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Six new species of Arthrinium from Europe and notes about A. caricicola and other species found in Carex spp. hosts
expand article infoÁngel Pintos, Pablo Alvarado§, Juan Planas|, Rene Jarling
‡ Departamento de Investigación Mycologica, Palma de Mallorca, Spain
§ ALVALAB, Santander, Spain
| Unaffiliated, Palma de Mallorca, Spain
Open Access

Abstract

Several new Arthrinium specimens were collected from various locations in Mediterranean and temperate Europe. A collection of the type species, A. caricicola, was obtained from dead leaves of Carex ericetorum in Berlin. Sequences of four genetic markers, ITS, 28S rDNA, tef1 and tub2 were produced from almost all collections and analyzed with those available in public databases. Results are employed to support six new species: A. balearicum, A. descalsii, A. esporlense, A. ibericum, A. italicum and A. piptatheri. The type species, A. caricicola, is related to other species occurring on Carex sp.; these might represent an independent lineage from Apiospora and the remaining species of Arthrinium. Finally, the sexual morph of A. marii is described and illustrated for the first time.

Keywords

Apiosporaceae, Ascomycota, Sordariomycetes, Xylariales, ITS, 28S rDNA, tef1, tub2

Introduction

The genus Arthrinium Kunze (Apiosporaceae, Sordariomycetes) differs from other anamorphic genera because of the presence of basauxic conidiophores, which arise from structures called conidiophore mother cells (Schmidt and Kunze 1817; Hughes 1953; Minter 1985). This infrequent type of conidiogenesis can be found also in Cordella Speg., Dictyoarthrinium S. Hughes, Pteroconium Sacc. ex Grove, and Spegazzinia Sacc. (Ellis 1971), but Pteroconium and Cordella are now considered synonyms of Athrinium (Seifert et al. 2011; Crous and Groenewald 2013). Apiospora Sacc., the sexual state of Arthrinium, is also considered a synonym based on the one fungus-one name policy (Hawksworth et al. 2011; Crous and Groenewald 2013), and Nigrospora Zimm. is thought to be the closest relative (Wang et al. 2017).

There are about 80 valid species names of Arthrinium. The most significant contributions to species diversity of Arthrinium before the DNA-era were those of Schmidt and Kunze (1817), Kunze and Schmidt (1823), Fuckel (1870, 1874), Ellis (1963, 1965, 1971, 1976), and Larrondo and Calvo (1990, 1992). Genetic evidence allowed to confirm some of these taxa and propose multiple new species, e.g. Crous and Groenewald (2013), Singh et al. (2013), Dai et al. (2016, 2017), Jiang et al. (2018), and Wang et al. (2018). Smith et al. (2003) produced the first genetic data (18S and 28S rDNA) of A. phaeospermum (Corda) M.B. Ellis, supporting that this genus, as well as Apiospora, represent a separate family within Xylariales. This was later confirmed by Spatafora et al. (2006) and Zhang et al. (2006) who added new information from gene-coding DNA markers (18S and 28S rDNA, tef1, rpb2). Singh et al. (2013) published a ITS rDNA phylogeny including several type sequences obtained by Ogawa et al. (unpublished), such as those of A. marii Larrondo & Calvo, A. hispanicum Larrondo & Calvo, A. mediterranei Larrondo & Calvo, A. serenense Larrondo & Calvo, and A. phaeospermum, and introduced the new species A. rasikravindrae Shiv M. Singh, L.S. Yadav, P.N. Singh, Rah. Sharma & S.K. Singh (as rasikravindrii). Soon afterwards, Crous and Groenewald (2013) published a comprehensive re-evaluation of Arthrinium based on multigenic data, introducing eight new species and providing genetic data from several type strains of other taxa. They formally proposed the synonymy between Arthrinium and Apiospora, giving priority to Arthrinium, but provided no data of the type species, A. caricicola Kunze & J.C. Schmidt. Sharma et al. (2014) published the new species A. jatrophae R. Sharma, G. Kulk. & Shouche and built a phylogenetic tree based on rDNA that showed three main clades: one formed by A. urticae M.B. Ellis, a second including A. puccinioides Kunze & J.C. Schmidt and A. japonicum Pollack & C.R. Benj., and a third including the remaining known species of Arthrinium and Apiospora. Multigenic data of the first two clades was first obtained by Ogawa et al. (unpublished), and also Crous and Groenewald (2013), although they did not include these data in their phylogenetic analyses. Some new species of Arthrinium were described in the next years (Crous et al. 2015; Senanayake et al. 2015; Hyde et al. 2016; Dai et al. 2016, 2017; Wang et al. 2018; Jiang et al. 2018), and the multilocus phylogenetic analysis revealed that the sister clade of Arthrinium was Nigrospora in Apiosporaceae (Wang et al. 2017).

Morphological features traditionally employed to discriminate between species of Arthrinium include conidial shape, conidiophores, presence or absence of sterile cells and the presence of setae. Two great groups of species can be discriminated: 1) those with irregularly shaped conidia (including the type species A. cariciola and several others mainly associated with Carex spp. (Cyperaceae, Poales), such as A. austriacum Petr., A. fuckelii Gjaerum, A. globosum Koskela, A. japonicum, A. kamtschaticum Tranzschel & Woron., A. morthieri Fuckel, A. muelleri M.B. Ellis, A. naviculare Rostr., A. puccinioides and A. sporophleum Kunze), and 2) the remaining species with globose to ellipsoid conidia, mainly associated with other plants in the Poales (Cyperaceae, Poaceae, Restionaceae), e.g. A. pterospermum (Cooke & Massee) Arx, A. phragmitis Crous, A. sacchari (Speg.) M.B. Ellis, A. saccharicola F. Stevens, A. kogelbergense Crous, and A. hysterinum (Sacc.) P.M. Kirk, or even a wider diversity of potential hosts, such as A. arundinis (Corda) Dyko & B. Sutton, A. phaeospermum, A. rasikravindrae and A. malaysianum Crous.

Spatafora et al. (2006) and Zhang et al. (2006) were the first to obtain genetic data from the type species of Apiospora, Ap. montagnei Sacc. (CBS 212.30, AFTOL-ID 951) and suggested that it belongs in a distinct family within Xylariales. Sequences of a few other species of Apiospora are also available, including Ap. sinensis K.D. Hyde, J. Fröhl. & Joanne E. Taylor (HKUCC 3143 in Smith et al. 2003), Ap. setosa Samuels, McKenzie & D.E. Buchanan (ICMP 6888 /ATCC 58184 ex type PDD 41017 in Huhndorf et al. 2004), and Ap. tintinnabula Samuels, McKenzie & D.E. Buchanan (ICMP 6889-96 ex type PDD 41022 in Jaklitsch and Voglmayr 2012). Jaklitsch and Voglmayr (2012) produced a 28S rDNA phylogeny where the type species Ap. montagnei seemed not significantly different from Ap. sinensis but distinct from the other species sequenced. In addition, some Apiospora sexual morphs have been biologically linked with putatively prioritary Arthrinium taxa: A. hysterinum = Ap. bambusae (Turconi) Sivan. (Sivanesan 1983; Kirk 1986; Réblová et al. 2016), A. arundinis = Ap. montagnei (Hyde et al. 1998), and A. sinense = Ap. sinense (Réblová et al. 2016). However, none of these putative synonymies has been confirmed with genetic data, as some type collections are missing or too old for standard DNA analysis.

The aim of the present study was to study new Arthrinium samples found in temperate and southern Europe, including one specimen of A. caricicola and several putatively new species, and compare them morphologically and genetically with existing taxa. In some cases, e.g. Ap. tintinnabula, type collections were loaned and additional sequences obtained to delimit the genetic boundaries of some species.

Materials and methods

Pure culture isolation

During the surveys conducted in 2017 and 2018, 34 fresh specimens were collected from various plant hosts in Germany, Italy, Portugal and Spain. To isolate the sexual morph, ascomata were removed from the stromata using a sterile razor blade, transferred to a water droplet mounted on a microscope slide, torn apart with forceps to release the ascospores from asci, and pipetted on a 2% malt extract agar (MEA) plate supplemented with 200 mg/L penicillin G and streptomycin sulphate. Germinated ascospores were then transferred to MEA 2% plates, which were sealed with plastic film and incubated at room temperature. To isolate the asexual morph, plate cultures were superficially scrapped with a needle to dislodge conidia that were transferred to a drop of water. The suspension was then picked up with a syringe, and small droplets sown on a MEA 2% plate supplemented with 200 mg/L penicillin G and streptomycin sulphate. The germinated conidia were then transferred to 2% MEA plates, which were sealed with laboratory film and incubated at room temperature. Cultures were deposited at CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands (CBS).

