they seldom occur alone - knaw · coleophoma coptospermatis cbs 251.39 thuja plicata, seedling uk:...

f u n g a l b i o l o g y 1 2 0 ( 2 0 1 6 ) 1 3 9 2e1 4 1 5

journa l homepage : www.e lsev ier . com/ loca te / funb io

They seldom occur alone

Pedro W. CROUSa,b,c,*, Johannes Z. GROENEWALDa

aCBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The NetherlandsbDepartment of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute (FABI),

University of Pretoria, 0002 Pretoria, South AfricacMicrobiology, Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands

a r t i c l e i n f o

Article history:

Received 11 March 2016

Received in revised form

16 May 2016

Accepted 19 May 2016

Available online 30 May 2016

Corresponding Editor:

Ana Crespo

Keywords:

Dothideales

Helotiales

Multigene phylogeny

Systematics

* Corresponding author. CBS-KNAW Fungal Bfax: þ31 30 2122600.

E-mail address: [email protected] (P. Whttp://dx.doi.org/10.1016/j.funbio.2016.05.0091878-6146/ª 2016 British Mycological Society

a b s t r a c t

Species of Coleophoma have been reported as plant pathogenic, saprobic or endophytic on

a wide host range. The genus is characterised by having pycnidial conidiomata, phialidic

conidiogenous cells intermingled among paraphyses, and cylindrical conidia. Coleophoma

has had a confusing taxonomic history with numerous synonyms, and its phylogeny has re-

mained unresolved. The aim of the present study was to use a polyphasic approach incor-

porating morphology, ecology, and molecular data of the partial large subunit of nrDNA

(LSU), the internal transcribed spacer region with intervening 5.8S nrDNA (ITS), partial b-tu-

bulin (tub2), and translation elongation factor 1-alpha (tef1) gene sequences to resolve its tax-

onomy and phylogeny. Based on these results the genus was found to be polyphyletic, with

taxa tentatively identified as Coleophoma clustering in Dothideomycetes and Leotiomycetes. Spe-

cies corresponding to the concept of Coleophoma s.str. (Dermateaceae, Helotiales, Leotiomycetes)

were found to form a distinct clade, with five new species. Furthermore, Coleophoma was

found to be linked to the newly established sexual genus, Parafabraea, which is reduced to

synonymy. Isolates occurring on Ilex aquifolium in the Netherlands also clustered in Derma-

teaceae, representing a novel genus, Davidhawksworthia. In the Dothideomycetes, several taxa

clustered in Dothiora (Dothideaceae, Dothideales), which is shown to have Dothichiza and Hormo-

nema-like asexual morphs, with four new species. Furthermore, Pseudocamaropycnis is intro-

duced as a new genus (Mytilinidiaceae, Mytilinidiales), along with Briansuttonomyces

(Didymellaceae, Pleosporales) and Dimorphosporicola (Pleosporaceae, Pleosporales).

ª 2016 British Mycological Society. Published by Elsevier Ltd. All rights reserved.

Introduction hyaline, collapsing paraphyses, and discrete, integrated phia-

The genus Coleophoma (von H€ohnel 1907), typified by Coleo-

phoma crateriformis, was established to accommodate coelo-

mycetous fungi that are presently known to be plant

pathogenic, saprobic or endophytic, occurring on awide range

of host plants. Coleophoma is characterised by having pycnidial

conidiomata with well developed lower, but poorly developed

upper walls, hyaline conidiophores intermingled among

iodiversity Centre, Uppsa

. Crous).

. Published by Elsevier L

lidic conidiogenous cells with prominent periclinal thicken-

ing, and smooth, hyaline, cylindrical, guttulate, straight

conidia with obtuse ends (Nag Raj 1978; Sutton 1980).

