 284 were variable, but parsimony-uninformative and 1699 were parsimony-informative. The best ML tree (lnL = - 72640.48) revealed by RAxML is shown in Fig. 1. The topologies resulting from ML and BI analyses of the concatenated dataset were congruent (Fig. 1). Isolates CFCC 54456 and CFCC 55883 from the present study, together with CFCC 53038, CFCC 53039, CBS 164.80 and IMI 326344, formed a clade distinct from Apiosporaceae and the other families in Amphisphaeriales. Hence, a new genus named Neoarthrinium is proposed herein for this clade. Arthriniumtrachycarpi, Ar.urticae and Wardomycesmoseri are transferred to Neoarthrinium. In addition, the two new isolates (CFCC 54456 and CFCC 55883) that form a sister clade to N.moseri, N.trachycarpi and N.urticae are described here as the new species N.lithocarpicola.

Figure 1.

Figure 1.

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Phylogram of Amphisphaeriales resulting from a Maximum Likelihood analysis, based on a combined matrix of ITS, LSU, tef1 and tub2. Numbers above the branches indicate ML bootstraps (left, ML BS ≥ 50%) and Bayesian Posterior Probabilities (right, BPP ≥ 0.90). The tree is rooted with Clypeosphaeriamamillana (CBS 140735) and Pseudosporidesmiumknawiae (CBS 123529). New species and combinations proposed in the present study are marked in blue.

Taxonomy

. Neoarthrinium

Ning Jiang gen. nov.

0F22D7F7-D920-516B-90DB-F1A07FFDFA3C

843845

Etymology.

Named after its morphological similarity to Arthrinium.

Type species.

Neoarthriniumlithocarpicola Ning Jiang

Description.

Hyphae formed on PDA hyaline, branched, septate. Asexual morph: Conidiophores cylindrical, septate, verrucose, flexuous, sometimes reduced to conidiogenous cells. Conidiogenous cells erect, blastic, aggregated in clusters on hyphae, hyaline to pale brown, smooth, doliiform, subglobose to lageniform, branched. Conidia brown to dark brown, smooth to finely roughened, subglobose, ellipsoid to lenticular, with a longitudinal germ slit, occasionally elongated to ellipsoidal. Sexual morph: Undetermined.

. Neoarthrinium lithocarpicola

Ning Jiang sp. nov.

080D8973-BDAF-5A96-AB80-82D4041D2664

843846

Fig. 2

Figure 2.

Figure 2.

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NeoarthriniumlithocarpicolaA colony on PDAB conidiomata formed in culture C–F conidiogenous cells giving rise to conidia G–I conidia. Scale bars: 500 μm (B), 10 μm (C–I).

Etymology.

Named for its host genus “Lithocarpus” and “-cola” = inhabiting.

Description.

Hyphae 1.5–4.5 μm diam., hyaline, branched, septate. Asexual morph: Conidiophores cylindrical, septate, verrucose, flexuous, sometimes reduced to conidiogenous cells. Conidiogenous cells erect, blastic, aggregated in clusters on hyphae, hyaline to pale brown, smooth, globose to subglobose, branched, (4–)5.5–8 × 2.5–3.5(–4) μm, mean ± SD = 6.6 ± 1.3 × 3.1 ± 0.4 μm, n = 50. Conidia brown to dark brown, smooth to finely roughened, subglobose to lenticular, with a longitudinal germ slit, occasionally elongated to ellipsoidal, (5–)6–8(–8.5) × (4.5–)5–5.5(–6) μm, mean ± SD = 7 ± 0.8 × 5.3 ± 0.5 μm, L/W = 1.1–1.8, n = 50. Sexual morph: Undetermined.

Culture characters.

Colonies on PDA flat, spreading, with flocculent aerial mycelium forming concentric rings, edge entire, mouse grey to greyish-green, reaching 60 mm diam. after 10 d at 25 °C, forming abundant conidiomata.

Specimens examined.

China. Guangdong Province, Guangzhou City, on leaf spots of Lithocarpusglaber (Thunb.) Nakai, Shang Sun (holotype CAF800050 = JNH0046; ex-type living culture: CFCC 54456; other living culture: CFCC 55883).

Notes.