Morphological observations

Hand sections of stromata or conidiomata were made using a razor blade and mounted in water on a microscope slide. Observations were made with a Zeiss Axioscop microscope using differential interference contrast (DIC), images were taken with a FLIR camera with A. Coloma open source software. Measurements were taken with FIJI ImajeJ software, reported with maximum and minimum values in parentheses, and the range representing the mean plus and minus the standard deviation, followed by the number of measurements in parentheses. For certain images of conidiophores, the image stacking software Zerene Stacker v. 1.04 (Zerene Systems LLC, Richland, WA, USA) was used. Morphological descriptions were based on cultures sporulating on 2% MEA medium at room temperature. The original specimens were deposited at the fungarium of the Real Jardin Botanico de Madrid (MA-Fungi).

DNA isolation, amplification and phylogenetic analyses

Total DNA was extracted from dry specimens employing a modified protocol based on Murray and Thompson (1980). PCR amplification was performed with the primers ITS1F and ITS4 (White et al. 1990; Gardes and Bruns 1993) for ITS region, while LR0R and LR5 (Vilgalys and Hester 1990; Cubeta et al. 1991) were used to amplify the 28S rDNA region, T1, Bt2a, and Bt2b (Glass and Donaldson 1995; O’Donnell and Cigelnik 1997) for the β-tubulin gene (tub2), and EF1-728F, EF1-983F and EF1-1567R (Rehner and Buckley 2005) for the translation elongation factor 1a (tef1) gene. PCR reactions were performed under a program consisting of a hot start at 95 °C for 5 min, followed by 35 cycles at 94 °C, 54 °C and 72 °C (45, 30 and 45 s respectively) and a final 72 °C step 10 min. PCR products were checked in 1% agarose gels, and positive reactions were sequenced with one or both PCR primers. Chromatograms were checked searching for putative reading errors, and these were corrected.

BLAST (Altschul et al. 1990) was used to select the most closely related sequences from INSDC public databases. Sequences came mainly from Crous and Groenewald (2013), Singh et al. (2013), Sharma et al. (2014), Crous et al. (2015), Senanayake et al. (2015), Dai et al. (2016, 2017), Hyde et al. (2016), Réblová et al. (2016), Jiang et al. (2018), and Wang et al. (2018), as well as Ogawa et al. (unpublished). Two distinct alignments were built in MEGA 5.0 (Tamura et al. 2011) and aligned with Clustal W with manual corrections: 1) a multigenic alignment including ITS, 28S rDNA, tub2 and tef1 data (without introns) from all Apiosporaceae and related families, and 2) a second alignment built with the same DNA markers (with introns) including only species related with A. sacchari (/saccharii clade). Introns were removed from tef1 and tub2, and GBlocks (Castresana 2000) was employed to remove 201 ambiguously aligned sites from ITS rDNA in the Apiosporaceae alignment, but not in the alignment of the /sacchari clade, in order to resolve this complex with all the phylogenetic signal available. The final alignment of the Apiosporaceae included five partitions with 217/461 (ITS rDNA), 229/846 (28S rDNA), 78/252 (tub2), 43/147 (tef1 EF1-728F to EF1-983F), and 76/413 (tef1 EF1-983F to EF1-1567R) variable sites, while the final alignment of the /sacchari clade had 35/535 (ITS rDNA), 18/837 (28S rDNA), 99/719 (tub2), 68/429 (tef1 EF1-728F to EF1-983F), and 4/407 (tef1 EF1-983F to EF1-1567R) variable sites. The aligned loci were loaded in PAUP* 4.0b10 (Swofford 2001) and subjected to MrModeltest 2.3 (Nylander 2004). Model GTR+G+I was selected and implemented in all partitions in MrBayes 3.2.6 (Ronquist and Huelsenbeck 2003), where a Bayesian analysis was performed (data partitioned, two simultaneous runs, six chains, temperature set to 0.2, sampling every 100th generation) until convergence parameters were met after about 3.43M generations (Apiosporaceae) or 0.9M (/sacharii clade), standard deviation having fell below 0.01. Finally, a full search for the best-scoring maximum likelihood tree was performed in RAxML (Stamatakis 2006) using the standard search algorithm (data partitioned, GTRMIX model, 2000 bootstrap replications). Significance threshold was set above 0.95 for posterior probability (PP) and 70% bootstrap proportions (BP).

Results

Phylogeny

The analysis of ITS, 28S rDNA, tef1 and tub2 data from the entire family Apiosporaceae (Fig. 1) produced a phylogeny with two main significantly supported clades: 1) composed of A. puccinioides, A. japonicum and newly sequenced specimens matching the species A. cariciola, A. curvatum var. minus, and A. sporophleum, and 2) a second clade containing all other sequences of Arthrinium and Apiospora. Among the other specimens analyzed, some matched the genetic concept of A. hysterinum, A. phragmitis, A. arundinis, A. rasikravindrae, or A. marii. Five new lineages were also found, which are formally proposed as new taxa below.

The analysis of ITS, 28S rDNA, tef1 and tub2 of the species around A. sacchari (/sacchari clade) (Fig. 2) showed that the clade of A. marii contains the types of A. hispanicum and A. mediterranei, but receives low overall support, maybe because of the incomplete data from these two species. Samples CBS 113535 and CBS 114803 were identified as A. marii too, but seem to represent an independent lineage.

Figure 1. 

50% majority rule consensus phylogram obtained in MrBayes from 25725 trees after the analysis of ITS rDNA, 28S rDNA, tef1 and tub2 sequences (introns excluded) of the family Apiosporaceae. Nodes were annotated if supported by > 70% ML BP or > 0.95 bayesian PP, but non-significant support values are exceptionally represented inside parentheses. Bold names represent samples sequenced in the present study.

Figure 2. 

50% majority rule consensus phylogram obtained in MrBayes from 6750 trees after the analysis of ITS rDNA, 28S rDNA, tef1 and tub2 sequences (introns included) of the /sacchari clade. Nodes were annotated if supported by > 70% ML BP or > 0.95 bayesian PP, but non-significant support values are exceptionally represented inside parentheses. Bold names represent samples sequenced in the present study.

Details of strains included in this study. Types are in bold.

Species Isolate CBS culture Herbarium code Host ITS rDNA 28S rDNA tef1 tub2
A. arundinis AP11118A CBS 145128 MA-Fungi 91722 Bambusa sp. MK014835 MK014868 MK017945 MK017974
A. balearicum, holotype AP24118 CBS 145129 MA-Fungi 91723 Undetermined poaceae MK014836 MK014869 MK017946 MK017975
A. caricicola AP23518 CBS 145127 MA-Fungi 91725 Carex ericetorum MK014838 MK014871 MK017948 MK017977
A. curvatum var. minus. AP25418 CBS 145131 MA-Fungi 91726 hojas de Carex sp. MK014839 MK014872 MK017949 MK017978
A. descalsii, holotype AP31118A CBS 145130 MA-Fungi 91724 Ampelodesmos mauritanicus MK014837 MK014870 MK017947 MK017976
A. esporlense, holotype AP16717 CBS 145136 MA-Fungi 91727 Phyllostachys aurea MK014845 MK014878 MK017954 MK017983
A. hysterinum AP15318 CBS 145132 MA-Fungi 91728 Phyllostachys aurea MK014840 MK014873 MK017950 MK017979
ICMP6889 Bambusa MK014841 MK014874 MK017951 MK017980
AP29717 CBS 145133 MA-Fungi 91729 Phyllostachys aurea MK014842 MK014875 MK017952 MK017981
AP2410173 CBS 145134 MA-Fungi 91730 Phyllostachys aurea MK014843 MK014876
AP12118 CBS 145135 MA-Fungi 91731 Phyllostachys aurea MK014844 MK014877 MK017953 MK017982
A. ibericum, holotype AP10118 CBS 145137 MA-Fungi 91732 Arundo donax MK014846 MK014879 MK017955 MK017984
A. italicum, holotype AP221017 CBS 145138 MA-Fungi 91733 Arundo donax MK014847 MK014880 MK017956 MK017985
AP29118 CBS 145139 MA-Fungi 91734 Phragmites australis MK014848 MK014881 MK017957 MK017986
A. marii AP13717 CBS 145140 MA-Fungi 91735 Arundo donax MK014849 MK014882 MK017958 MK017987
AP10118A Phragmites australis MK014850 MK014883 MK017959 MK017988
AP11717A CBS 145141 MA-Fungi 91737 Ampelodesmos mauritanicus MK014851 MK014884 MK017960 MK017989
AP191017 MA-Fungi 91738 Phragmites australis MK014852 MK014885 MK017961 MK017990
AP261017 CBS 145142 MA-Fungi 91739 Piptatheri miliaceum MK014853 MK014886 MK017962 MK017991
Vog2 CBS 145143 MA-Fungi 91740 Phragmites australis MK014854 MK014887 MK017963 MK017992
AP31118 CBS 145144 MA-Fungi 91736 Ampelodesmos mauritanicus MK014855 MK014888 MK017964 MK017993
A. phragmitis AP281217A1 CBS 145145 MA-Fungi 91741 Phragmites australis MK014856 MK014889 MK017965 MK017994
AP2410172A CBS 145146 MA-Fungi 91742 Phragmites australis MK014857 MK014890 MK017966 MK017995
AP3218 CBS 145147 MA-Fungi 91743 Phragmites australis MK014858 MK014891 MK017967 MK017996
AP29717A CBS 145148 MA-Fungi 91744 Arundo donax MK014859 MK014892 MK017968 MK017997
A. piptatheri, holotype AP4817A CBS 145149 MA-Fungi 91745 Piptatherum miliaceum MK014860 MK014893 MK017969
A. puccinioides AP26418 CBS 145150 MA-Fungi 91746 Carex arenaria MK014861 MK014894 MK017970 MK017998
A. rasikravindrii AP8817 CBS 145151 MA-Fungi 91747 Phyllostachys aurea MK014862 MK014895
AP10418 CBS 145152 MA-Fungi 91748 Phyllostachys aurea MK014863 MK014896 MK017971 MK017999
AP2410171 CBS 145153 Phyllostachys aurea MK014864 MK014897 MK017972 MK018000
A. sporophleum AP21118 CBS 145154 MA-Fungi 91749 Juncus sp. MK014865 MK014898 MK017973 MK018001