Species of Coleophoma differ in their ecology, being endo-

phytic (e.g. Coleophoma prunicola in living leaves of Prunus lusi-

tanica; Duan et al. 2007), saprobic (Coleophoma empetri on leaf

litter; Wu et al. 1996), and plant pathogenic, e.g. Coleophoma

fusiformis on leaves of Rhododendron (Sutton 1980; Duan et al.

lalaan 8, 3584 CT Utrecht, The Netherlands. Tel.: þ31 30 2122643;

td. All rights reserved.

mailto:[email protected]

http://crossmark.crossref.org/dialog/?doi=10.1016/j.funbio.2016.05.009&domain=pdf

http://www.elsevier.com/locate/funbio

http://dx.doi.org/10.1016/j.funbio.2016.05.009



They seldom occur alone 1393

2007), Coleophoma eucalypti and Coleophoma eucalyptorum on Eu-

calyptus (Yuan 1996; Crous et al. 2011), C. empetri on Vaccinium

(Polashock et al. 2009), Coleophoma gevuinae on Gevuina

(Bianchinotti & Rajchenberg 2004), and Coleophoma proteae on

Protea caffra (Crous et al. 2012).

Based on the phylogenetic position of C. crateriformis, De

Gruyter et al. (2009) placed Coleophoma in Dothideales, while

Coleophoma maculans grouped in Helotiales, showing the genus

to be paraphyletic (Tanaka et al. 2015). In a subsequent study,

Thambugala et al. (2014) confirmed Coleophoma s.str. to belong

to Dothideales (Dothideaceae), being closely related to species of

Dothiora and Cylindroseptoria. However, Dothiora is typified by

Dothiora pyrenophora, which has Dothichiza sorbi as asexual

morph (Sivanesan 1984). Cylindroseptoria is typified by Cylindro-

septoria ceratoniae, but Cylindroseptoria pistacina was allocated

to Neocylindroseptoria by Thambugala et al. (2014), as the genus

was paraphyletic.

Several genera have to date been reduced to synonymy un-

derColeophomabasedonmorphology,namelyBasilocula,Ceutho-

sira, and Xenodomus (Nag Raj 1978), as well as Coleonaema,

Bactropycnis, and Rhabdostromina (Sutton 1980). Given differ-

ences in conidiomatal development between Coleonaema and

Coleophoma, however, Duan et al. (2007) were of the opinion

that Coleonaema, typified by Coleonaema oleae, should again be

resurrected as distinct genus. Other than the few isolates in-

cluded in phylogenetic studies dealing with other genera in

Dothideales, the genus Coleophoma, which clearly includes sev-

eral species associated with important plant diseases, remains

insufficiently known, and in urgent need of revision (Sutton

1980). The aim of the present study was thus to employ mor-

phology and multigene phylogenetic data to clarify relation-

ships of Coleophoma among other genera in Dothideaceae, to

resolve theparaphyletic nature of thegenus, and also try to elu-

cidate thehost rangeof thevarious speciesknownfromculture.

Materials and methods

Isolates

The majority of the isolates used in this study were obtained

from the culture collection of the CBS-KNAW Fungal Biodiver-

sity Centre (CBS), Utrecht, The Netherlands. Isolates included

were through the years identified as species of Coleophoma

based on the fact that they had pycnidial conidiomata, and cy-

lindrical conidia. In addition, fresh collections were made

from conidiomata on symptomatic leaves of diverse hosts.

Single conidial colonies were established from sporulating

conidiomata on Petri dishes containing pine needle agar

(PNA) (Smith et al. 1996), 2 % malt extract agar (MEA), potato-

dextrose agar (PDA), and oatmeal agar (OA) (Crous et al.

2009b), and incubated at 25 �C under continuous near-

ultraviolet light to promote sporulation.

DNA isolation, amplification, sequencing, and phylogeneticanalysis

Genomic DNAwas isolated from fungal mycelium growing on

MEA or OA, using the UltraClean� Microbial DNA Kit (MO Bio,

Carlsbad, CA, USA). The internal transcribed spacer region

(ITS) was amplified with the primers ITS5 and ITS4 (White

et al. 1990), or V9G (De Hoog & Gerrits van den Ende 1998),

the large subunit of nrDNA (LSU) with LR0R (Vilgalys &

Hester 1990) or LSU1Fd (Crous et al. 2009a) and LR5 (Vilgalys

& Hester 1990), the b-tubulin gene (tub2) with T1 (O’Donnell

& Cigelnik 1997) or Bt-2a and Bt-2b (Glass & Donaldson 1995),

and translation elongation factor 1-alpha (tef1) with EF1-728F

(Carbone & Kohn 1999) and EF-2 (O’Donnell et al. 1998) or

EF1-986R (Carbone & Kohn 1999). PCR and reaction mixtures

followed Groenewald et al. (2013) for ITS, tef1, and tub2, and

Crous et al. (2009a) for LSU. PCR products were sequenced in

both directions and a consensus sequence calculated, as de-

scribed by Gomes et al. (2013).