Two isolates of Neoarthriniumlithocarpicola from Lithocarpusglaber (Thunb.) Nakai formed a well-supported monophyletic clade, distinct from N.moseri, N.trachycarpi and N.urticae (Fig. 1). Morphologically, N.lithocarpicola is distinguished from N.moseri in smaller conidia (5–8.5 × 4.5–6 µm in N.lithocarpicola vs. 10–14 × 3–4.5 µm in N.moseri; Gams 1995). Neoarthriniumlithocarpicola is different from N.urticae by lacking thick blackish septa in conidiophores (Ellis 1965). Neoarthriniumlithocarpicola is similar to N.trachycarpi in the size of its conidiogenous cells and conidia, but it can be distinguished by its globose to subglobose conidiogenous cells (Yan et al. 2019).

. Neoarthrinium moseri

(W. Gams) Voglmayr comb. nov.

F199C77A-6306-51CB-A79A-84705D6FABDA

844772

Basionym.

Wardomycesmoseri W. Gams, Beih. Sydowia 10: 67 (1995)

Notes.

Based on a placement within Xylariales in phylogenetic analyses, Sandoval-Denis et al. (2016) excluded this species from the genus (Microascales); however, they did not suggest an alternative generic classification. The blastic hyaline, smooth, lageniform conidiogenous cells aggregated in clusters and the subglobose to ellipsoid dark brown conidia with a longitudinal germ slit (Gams 1995) fully matched the genus Neoarthrinum. The ITS, LSU and tub2 sequences of the ex-holotype strain of N.moseri (CBS 164.80) are almost identical to those of N.trachycarpi, indicating that they may be synonymous. Both species were isolated from petioles of palms: N.moseri from Mauritiaminor Burret in Colombia and N.trachycarpi from Trachycarpusfortunei (Hook.) H.Wendl. in China. However, the two species were reported to differ in conidial size (10–14 × 3–4.5 µm in N.moseri vs. 6.1–8.5 × 4.2–5.8 μm in N.trachycarpi; Gams 1995; Yan et al. 2019) and for the time being, we therefore kept them separate.

. Neoarthrinium trachycarpi

(C.M. Tian & H. Yan) Ning Jiang comb. nov.

FDA9EAE0-58E6-5223-B458-E47E1D6B83C2

843847

Basionym.

Arthriniumtrachycarpi C.M. Tian & H. Yan [as ‘trachycarpum’], Phytotaxa 400(3): 208 (2019)

. Neoarthrinium urticae

(M.B. Ellis) Ning Jiang comb. nov.

AC635989-1929-5909-8FE9-29C2E571041F

843848

Basionym.

Arthriniumurticae M.B. Ellis, Mycol. Pap. 103: 16 (1965)

Notes.

The possibility that Apiosporellaurticae (Rehm) Höhn. is the sexual morph of Arthriniumurticae is raised by the fact that both share the same host (Urtica) and are classified as members of the Apiosporaceae (Index Fungorum, accessed 4 July 2022). This evidence would have far reaching nomenclatural consequences not only for species, but also for generic classification, as Apiosporella (Höhnel 1909) may then qualify for an older genus name to be used for Neoarthrinium. However, according to L. Holm, the holotype specimen of its basionym, Apiosporaurticae (S-F12119), represents a very different fungus, Didymellaeupyrena (Didymellaceae, Pleosporales, Dothideomycetes; https://herbarium.nrm.se/specimens/F12119, accessed 4 July 2022). The status of the genus Apiosporella is still unclear because Höhnel (1909) did not choose a type from the six different species included in the genus. However, none of the original species is a close relative of Apiosporaceae or Neoarthrinium; therefore, Apiosporella should be excluded from Apiosporaceae.

No sequence data are available for isolates from the type host Urticadioica L. (Urticaceae). The single culture sequenced (IMI 326344) was isolated from unidentified leaf litter collected in India. Additional molecular studies on verified isolates from Urtica collected in Europe are necessary to reveal whether IMI 326344 represents true N.urticae. However, N.urticae appears to be very rare and we are unaware of any additional collections with the exception of the type.