Details of all strains included in the phylogenetic analyses. Sequences generated in this study are shown in bold.

Species voucher/culture ITS rDNA 28S rDNA tub2 tef1
Apiospora setosa ICMP 4207 DQ368631 DQ368620
Apiospora tintinnabula ICMP6889 MK014841 MK014874 MK017951 MK01980
Arthrinium ‘vietnamense IMI 99670 KX986096 KX986111 KY019466
Arthrinium arundinis CBS 106 12 KF144883 KF144927 KF144973 KF145015
Arthrinium arundinis CBS 145128 MK014835 MK014868 MK017945 MK017974
Arthrinium arundinis CBS 449 92 KF144887 KF144931 KF144977 KF145019
Arthrinium arundinis CBS 450 92 AB220259 KF144932 KF144978 KF145020
Arthrinium arundinis CBS 124788 KF144885 KF144929 KF144975 KF145017
Arthrinium arundinis CBS 133509 KF144886 KF144930 KF144976 KF145018
Arthrinium arundinis CBS 114316 KF144884 KF144928 KF144974 KF145016
Arthrinium arundinis CBS 464 83 KF144888 KF144933 KF144979 KF145021
Arthrinium arundinis CBS 732 71 KF144889 KF144934 KF144980 KF145022
Arthrinium arureum CBS 24483 AB220251 KF144935 KF144981 KF145023
Arthrinium balearicum CBS 145129 MK014836 MK014869 MK017946 MK017975
Arthrinium camelliae-sinensis LC8181 KY494761 KY494837 KY705229 KY705157
Arthrinium camelliae-sinensis LC5007 KY494704 KY494780 KY705173 KY705103
Arthrinium caricicola CBS 145127 MK014838 MK014871 MK017948 MK017977
Arthrinium curvatum var. minus CBS 145131 MK014839 MK014872 MK017949 MK017978
Arthrinium descalsii CBS 145130 MK014837 MK014870 MK017947 MK017976
Arthrinium dichotomanthi LC8175 KY494755 KY494831 kY705223 KY705151
Arthrinium dichotomanthi LC4950 KY494697 KY494773 KY705167 KY705096
Arthrinium esporlense CBS 145136 MK014845 MK014878 MK017954 MK017983
Arthrinium euphorbiae IMI 285638b AB220241 AB220335 AB220288
Arthrinium garethjonesii JHB004 KY356096 KY356091
Arthrinium garethjonesii HKAS 96289 NR_154736 NG_057131
Arthrinium guizhouense LC5322 KY494709 KY494785 KY705178 KY705108
Arthrinium guizhouense LC5318 KY494708 KY494784 KY705177 KY705107
Arthrinium hydei CBS 114990 KF144890 KF144936 KF144982 KF145024
Arthrinium hydei LC7103 KY494715 KY4947911 KY705183 KY705114
Arthrinium hyphopodii MFLUCC 15-003 NR_154699
Arthrinium hyphopodii JHB003 Art KY356098 KY356093
Arthrinium hysterinum CBS 145133 MK014842 MK014875 MK017952 MK01981
Arthrinium hysterinum CBS 145135 MK014844 MK014877 MK017953 MK01982
Arthrinium hysterinum CBS 145132 MK014840 MK014873 MK017950 MK01879
Arthrinium hysterinum CBS 145134 MK015843 MK014876
Arthrinium ibericum CBS 145137 MK014846 MK014879 MK017955 MK017984
Arthrinium italicum CBS 145138 MK014847 MK014880 MK017956 MK017985
Arthrinium italicum CBS 145139 MK014848 MK014881 MK017957 MK017986
Arthrinium japonicum IFO30500 AB220262 AB220309 AB220309
Arthrinium japonicum IFO31098 AB220264 AB220311 AB220311
Arthrinium jatrophae CBS 134262 NR_154675
Arthrinium jatrophae MMI00051 AB743995
Arthrinium jiangxiense LC4577 KY494693 KY494769 KY705163 KY705092
Arthrinium jiangxiense LC4494 KY494691 KY494766 KY705160 KY705089
Arthrinium kogelbergense CBS 113332 KF144891 KF144937 KF144983 KF145025
Arthrinium kogelbergense CBS 113333 KF144892 KF144938 KF144984 KF145026
Arthrinium kogelbergense CBS 113335 KF144893 KF144939 KF144985 KF145027
Arthrinium kogelbergense CBS 117206 KF144895 KF144941 KF144987 KF145029
Arthrinium longistromum MFLU 15-1184 NR_154716
Arthrinium longistromum MFLUCC 11-0481 KU940141 KU863129
Arthrinium malaysianum CBS 102053 KF144896 KF144942 KF144988 KF145030
Arthrinium malaysianum CBS 251.29 KF144897 KF144943 KF144989 KF145031
Arthrinium marii CPC 18902 KF144901 KF144948
Arthrinium marii CBS 145140 MK014849 MK014882 MK017958 MK017987
Arthrinium marii CBS 114803 KF144899 KF144945 KF144991 KF145033
Arthrinium marii CBS 113535 KF144898 KF144944 KF144990 KF145032
Arthrinium marii CBS 145141 MK014851 MK014884 MK017960 MK017989
Arthrinium marii CBS 145142 MK014853 MK014886 MK017962 MK017991
Arthrinium marii CBS 145143 MK014854 MK014887 MK017963 MK017992
Arthrinium marii CBS 145144 MK014855 MK014888 MK017964 MK017993
Arthrinium mediterranei IMI 326875 AB220243 AB220337 AB220290
Arthrinium neosubglobosa HKAS 96354 NR_154737 NG_057131
Arthrinium neosubglobosa JHB006 KY356089 KY356094
Arthrinium obovatum LC8177 KY494757 KY494833 KY705225 KY705153
Arthrinium obovatum LC4940 KY494696 KY494772 KY705166 KY705095
Arthrinium ovatum CBS 115042 KF144903 KF144950 KF144995 KF145037
Arthrinium phaeospermum CBS 114317 KF144906 KF144953 KF144998 KF145040
Arthrinium phaeospermum CBS 114318 KF144907 KF144954 KF144999 KF145041
Arthrinium phaeospermum CBS 114315 KF144905 KF144952 KF144997 KF145039
Arthrinium phaeospermum CBS 114314 KF144904 KF144951 KF144996 KF145038
Arthrinium phragmitis CBS 145145 MK014856 MK014889 MK017965 MK017994
Arthrinium phragmitis CBS 145146 MK014857 MK014890 MK017966 MK017995
Arthrinium phragmitis CBS 135458 KF144909 KF144956 KF145001 KF145043
Arthrinium phragmitis CBS 145147 MK014858 MK014891 MK017967 MK017996
Arthrinium phragmitis CBS 145148 MK014859 MK014892 MK017968 MK017997
Arthrinium piptatheri CBS 145149 MK014860 MK014893 MK017969
Arthrinium pseudosinense CBS 135459 KF144910 KF144957 KF145044
Arthrinium pseudospegazzinii CBS 102052 KF144911 KF144958 KF145002 KF145045
Arthrinium pterospermum CBS 123185 KF144912 KF144959 KF145003
Arthrinium pterospermum CBS 134000 KF144913 KF144960 KF145004 KF145046
Arthrinium puccinioides CBS 145150 MK014861 MK014894 MK017970 MK017998
Arthrinium rasikravindrae CBS 33761 KF144914 KF144961
Arthrinium rasikravindrae CBS 145151 MK014862 MK014895
Arthrinium rasikravindrae CPC 21602 KF144915
Arthrinium rasikravindrae CBS 145152 MK014863 MK014896 MK017971 MK017999
Arthrinium rasikravindrae LC7115 KY494721 KY494797 KY708159 KY705118
Arthrinium rasikravindrae CBS 145153 MK014864 MK014897 MK017972 MK018000
Arthrinium sacchari CBS 30149 KF144917 KF144963 KF145006 KF145048
Arthrinium sacchari CBS 21230 KF144916 KF144962 KF145005 KF145047
Arthrinium sacchari CBS 66474 KF144919 KF144965 KF145008 KF145050
Arthrinium sacchari CBS 37267 KF144918 KF144964 KF145007 KF145049
Arthrinium saccharicola (1) CBS 19173 KF144920 KF144966 KF145009 KF145051
Arthrinium saccharicola (1) CPC 18977 KF144923
Arthrinium saccharicola (2) CBS 33486 AB220257 KF144967 KF145010 KF145052
Arthrinium saccharicola (2) CBS 83171 KF144922 KF144969 KF145012 KF145054
Arthrinium saccharicola (2) CBS 46383 KF144921 KF144968 KF145011 KF145053
Arthrinium serenense ATCC 76309 AB220240 AB220334 AB220287
Arthrinium serenense IMI 326869 AB220250 AB220344 AB220297
Arthrinium sporophleum CBS 145154 MK014865 MK014898 MK017973 MK018001
Arthrinium subglobosa MFLUCC 11-0397 KR069112 NG_057070
Arthrinium subglobosa (‘hyphopodii’) MFLUCC 15-003 KR069111
Arthrinium subroseum LC7292 KY494752 KY494828 KY705220 KY705148
Arthrinium subroseum LC7215 KY494740 KY494816 KY705208 KY705236
Arthrinium thailandicum LC5630 KY494714 KY494790 KY806200 KY705113
Arthrinium thailandicum MFLUCC 15-0202 KU940145 KU863133