Phylogenetic analyses

Novel sequences generated in this study were blasted against

the NCBI’s GenBank nucleotide database to determine the

closest relatives for a taxonomic framework of the studied iso-

lates. Alignments of different gene regions, including se-

quences obtained from this study and sequences

downloaded from GenBank, were initially performed by using

the MAFFT v. 7 online server (http://mafft.cbrc.jp/alignment/

server/index.html) (Katoh & Standley 2013), and then manu-

ally adjusted in MEGA v. 6.06 (Tamura et al. 2007). To check

the congruence of different gene regions, individual gene trees

were manually compared prior to concatenation. Maximum

parsimony (MP; LSU overview and species phylogenies) and

Bayesian analyses (LSU overview phylogenies) were used to

determine the phylogenies. The MP analyses were conduct

in PAUP v. 4.0b10 (Swofford 2003) with the heuristic search op-

tion set to 100 random taxa addition, and the tree bisection-

reconnection (TBR) as the branch-swapping algorithm. All

characters were weighted equally and alignment gaps were

treated as new state data and bootstrap analyses were based

on 1000 replications. Tree length (TL), consistency index (CI),

retention index (RI), and rescaled consistency index (RC)

values were also calculated. Bayesian analyses were per-

formed in MrBayes v. 3.2.5 (Ronquist et al. 2012) and the best

nucleotide substitution model per gene region was selected

using MrModeltest v. 2.3 (Nylander 2004). The Markov Chain

Monte Carlo (MCMC) analysis used four chains and started

from a random tree topology. The heating parameter was set

to 0.2 and trees were sampled every 100 generations. Analyses

stopped once the average standard deviation of split frequen-

cies was below 0.01. Sequences generated in this study were

deposited in GenBank (Table 1) and alignments and phyloge-

netic trees in TreeBASE (www.treebase.org). Nomenclatural

novelties were deposited in MycoBank (Crous et al. 2004).

Morphology

Observations were made with a Nikon SMZ25 stereo-

microscope, and with a Zeiss Axio Imager 2 light microscope

using differential interference contrast (DIC) illumination

and a Nikon DS-Ri2 camera and software. Colony characters

and pigment production were noted after 2 wk of growth on

MEA, PDA, and OA incubated at 25 �C. Colony colours (surface

and reverse) were rated according to the colour charts of

Rayner (1970). Morphological descriptions were based on

http://mafft.cbrc.jp/alignment/server/index.html

http://mafft.cbrc.jp/alignment/server/index.html

http://www.treebase.org

Table 1 e Details of strains included in the molecular and morphological analyses.

Species Culture collectiona,b Isolation source Locality Collector GenBank accession numbersc

ITS LSU tef1 tub2

Briansuttonomyces eucalypti CBS 114879ET; CPC 362 Eucalyptus leaf litter South Africa: Western Cape

Province, Grabouw

P.W. Crous KU728479 KU728519 e KU728595

Briansuttonomyces eucalypti CBS 114887; CPC 363 Eucalyptus leaf litter South Africa: Western Cape