Discussion

Arthrinium and related genera are important fungal taxa whose concepts and classification have undergone many changes and additions (e.g. Cooke 1954; Samuels et al. 1981; Larrondo and Calvo 1990; Hyde et al. 1998; Jaklitsch and Voglmayr 2012; Crous and Groenewald 2013; Singh et al. 2013; Sharma et al. 2014; Dai et al. 2016, 2017; Hyde et al. 2016; Jiang et al. 2018, 2020; Wang et al. 2018; Pintos et al. 2019; Pintos and Alvarado 2021). In recent years, substantial changes in classification were implemented in the course of unitary nomenclature. A large number of newly-discovered species have been described as a result of extensive sampling of new isolates, based on multigene phylogenies (e.g. Crous and Groenewald 2013; Wang et al. 2018; Pintos and Alvarado 2021). Currently, Arthrinium-like asexual morphs are shared by three distinct lineages within Amphisphaeriales, viz. Apiospora, Arthriniums. s. and Neoarthrinium as shown in Fig. 1. Arthriniums. s. is the sister genus to Nigrospora, which morphologically differs from Apiospora, Arthrinium and Neoarthrinium in conidial ontogeny (Wang et al. 2017). The phylogram shown in Fig. 1 is consistent with that shown in Tian et al. (2021) in placing Apiospora, Arthrinium and Nigrospora within a clade that is distinct from the new genus Neoarthrinium, although Apiospora and Arthrinium share conidial morphology similar to that of Neoarthrinium.

Morphologically, Apiospora, Arthrinium and Neoarthrinium are similar in having basauxic conidiogenesis. Conidia of Apiospora and Neoarthrinium are generally more or less rounded in face view and lenticular in side view, while those of Arthrinium are variously shaped, viz. globose, angular, polygonal, curved, fusiform or navicular (Yan et al. 2019; Pintos and Alvarado 2021). However, the conidiophores of several Arthrinium and Neoarthrinium species have thick blackish septa, which are rarely observed in Apiospora (Ellis 1965; Wang et al. 2018; Pintos and Alvarado 2021). Hence, these three genera are difficult to distinguish by only asexual morphology.

Regarding their hosts, there are some tendencies in host preferences, while Arthrinium species are predominantly found in Cyperaceae and Juncaceae (Pintos and Alvarado 2021) and species of Apiospora primarily occur on Poaceae (but also on many other hosts; Wang et al. 2018). Four Neoarthrinium species were discovered on four hosts from three distantly-related host families (i.e. N.lithocarpicola from Lithocarpusglaber (Thunb.) Nakai, Fagaceae; N.moseri from Mauritiaminor Burret, Arecaceae; N.trachycarpi from Trachycarpusfortune (Hook.) H.Wendl., Arecaceae; and N.urticae from Urticadioica L., Urticaceae; Ellis 1965; Yan et al. 2019). Hence, host association is not a fully reliable feature to distinguish Apiospora, Arthrinium and Neoarthrinium.

Compared to species, generic delimitation is much more subjective. However, there is a broad agreement that genera, along with all taxonomic classification units at all ranks, should be monophyletic. As morphology is frequently insufficient for phylogenetic classification, molecular evidence is regarded as significant data or even an essential characteristic in the classification and identification of fungal taxa. In the present study, Neoarthrinium is proposed as a new genus for a group of species phylogenetically distinct from Apiospora, Arthrinium and Nigrospora to maintain monophyletic Arthrinium-like genera. Using morphological and phylogenetic data, however, we need more samples to improve our understanding of Arthrinium-like taxa and genera in the Amphisphaeriales.

Supplementary Material

XML Treatment for Neoarthrinium
XML Treatment for Neoarthrinium lithocarpicola
XML Treatment for Neoarthrinium moseri
XML Treatment for Neoarthrinium trachycarpi
XML Treatment for Neoarthrinium urticae

Acknowledgements

This research was funded by the National Microbial Resource Center of the Ministry of Science and Technology of the People’s Republic of China (NMRC-2021-7). The three anonymous reviewers are also acknowledged for their useful comments.

Citation

Jiang N, Voglmayr H, Ma C-Y, Xue H, Piao C-G, Li Y (2022) A new Arthrinium-like genus of Amphisphaeriales in China. MycoKeys 92: 27–43. https://doi.org/10.3897/mycokeys.92.86521

Funding Statement

National Microbial Resource Center of the Ministry of Science and Technology of the People’s Republic of China (NMRC-2021-7).

Contributor Information

Ning Jiang, Email: n.jiang@caf.ac.cn.

Yong Li, Email: lylx@caf.ac.cn.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

XML Treatment for Neoarthrinium
mycokeys.92.86521-treatment1.xml (3.7KB, xml)
XML Treatment for Neoarthrinium lithocarpicola
mycokeys.92.86521-treatment2.xml (14.5KB, xml)
XML Treatment for Neoarthrinium moseri
mycokeys.92.86521-treatment3.xml (9.5KB, xml)
XML Treatment for Neoarthrinium trachycarpi
mycokeys.92.86521-treatment4.xml (3KB, xml)
XML Treatment for Neoarthrinium urticae
mycokeys.92.86521-treatment5.xml (8.3KB, xml)

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