Taxonomy

Arthrinium balearicum Pintos & P. Alvarado, sp. nov.

MycoBank No: 828866
Fig. 3

Etymology

Refers to the Balearic Islands (Spain), where the holotype was found.

Diagnosis

Sexual morph: Stromata forming black, linear, confluent raised areas on host surface, with the longer axis broken at the apex, (500–)600–1500(–2000) µm × (200–)320–450(–500) µm (n = 20). Ascomata globose to subglobose, with flattened base, blackish brown, (120–) 140–180 (–200) µm in diameter (n = 30). Peridium 8–15 µm thick, consisting of 4–5 layers of cells arranged in textura angularis, externally dark brown, hyaline in the inner part. Ostiole single, central, 30–60 µm in diameter, with a periphysate channel 20–30 µm long. Peryphises broad, colourless. Hamathecium composed of dense hypha-like, broad septate paraphyses, deliquescing early, 4–6 µm thick. Asci 8-spored, unitunicate, clavate, broadly cylindrical, with an inconspicuous pedicel, rounded apex, thin-walled, without an apical apparatus, measuring (77–)80–98(–105) × (14–)15–19(–21) µm (n = 22). Ascospores 1–3-seriate, hyaline, apiospore smooth-walled, fusiform, elliptical, reniform, straight or curved, bicellular, wider at the center of the longest cell, measuring (23–)26–30(–32) × (7–)9–10(–12) µm (n = 35), basal cell 3–6 µm long, sometimes containing a droplet. Asexual morph: not observed. Culture characteristics: colonies flat spreading on MEA 2%, with moderate aerial mycelium, reverse withish.

Type

Spain: Balearic Islands: Mallorca, Llucmajor, on undetermined Poaceae, 24 Jan. 2018, A. Pintos (MA-Fungi 91723 holotype, AP24118 isotype, CBS 145129 ex-type culture).

Notes

Arthrinium balearicum is related with A. descalsii, but has some genetic differences with this species having only 93% (482/518 bp) of its ITS rDNA, 99% (821/823 bp) of 28S rDNA, 97% (688/707 bp) of tef1, and 98% (406/413 bp) of tub2 similar. It is also phylogenetically close to A. phragmitis, a species with a similar ascospore size, (23–)26–30(–32) × (7–)9–10(–12) µm in A. balearicum and (22–)23–28(–30) µm × (6–)7–9(–10) µm in A. phragmitis. Unfortunately, the asexual morph of A. balearicum could not be studied to compare it with that of A. phragmitis.

Figure 3. 

A. balearicum A stromata on host; B asci C–F ascospores G colony on MEA. Scale bars: 200 µm (A); 20 µm (B); 5 µm (C–F).

Arthrinium caricicola Kunze & J.C. Schmidt, Mykologische Hefte (Leipzig) 1: 9 (1817)

Fig. 4

Description

Asexual morph: colonies on the host punctiform, pulvinate, 140–400 µm in diameter, blackish brown. Mycelium formed by hyaline smooth, branched hyphae, 2–5 µm in diameter. Conidiophore mother cells arising from a superficial or erumpent mycelial mat, subspherical to lageniform in shape, hyaline with brown pigments at the base, measuring (4–)5–7(–8) × (8–)9–11(–12) µm (n = 45). Conidiophores erect or ascending, simple, straight or flexuous, cylindrical, smooth-walled, colourless excepting for the thick, brown to dark brown, transversal septa, 15–100 × 3–5 µm (n = 50). Conidia fusiform or broadly spindle-shaped, smooth-walled, broader at the middle, tapering towards the narrowly rounded ends, dark brown with a hyaline rim, (37–)44–51(–55) µm in frontal view, (8–)9–11(–12) µm in side view (n = 50). Sterile cells smaller, 15–19 × 10–13 µm, and paler than conidia, bicuspidate or irregularly lobed. Culture characteristics: flat colonies spreading on MEA 2%, with moderately abundant, white cottony aerial mycelium, reverse whitish too, circular in shape with irregular edge.

Notes

The conidia of A. caricicola and A. japonicum have a similar fusiform shape and length, but differ in width ((8–)9–11(–12) µm vs 12–16(–20) µm). Conidia of A. mytilimorphum have also a similar shape, but turns out shorter and thinner (20–30 × 6–8.5 µm). The morphological characters of the syntype of A. caricicola deposited by Fries in the Herbarium of Uppsala University as Fung. Scleromyc. Suecici, fully match the specimen collected in this study. The closely related species A. sporophleum has very different lemon-shaped conidia, while those of A. curvatum var. minus are curved, and those of A. puccinioides are polygonal.

Specimens examined

Germany: Brandenburg: south of Liberose, on dead leaves of Carex ericetorum, 14 May 2018, R. Jarling (MA-Fungi 91725).

Figure 4. 

A. caricicola A colony on host B colony on MEA C conidiophore mother cell D, E conidiophore mother cell, conidiophore bearing conidia, conidia F–H conidia I conidia with scar J lobate sterile cells. Scale bars: 200 µm (A); 5 µm (C–I); 10 µm (J). K A. caricicola syntype, colonies on host; L, M conidia.

Arthrinium curvatum var. minus M.B. Ellis, Trans. Brit. Mycol. Soc. 34: 501 (1951)

Fig. 5

Physalospora scirpi Arx, Gen. Fungi Sporul. Cult. (Lehr): 116 (1970).

Pseudoguignardia scirpi Gutner, Mater. Mikol. Fitopat. Ross. 6(1): 311 (1927).

Description

Asexual morph: Colonies are compact, round, dark to black, 80–320 in diameter. Mycelium is composed of hyaline to pale brown smooth hyphae 2–7 µm in diameter. Conidiophore mother cells spherical to lageniform, hyaline with brown pigments at the base, measuring (4–)5–7(–8) × (4–)5–6(–7) µm (n = 30). Conidiophores cylindrical unbranched, straight or flexuous, hyaline and smooth walled, with a single brown transversal septa, measuring 30–100 × 2–4 µm. (n = 30). Conidiogenous cells cylindrical 1–1.5 × 1–1.5 µm (n = 20). Conidia borne along the sides of conidiophores, curved, rounded at the ends, brown, with a hyaline germ slit and a clearly visible scar, (8–)9–10(–11) µm long in frontal view, (5–)6–7(–8) µm in side view (n = 30). Sterile cells rounded, paler than conidia. Culture characteristics flat colonies spreading on MEA 2% with moderate aerial mycelium, reverse withish.

Notes

Arthrinium curvatum var. minus can be confused with A. curvatum var. curvatum , but conidia of var. minus measure (8–)9–10(–11) × (5–)6–7(–8) µm, while those of A. curvatum var. curvatum measure 11–15 × 6–8 µm. Gutner (1927) described Pseudoguignardia scirpi, a sexual morph of A. curvatum, later combined as Physalospora scirpi (Arx 1970). Arthrinium curvatum var. minus is closely related with A. sporophleum (with lemon-shaped conidia) and A. japonicum (with larger fusiform conidia) and to a lesser extent also with A. caricicola (with larger fusiform conidia) and A. puccinioides (with polygonal conidia). Ellis et al. (1951) described A. curvatum var. minus, a taxon with similarly shaped but smaller conidia than A. curvatum. The specimen studied in the present work matches the shape and size of conidia reported by Ellis et al. (1951) for A. curvatum var. minus, rather than those of A. curvatum var. curvatum.

Specimens examined

Germany: Brandenburg: south of Liberose, on dead leaves of Carex sp., 28 Mar. 2018, R. Jarling (MA-Fungi 91726).

Figure 5. 

A. curvatum var. minus A colony on host B conidiophore mother cell C, D conidiophore mother cell, conidiophore bearing conidia E, F curved conidia G colony on MEA. Scale bars: 200 µm (A); 5 µm (B–F).

Arthrinium descalsii Pintos & P. Alvarado, sp. nov.

MycoBank No: 828867
Fig. 6

Etymology

Named to honor the eminent mycologist Enric Descals Callisen.

Diagnosis

Sexual morph: Stromata forming black fusiform spots that merge with each other with age, forming an erumpent black mass visible at the naked eye, 2–10 × 0.2–0.5 mm in size, with the long axis broken at the top revealing the ostioles of pseudothecia. Ascomata pseudothecia, subglobose with a flattened base, arranged in rows, brown to dark brown, 150–220 μm high × 150–250 μm wide (n = 20). Peridium with several layers of cells arranged in textura angularis, with a conspicuous ostiole 50–80 μm in diameter, periphysate. Hamathecium paraphyses hyphae-like, septate, hyaline. Asci cylindrical, clavate, with a short or indistinct pedicel, with rounded apices, measuring (73–)82–95(–111) × (16–)17–20(–23) μm (n = 30). Ascospores uniseriate to biseriate, hyaline, smooth-walled, apiosporic, composed of a large curved upper cell and smaller lower cell, fusiform to slightly curved in shape with narrowly rounded ends, guttulated, sometimes with a thick gelatinous sheath, (17–)18–22(–24) × (6–)7–9(–10) μm, and a basal cell 3–5 μm (n = 45). Asexual morph: Mycelium hyaline, septate, branched, hyphae 1.5–4.5 μm in diameter Conidiophores reduced to the conidiogenous cells. Conidiogenous cells solitary on hyphae, ampuliform, hyaline to brown, 5 × 4 μm. Conidia brown, smooth, guttulate, globose to ellipsoid (5–)7(–8) µm long (n = 20) in face view, lenticular with a paler equatorial slit and 6-7 μm long in side view (n = 10). Sterile cells elongated, sometimes mixed among conidia. Culture characteristics: ascospores germinating on MEA 2% within 24–48 h. Colonies flat, spreading, with sparse aerial mycelium, pale siena.

Notes

Arthrinium descalsii is closely related with A. phragmitis and A. balearicum. It was found in the Mediterranean grass Ampelodesmos mauritanicus, although additional samples are needed before concluding if it could be exclusively associated with this endemic host. Ascospore size is often smaller than that of A. balearicum, (23–)26–30(–32) × (7–)9–10(–12) µm, but it matches that reported in the protologue of A. phragmitis, (20–)22–24(–25) × (7–)8–9(–10) µm. However, the conidiophores of A. descalsii are reduced to conidiogenous cells, while those of A. phragmitis measure about 10–45 × 1.5–2 µm, and conidia are slightly smaller in face view, measuring (5–)7(–8) µm long in A. descalsii and up to 8–10(–11) µm in A. phragmitis.

Type

Spain: Balearic Islands: Mallorca, es Capdella, on dead stems of Ampelodesmos mauritanicus, 31 Jan. 2018, A. Pintos (MA-Fungi 91724 holotype, AP31118A isotype, CBS 145130 ex-type culture).

Figure 6. 

A. descalsii A stromata on host B–D asci with ascospores E paraphyses F, G ascospores I, J ascospores with sheath K colony on MEA 2%; coniogenous cell giving rise to conidia; conidiogenous cells giving rise to conidia and conidia cluster G conidia. Scale bars: 200 µm (A); 10 µm (B–E); 5 µm (F–J); 5 µm (L–N).

Arthirnium esporlense Pintos & P. Alvarado, sp. nov.

MycoBank No: 828868
Fig. 7

Etymology

In reference to Esporles, the village of Mallorca (Spain) where it was found.

Diagnosis

Asexual morph: Mycelium consisting of smooth, hyaline, branched septate hyphae about 1.5–4 µm in diameter. Conidiophores reduced to conidiogeous cells. Conidiogenous cells polyblastic, aggregated in clusters on hyphae, smooth, hyaline to pale brown, ampuliform, cylindrical or lageniform, measuring 4–22 × 4–8 μm. Conidia brown, smooth, globose with a pale equatorial slit and (8–)9–12(–13) µm long in frontal view, lenticular and 6–8 μm long in side view (n = 30). Sterile cells elongated, sometimes mixed among conidia, paler than them. Culture characteristics: colonies flat, spreading, with moderate aerial mycelium, on MEA 2% surface white with yellowish patches, reverse concolour with age.

Type

Spain: Balearic Islands: Mallorca, Esporles, on dead culms of Phyllostachys aurea, 16 July 2017, A. Pintos (MA-Fungi 91727 holotype, AP16717 isotype, CBS 145136 ex-type culture).

Notes

Arthrinium esporlense is closely related with A. xenocordella and A. kogelbergense. However, A. esporlense does not produce brown setae as A. xenocordella, a species until now known only from soil samples (Crous and Groenewald 2013). Arthrinium esporlense morphologically differs from A. kogelbergense by producing slightly bigger conidiogenous cells (4–22 × 4–8 μm vs 5–12 × 4–5 μm). These three species are genetically related (1.00 PP, 96 BP) to the group formed by A. arundinis, A. thailandicum D.Q. Dai & K.D. Hyde, A. malaysianum and the new species A. italicum proposed below.

Figure 7. 

A. esporlense A colony on MEA B–F coniogenous cell giving rise to conidia G conidia. Scale bars: 5 µm (B–G).

Arthrinium hysterinum (Sacc.) P.M. Kirk, Trans. Brit. Mycol. Soc. 86: 409 (1986)

Fig. 8

Melanconium hysterinum Sacc., Bolm Soc. broteriana, Coimbra, sér. 1 11: 21 (1893) [Basionym].

Scyphospora hysterina (Sacc.) Sivan., Trans. Brit. Mycol. Soc. 81: 331 (1983).

Melanconium bambusae Turconi, Atti Ist. bot. R. Univ. Pavia, sér. 2 16: 251 (1916).

Scirrhia bambusae Turconi, Atti Ist. bot. R. Univ. Pavia, sér. 2 16: 531 (1916).

Scirrhodothis bambusae (Turconi) Trotter, in Saccardo, Syll. Fung. 24: 611 (1926).

Placostroma bambusae (Turconi) R. Sprague, Diseases Cereals Grasses N. Amer.: 121 (1950).

Apiospora bambusae (Turconi) Sivan., Trans. Brit. Mycol. Soc. 81: 331 (1983).

Scyphospora phyllostachydis L.A. Kantsch., Bolêz. Rast. 17: 88 (1928).

Cordella johnstonii M.B. Ellis, Mycol. Pap. 103: 31 (1965).

Apiospora setosa Samuels et al., New Zealand J. Bot. 19: 142 (1981).

Apiospora tintinnabula Samuels et al., New Zealand J. Bot. 19: 142 (1981).

Description

Sexual morph: Stromata black, fusiform, forming rows of densely arranged perithecial ascomata parallel to the main axis of the host, measuring (400–) 600–2500(–3000) × (250–)320–450(–550) µm (n = 30). Ascomata globose to subglobose, with a flattened base, blackish brown, (130–)250–290(–320) µm in diameter (n = 30). Peridium consisting of 3 or 4 layers of cells arranged in textura angularis, dark brown in the external side, hyaline in the inside, ostiole single, central, 10–30 µm in diameter, with a periphysate channel 20–35 µm long. Peryphises broad, colourless. Hamathecium composed of dense hypha-like, broad septate paraphyses, early deliquescing. Asci 8-spored, unitunicate, clavate, broadly cylindrical, pedicel indistinct, apical rounded, thin-walled, without an apical apparatus, measuring (76–) 85–98(–115) × (20–)22–26(–28) µm (n = 22). Ascospores uni- to tri-seriate, hyaline, apiosporic, smooth-walled, fusiform, elliptical, reniform, straight or curved, smooth-walled, sometimes with an internal droplet, bicellular, the widest part located in the central part of the longest cell, some ascospores have a mucose sheath covering them, (28–)32–34(–38) × (8–)9–11(–13) (n = 35) µm, basal cell 5–7 µm. Asexual morph: Mycelium branched, septate. Conidiomata on host surrounding the stromata of the sexual phase, parallel to the longitudinal axis of the stem, subepidermal, opening by longitudinal splitting of the epidermis and revealing a black conidial mass, (450–) 630–950(–1000) × (275–)345–550 (–600) µm (n = 35). Conidiophore mother cell arising from the stroma, ampuliform, lageniform, cupulate or cylindrical, sometimes with granular pigments at the apex, (5)6–10(–16) × (3–)5–7(–8) µm (n = 24). Conidiophores basauxic, polyblastic, cylindrical, hyaline to light brown, smooth or with granular pigments in all their length, straight or flexuous, septate or not, sometimes exceeding 90 μm in length × 2–4 μm wide (n = 43). Conidia globose to obovoid, dark brown, with a central scar at the base, (15–)16–20(–21) in frontal view, (14–)15–18(–19) in side view (n = 40). Sterile cells gray, irregularly angled and lobed, (15–)17–41(–42) × (10–)14–23(–25) µm (n = 30). Culture characteristics: colonies in MEA 2% flat, spreading, first white and cottony, later became dark pink, mycelium branched, septate, hyaline, reverse dark.

Notes

After the works of Samuels (1981), Sivanesan (1983), Kirk (1986) and Réblová et al. (2016), Ap. bambusae, Ap. setosa and Ap. tintinnabula, as well as Scyphospora phyllostachydis, are all considered synonyms of A. hysterinum. Arthrinium hysterinum is phyllogenetically close to A. yunnanum D.Q. Dai & K.D. Hyde, but morphologically differs from the latter because of its thinner asci (76–115 × 20–28 vs 85–100 × 30–35 μm). In addition, A. hysterinum has longer conidiophores up to 90 μm long, and lobed sterile cells while in A. yunnanum conidiophores do not exceed 50 μm, and sterile cells are lacking.

Specimens examined

New Zealand: Waikato: Paeroa, on dead culm of Bambusa sp., 28 Feb. 1980, E.H.C. McKenzie & P.R. Johnston (ICMP 6889 ex-type culture).

Spain: Galicia: Santiago de Compostela, on dead culms of Phyllostachys aurea, 12 Jan. 2018, A. Pintos (MA-Fungi 91731, AP12118). Balearic Islands: Mallorca, Esporlas, on dead culms of Phyllostachys aurea, 29 July 2017, A. Pintos (MA-Fungi 91729, AP29717). Mallorca, Jardin Botanico de Soller, on dead culms of Phyllostachys aurea, 24 Oct. 2017, A. Pintos (MA-Fungi 91730, AP2410173). Mallorca, Soller, on dead culms of Phyllostachys aurea, 15 Mar. 2018, A. Pintos (MA-Fungi 91728, AP15318).

Figure 8. 

A. hysterinum lenticular-shaped colonies on host A stromata and conidiomata B, C asci D–G ascospores H colony on MEA I black masses of conidia in culture K, L conidiophore mother cell M rugose conidiogenous cell N–P conidia with lobate sterile cells O conidia. Scale bars: 200 µm (A); 10 µm (B, C); 5 µm (D–G); 200 µm (I); 5 µm (K, M, O); 10 µm (P).

Arthrinium ibericum Pintos & P. Alvarado, sp. nov.

MycoBank No: 828869
Fig. 9

Etymology

In reference to the Iberian Peninsula, where the holotype was collected.

Diagnosis

Sexual morph: Stromata solitary to gregarious, immersed or semi-immersed, fusiform to ellipsoid in shape, black, with the long axis broken at the top, 2–5 × 0.5–1 mm. Ascomata perithecial, subglobose with a flattened base, arranged in rows, brown to dark brown, exudating a white cirrhus of ascospores, 170–300 µm in diameter and 200–300 µm high. Peridium consisting in 3 or 4 layers of cells arranged in textura angularis. Ostiole single, central, 12–30 µm in diameter, with a periphysate channel. Hamathecium composed of dense, septate, branched paraphyses. Asci 8-spored, clavate or cylindrical, lacking an apical apparatus, shortly pedicelate, measuring (82–)90–125(–128) × (14–)15–19(–21) μm (n = 30). Ascospores uniseriate to biseriate, hyaline, smooth-walled, apiosporic, composed of a large curved upper cell and small lower cell, fusiform or slightly curved in shape with narrowly rounded ends, uniguttulated, lacking a gelatinose sheath, measuring (28–)29–34(–37) × (5–)6–8(–9) μm, and a basal cell 5–7 μm (n = 45). Asexual morph: Mycelium hyaline, septate, branched, hyphae 2–4 μm in diameter. Conidiophores reduced to the conidiogenous cells. Conidiogenous cells aggregated in clusters on hypha or solitary, ampuliform or cylindrical, 6–12 × 3 μm. Conidia brown, smooth, globose to ellipsoid (9–)10(–12) µm long (n = 30) in face view, lenticular, with a paler equatorial slit, and (6–)7(–8) μm long (n = 40) in side view. Sterile cells elongated, rolled up, sometimes mixed among conidia. Culture characteristics: ascospores germinating on MEA 2% within 24–48 h. Colonies flat, spreading, with sparse aerial mycelium, pale siena with white patches.

Type

Portugal. Viana do Castelo: Valença do Minho, on dead culms of Arundo donax. 10 Jan. 2018, A. Pintos (MA-Fungi 91732 holotype, AP10118 isotype, CBS 145137 ex-type culture).

Notes

Arthrinium ibericum belongs to the large clade around A. sacchari, where it shows a relation with the subclade of A. phaeospermum, A. saccharicola, and the modern species A. serenense, A. camelliae-sinensis, A. jiangxiense, A. dichotomanthi, A. obovatum and A. pseudosinense. The size of conidia is more or less similar to that of A. camelliae-sinensis, where these measure about 9.0–13.5 μm in frontal view, but conidiogenous cells are a bit smaller in this species, measuring about 4.0–9.5 × 3.0–6.0 μm. Arthrinium pseudosinense has slightly smaller asci measuring 85–100 × 15–20 µm, and ellipsoid conidia covered with a mucilaginous sheath. Arthrinium saccharicola has hyphae slightly wider, about 3–5 µm. The genetic identity of A. phaeospermum is still dubious because of the lack of a proper type, but the lineages of this species in the work of Crous and Groenewald (2013) have slightly smaller conidiogenous cells measuring 5–10 × 3–5 μm, and a different iron-grey colour of colonies in MEA.

Figure 9. 

A. ibericum A ascomata with oozing ascospores B–D asci E–H ascospores I colony on MEA J–M conidiogenous cells giving rise to conidia N sterile cell with conidia O conidia. Scale bars: 200 µm (A); 10 µm (B–D); 20 µm (C); 5 µm (E–H); 5 µm (J–O).

Arthrinium italicum Pintos & P. Alvarado, sp. nov.

MycoBank No: 828870
Fig. 10

Etymology

In reference to Italy, the country where the holotype was found.

Diagnosis

Sexual morph: Stromata solitary to gregarious, inmersed to erumpent, fusiform, with long axis broken at the top by one or two cracks, 0.5–4 × 0.2–0.5 mm (n = 20). Ascomata uniseriate or irregularly arranged beneath stromata, pseudothecial, black, globose to subglobose with a flattened base, 150–200 μm high × 230–300 μm wide. Peridium composed of 5 or 6 layers of brown cells arranged in textura angularis, with a conspicuous peryphisate ostiole. Hamathecium paraphyses hyphae-like. Asci broadly cylindrical, clavate or subglobose, pedicel indistinct, apically rounded (70–)72–93(–96) × (14–)15–18(–20) μm (n = 30). Ascospores apiosporic, clavate to fusiform with narrowly rounded ends, composed of a large upper cell and small lower cell, hyaline, smooth-walled, surrounded by a gelatinose sheath, measuring (20–)21–25(–26) × (5–)6– 9(–10) μm, basal cell 3–5 μm (n = 45). Asexual morph: Mycelium consisting of smooth, hyaline, branched, septate hyphae 1.5–4 µm in diameter. Conidiophores straight or flexuous, cylindrical, colourless except for the thick brown transversal septa, smooth-walled, 10–50 × 1–3 μm. Conidiogenous cells ampuliform, cylindrical or doliform, hyaline to brown, (3–)4–7(–9) × (1.5–)2–3(–5) μm (n = 30). Conidia brown, smooth, globose in face view, lenticular in side view, 4–6 × 3–4 μm (n = 65), with a pale equatorial slit. Culture characteristics: on MEA 2%, sparse aerial mycelia, surface dirty white, reverse pale yellowish.

Type

Italy: Sicily: On dead culms of Arundo donax, 19 June 2016, H. Voglmayr (MA-Fungi 91733 holotype, AP221017 isotype, CBS 145138 ex-type culture).

Notes

Arthrinium italicum is phylogenetically close to A. thailandicum, and to a lesser extent to A. malaysianum. Stromata of A. thailandicum are smaller than those of A. italicum, measuring 0.45–0.99 × 0.3–0.55 mm, ascomata are perithecical, its conidiogenous cells are longer (11.5–39 × 2–3.5 μm) and branched, and conidia measure 5–9 × 5–8 μm. The conidia of A. malaysianum are similar in size, but this species does not produce conidiophores.

Other specimens examined

Spain: Balearic Islands: Mallorca, Puerto de Andratx, on dead culms of Phragmites australis, 29 Jan. 2018, A. Pintos (MA-Fungi 91734, AP29118).

Figure 10. 

A. italicum A, B stromata on host C asci D, E, G ascospores F ascospores with sheath H colony on MEA I–M conidiogenous cell giving rise to conidia N, O conidia. Scale bars: 200 µm (A, B); 5 µm (D–G); 5 µm (H–L, N, O); 10 µm (M).

Arthrinium marii Larrondo & Calvo, Mycologia 82: 397 (1990)

Fig. 11

Description

Sexual morph: Stromata forming black fusiform spots, visible at the naked eye, with a long axis broken at the top revealing the ostioles of pseudothecia, 2–6 × 0.2–0.5 mm in size. Ascomata subglobose, sometimes with a flattened base, brownish to reddish brown, 150–190 μm high × 160–250 μm wide (n = 20). Peridium with several layers of cells arranged in textura angularis, with a conspicuous ostiole 50–7–80 μm diameter, periphysate. Hamathecium paraphyses not prominent, hyphae-like, septate, hyaline. Asci 8-spored, unitunicate, broadly cylindrical to clavate, with rounded apex and a short pedicel, (60–)70–100(–115) × (16–)18–20(–22) μm (n = 30). Ascospores fusiform to elliptical, with narrowly rounded ends, hyaline, with multiple guttules, surrounded by a mucilaginous sheath, (16)19–23(–24) × (6–)7–8(–10) μm, basal cell 2–5 (n = 30). Asexual morph: Mycelium consisting of smooth, hyaline, branched, septate hyphae measuring 1.5–5 µm in diameter. Conidiophores straight or flexuous, cylindrical, colourless except for the thick brown transverse septa, measuring 10–40 × 2–3 μm. Conidiogenous cells ampuliform to cylindrical, hyaline to brown, (3–)4–7(–11) × (1.4–)2–4(–5) μm (n = 30). Conidia, brown, smooth, granular, globose in face view, lenticular in side view, measuring (6–)7–8(–9) × 4–5(–6) µm, with a pale equatorial slit. Sterile cells elongated, brown. Culture characteristics: ascospores germinating on MEA 2% within 24–48 h. Colonies flat, spreading, with sparse aerial mycelium, reverse concolour with agA.

Notes

Arthrinium marii was proposed by Larrondo and Calvo (1990) who described its asexual morph. This apparently frequent species has been isolated from the atmosphere, pharmaceutical excipients, home dust, and beach sand, as well as from various plant hosts (Crous 2013). In the present work the sexual morph is described for the first time. Genetically, samples identified as A. marii seem to represent two distinct clades (Fig. 2), with differences in tub2 and tef1 genes, but it should be further investigated with additional data before concluding if these clades should be interpreted as intraspecific variability, partially isolated lineages, or fully isolated species. Similarly, the incomplete data from the type specimens of A. hispanicum and A. mediterranei do not allow one to conclude if these apparently related species represent a single taxon or even belong to A. marii.

Specimens examined

Austria: Oberösterreich: St. Willibald, on dead culms of Phragmites australis, 10 July 2016, H. Voglmayr, (MA-Fungi 91738, AP191017).

Italy: Sicily: casa de la Monache, on dead culms of Phragmites australis, 16 July 2016, H. Voglmayr (MA-Fung 91740, APVog2).

Portugal: Viana do Castelo: Valença do Minho, on dead culms of Phragmites australis, 10 Jan. 2018, A. Pintos (AP10118A).

Spain: Balearic Islands: Mallorca, Esporlas, on dead culms of Arundo donax, 13 July 2017, A. Pintos (MA-Fungi 91735, AP13717). Ibidem., 29 July 2017, A. Pintos (AP29717). Palma de Mallorca, on Ampelodesmos mauritanicus, 11 July 2017, A. Pintos (MA-Fungi 91737, AP11717A). Palma de Mallorca, on dead culms of Phragmites australis, 26 July 2017, A. Pintos (MA-Fungi 91739, AP261017).

Figure 11. 

A. marii A stromata on host B asci C–F ascospores G colony on MEA H–I, K conidiogenous cells giving rise to conidia J conidiophore bearing conidia L conidia and sterile cells. Scale bars: 200 µm (A); 10 µm (B); 5 µm (C–F); 5 µm (H–L).

Arthrinium piptatheri Pintos & P. Alvarado., sp. nov.

MycoBank No: 828871
Fig. 12

Etymology

Named after Piptatherum, the host plant from which it was first isolated.

Diagnosis

Asexual morph: Mycelium consisting of smooth, hyaline, branched, septate hyphae measuring 1–4 µm in diameter. Conidiophore mother cells hyaline to brown, aggregated in clusters or solitary on hyphae, ampuliform, cylindrical or doliform, 4–11 × 2–5 µm, growing above one or several hyaline cylindrical cells. Conidiophore reduced to a conidiogenous cell. Conidiogenous cells basauxic, polyblastic, sympodial, cylindrical, discrete, sometimes branched, smooth-walled, measuring 6–27 × 2–5 μm (n = 25). Conidia globose to ellipsoidal, pale brown to brown, with a thin hyaline germ-slit, 6–8 × 3–5 μm (n = 30). Sterile cells eloganted, brown, sometimes mixed among conidia, 13–16 × 4–5 μm (n = 30). Culture characteristics: on MEA 2%, colonies flat, spreading, with sparse aerial mycelium, reverse concolour with agar.

Type

Spain: Balearic Islands: Mallorca: Llucmajor, on dead stems of Piptatherum miliaceum, 4 Aug. 2017, A. Pintos (MA-Fungi 91745 holotype, AP4817A isotype, CBS 145149 ex-type culture).

Notes

Arthrinium piptatheri is genetically close, but genetically distinct from A. marii, A. sacchari, A. guizhouense, A. hispanicum, A. mediterranei, A. longistromum D.Q. Dai & K.D. Hyde, and to a lesser extent A. pseudospegazzinii (Fig. 2) and the clade around A. phaeospermum (Fig. 1). The incomplete genetic data available is probably the cause behind the lack of significant support for some of these taxa. Morphologically, A. piptatheri differs from A. marii because of its sympodial, branched conidiogenous cells. Arthrinium guizhouense has shorter conidiogenous cells (3.5–8.0 μm). Finally, some sequences of Ap. montagnei are related also with this group (Fig. 2), but this species is considered the sexual morph of A. arundinis, with a very different genetic profile in Crous and Groenewald (2013), so its actual identity should be further investigated.

Figure 12. 

A. piptatheri A colony on MEA B–K conidiogenous cells giving rise to conidia. Scale bars: 5 µm (B–K).

Arthrinium puccinioides Kunze & J.C. Schmidt, Mykologische (Leizpig) 2: 103 (1823)

Fig. 13

Conoplea puccinioides DE Candolle, 1905, Flore Francaise, Ed. 3, Tome 2, p.73, ex Mérat, Novuvelle Flore des environs de Paris, 1821, p. 16.

Goniosporium puccinioides (Kunze & J. C.Schmidt) Link, in Willdenow, Sp.pl., Edn 4 6(1): 44 (1824).

Gonatosporium puccinioides (Kunze & J. C.Schmidt) Corda, Icon. Fung. (Prague) 3:8 (1839).

Description

Asexual morph: Mycelium consisting on smooth hyaline, branched, septate hyphae measuring 1.5–5 µm in diameter. Colonies are small, rounded or ovoid, dark brown, 50–400 µm in diameter. Conidiophore mother cells subspherical, lageniform or barrel-shaped, 4–5 × 3–5 µm (n = 30). Conidiophores cylindrical, straight or flexuous, septate, hyaline excepting for the thick brown or dark brown transversal septa, 20–140 × 3–4 µm (n = 30). Conidiogenous cells cylindrical, occurring between the conidiophore septa, 0.9–1.8 µm. Conidia dark brown, smooth, polygonal with rounded angles to hemispherical, measuring (8–)9–11(–12) × 8–9 µm, with one or two concentric pale rings. Sterile cells spherical, triangular or polygonal, with refractive bodies inside, paler than conidia, 6–9 µm in diameter. Culture characteristics colonies flat spreading on MEA 2%, with moderate aerial mycelium, reverse whitish, no esporulate on culture.

Notes

Arthrinium puccinioides is the only species of Arthrinium with polygonal conida. It shows a genetic relationship with other species found in Carex sp. hosts, such as A. caricicola, A. curvatum var. minus, A. japonicum or A. sporophleum. The present sample fits the original description of A. puccinioides by Kunze and Schmidt (1823) as well as those by Ellis et al. (1951), Ellis (1965), and Scheuer (1996).

Specimens examined

Germany: Berlin: Köpenick, Stellingdamm, on dead leaves of Carex arenaria, 26 April 2017, R. Jarling (MA-Fungi 91746, AP26418).

Figure 13. 

A. puccinioides A colony on host B colony on MEA C conidiophore mother cell D–F conidiophore bearing conidia G–H conidia in side view. Scale bars: 100 µm (A); 5 µm (C–H).

Arthrinium sporophleum Kunze, 1823, in Kunze & Schmidt's Mykologische Hefte, 2, p. 104; Fries, 1832, Systema Mycol., 3, p. 377

Fig. 14

Sporophleum gramineum Nees, 1824, apud Link in Linne, Species Plantarum, ed. 4 (Willdenow's), 6, 1, p. 45.

Torula eriophori Berkeley, 1836, Fungi in J. E. Smith's English Flora, 5 (2), p. 359.

Arthrinium sporophleoides Fuckel, Jb. nassau. Ver. Naturk. 27–28: 78 (1874) [1873–74]

Description

Asexual morph: Mycelium consisting on smooth hyaline branched hyphae, 2–5 µm in diameter. Colonies oval to irregular, dark blakish brown, 300–1200 × 150–650 µm. Conidiophore mother cells sub-cylindrical, hyaline to pale brown, measuring 5–7 × 5–7 µm (n = 20). Conidiophores straight to flexuous, cylindrical, hyaline except for the thick brown to dark brown transversal septa, 30–130 × 2–4 µm (n = 20). Conidia brown, smooth, lemon-shaped in face view, measuring (10–)11–14(–15) × (5–)6–8(–9) µm (n = 45), triangular with the outer edge curved and rounded angles in side view, measuring 5–8 µm thick. Sterile cells paler than conidia, subspherical or triangular, 5–8 µm wide. Culture characteristics: on MEA 2% colonies cottony, white with grey patches, reverse pale grey.

Notes

Arthrinium sporophleum is the only species of Arthrinium with lemon-shaped conidia. Kunze (1823) considered that Sporophleum gramineum represents a synonym of this species, and Cooke (1954) considered A. sporophleoides Fuckel a synonym of this species too. The only sample analyzed in the present work fits the descriptions of this species by Kunze (1823), Ellis et al. (1951), Ellis (1965) and Scheuer (1996). This sample was found in Juncus sp., but this remarkable species has been often reported from Carex sp. hosts (Ellis 1965). Interestingly, other species occurring in Carex sp. present also conidia with unusual shapes, e.g. A. puccinioides (polygonal), A. curvatum var. minus (curved), and A. caricicola or A. japonicum (fusiform).

Specimens examined

Spain: Balearic Islands: Mallorca, Escorca, on dead leaves of Juncus sp., 21 Feb. 2018, A. Pintos 21218 (MA-Fungi 91749).

Other specimens studied

Arthrinium arundinis : Spain: Galicia: Santiago de Compostela, city garden, culms of Bambusa sp., 11 Jan. 2018, A. Pintos 11118A (MA-Fungi 91722). Arthrinium phragmitis: Spain: Balearic Islands: Mallorca, Esporles, on dead culms of Arundo donax, 29 July 2017, A. Pintos (MA-Fungi 91744, AP29717A). Ibidem., on dead stem of Phragmites australis, 3 Feb. 2018, A. Pintos (MA-Fungi 91743, AP3218). Jardin Botanico de Soller, on dead culms of Arundo donax, 24 Oct. 2017, A. Pintos (MA-Fungi 91742, AP2410172A). Puigpunyent, on dead culms of Phragmites australis, 28 Dec. 2017, A. Pintos (MA-Fungi 91741, AP281217A1). Arthrinium rasikravindrii: Spain: Balearic Islands: Mallorca, Esporlas, on dead culms of Phyllostachys aurea, 8 Aug. 2017, A. Pintos (MA-Fungi 91747, AP8817). Jardin Botanico de Soller, on dead culms of Bambusa sp., 24 Oct. 2017, A. Pintos (AP2420171). Soller, on dead culms of Phyllostachys aurea, 10 Apr. 2018, A. Pintos (MA-Fungi 91748, AP10418).

Figure 14. 

A. sporophleum A colony on host B conidiophore mother cells C–E conidiophore mother cells with conidiophore bearing conidia, F with sterile cell F–H conidia I colony on MEA. Scale bars: 100 µm (A); 5 µm (B–H).

Discussion

Arthrinium is thought to represent the asexual morph of Apiospora because genetic data of Ap. montagnei (type species of Apiospora, Müller and Arx 1962) grouped together with other species of Arthrinium (Crous and Groenewald 2013; Senanayake et al. 2015; Réblová et al. 2016). Unfortunately, no data from the type species of Arthrinium, A. caricicola, was available to confirm this synonymy. In the present work, a phylogenetic relationship was found between a specimen identified as A. caricicola and other species of Arthrinium mainly occurring in Carex sp., such as A. curvatum var. minus, A. japonicum, A. puccinioides and A. sporophleum. Moreover, this clade was not significantly related with all other species of Arthrinium and Apiospora found in other hosts or substrates, suggesting that both clades could be interpreted as independent genera sister to Nigrospora. In this case, the synonymy between Arthrinium and Apiospora could be rejected, requiring new combinations. However, this hypothesis should be further confirmed after the analysis of the remaining known species occurring in Cyperaceae hosts, such as A. austriacum, A. fuckelii, A. globosum, A. kamtschaticum, A. morthieri, A. muelleri, or A. naviculare.

Arthrinium species have been found in several different plant hosts (Ramos et al. 2010; Sharma 2014), where they sometimes cause plant diseases (Martínez-Cano et al. 1992; Mavragani et al. 2007; Chen et al. 2014; Li et al. 2016). They are also isolated from lichens (He and Zhang 2012), marine algae (Suryanarayanan 2012), soil (Singh et al. 2013) and can even cause infections in humans (Rai 1989; Zhao et al. 1990; Hoog et al. 2000). In the present study six new species of Arthrinium are proposed: A. balearicum, A. descalsii, A. esporlense, A. ibericum, A. italicum, and A. piptatheri, all of them found in the Mediterranean biogeographical region, excepting for A. ibericum, which was found in the Atlantic areas of Spain. All these new taxa were found growing on plant hosts of the Poaceae family, such as Arundo donax or Piptatherum miliaceum. However, A. marii was the species most frequently found in the surveys, occurring on the Poaceae grasses Ampelodesmos mauritanicus and Phragmites australis, in agreement with the data reported by Crous and Groenewald (2013). Arthrinium phragmitis was found also on Phragmites australis and less commonly in Arundo donax, while A. hysterinum and A. rasikravindrae were associated with the Poaceae bamboos Phyllostachys aurea and Bambusa sp. Several colonies of A. rasikravindrae were found growing on Phyllostachys aurea as well, where they developed acervular conidiomata, a feature not observed in the protologue of this species, and therefore not considered diagnostic, in the same way as conidial shape, presence of setae, or lobate sterile cells.

Apiospora tintinnabula (Samuels et al. 1981) is considered a synonym of A. hysterinum (Sivanesan 1983; Kirk 1986). Multigenic data from the ex-type culture ICMP 6889 of Ap. tintinnabula was obtained so as to compare it with the newly found specimens of A. hysterinum, and no significant difference could be found. Interestingly, the collections of A. hysterinum studied in the present work presented sterile lobed cells, a feature not mentioned in the protologue of Ap. tintinnabula. The genetic data available from Ap. setosa and Ap. bambusae (28S and tub2) are not significantly different from those of A. hysterinum and Ap. tintinnabula, although additional markers would be needed to confirm a putative synonymy.

Acknowledgements

We thank Dr Hermann Voglmayr for his valuable advice, Chris Yeates and Martin Bemmann for providing literature, and Äsa Kruys for providing details about type collection of Arthrinium caricicola.

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