Province, Grabouw

P.W. Crous KU728480 KU728520 e KU728596

Coleophoma caliginosa CBS 124806ET; CPC 14048 Eucalyptus caliginosa,

leaves

Australia: New South

Wales, Northern

Tablelands, Mt Mackenzie

Nature Reserve

B.A. Summerell GU973505 KR858881 e e

Coleophoma camelliae CBS 101376ET Camellia japonica, rotting

petals

New Zealand: New

Plymouth, Taranaki

L. Mattson KU728481 KU728521 KU728558 KU728597

Coleophoma coptospermatis CBS 251.39 Thuja plicata, seedling UK: England, Devon,

Dartmoor

F.R. Peace KU728482 KU728522 KU728559 KU728598

Coleophoma coptospermatis CPC 19864ET Coptosperma littorale, leaf

spots

South Africa: Western Cape

Province, Kirstenbosch

P.W. Crous KU728483 KU728523 KU728560 KU728599

Coleophoma cylindrospora CBS 449.70 Liriodendron tulipifera,

decaying leaves

Netherlands: Utrecht

Province, Baarn, Groeneveld

H.A. van der Aa KJ663834 KJ663874 KU728561 KU728600

Coleophoma cylindrospora CBS 502.76 Helleborus sp., leaf Italy: Val Molino near

Bezzecca

W. Gams KU728484 KU728524 KU728562 KU728601

Coleophoma cylindrospora CBS 505.71; IFO 32644 Empetrum nigrum, dry

leaves

Germany: Kr. Wittmund,

Knyphauser Wald

W. Gams KU728485 KU728525 KU728563 KU728602

Coleophoma cylindrospora CBS 591.70 Vinca minor, leaf spot Netherlands: Utrecht

Province, Baarn,

Cantonspark

H.A. van der Aa KU728486 KU728526 KU728564 KU728603

Coleophoma cylindrospora CBS 592.70 Hedera helix, leaf spot on

living and withering

leaves

Netherlands: Gelderland

Province, Putten,

Schovenhorst


Coleophoma ericicola CBS 301.72ET Erica cinerea, leaf UK: England, Cornwall,

Bodmin Moor


Coleophoma eucalypticola CBS 124810ET; CPC 13755 Eucalyptus globulus Australia: Victoria, Otway I. Smith GQ303279 GQ303310 e e

Coleophoma eucalyptorum CBS 131314ET; CPC 19299 Eucalyptus piperita,

leaves

Australia: New South

Wales, Blue Mountains,

Kurrajong Heights

B.A. Summerell JQ044430 JQ044449 KU728567 KU728606

Coleophoma eucalyptorum CPC 19293 Eucalyptus gummifera,

leaves

Australia: Northern

Territory, Darwin


Coleophoma eucalyptorum CPC 19865 Coptosperma littorale, leaf

spots

South Africa: Western Cape



Coleophoma

paracylindrospora

CBS 109074ET Hypericum sp., leaf spot New Zealand: Auckland,

Great North Road, Western

Springs Garden

C.F. Hill KU728491 KU728531 KU728570 KU728609

Coleophoma

paracylindrospora

CBS 115328 Amelanchier lamarckii,

dead leaf


Province, Baarn, Park

Kasteel Groeneveld

P.W. Crous & G.

Verkley

KU728492 KU728532 KU728571 KU728610

Coleophoma parafusiformis CBS 129169; MSCL 1028 Rhododendron sp. Latvia: Riga I. Apine KU728493 KU728533 KU728572 KU728611

1394

P.W

.Cro

us,

J.Z.Gro

enewald

Coleophoma parafusiformis CBS 132692ET; Rhod 1-1 Rhododendron sp., leaf

spot

Sweden: Uppsala O. Pettersson KU728494 KU728534 KU728573 KU728612

Coleophoma proteae CBS 132532ET; CPC 19714 Protea caffra, leaves South Africa: Gauteng

Province, Roodepoort,

Walter Sisulu National

Botanical Gardens

P. Crous, M.K.

Crous & M. Crous

JX069866 JX069850 KU728574 KU728613

Coleophoma sp. 1 CBS 896.69 Populus balsamifera,

prematurely fallen leaf


Province, Baarn, garden

Eemnesserweg 90

H.A. van der Aa KU728495 EU754147 KU728575 KU728614

Coleophoma sp. 2 CPC 20683 Lauriade leaf litter Netherlands: Utrecht

Province, Bilthoven,

Sweelincklaan 87


Davidhawksworthia ilicicola CBS 261.95; PD 94/1488 Ilex aquifolium Netherlands: Noord-

Holland Province, Aalsmeer

J.W. Veenbaas KU728516 KU728555 KU728592 KU728630

Davidhawksworthia ilicicola CBS 734.94ET; PD 94/1488 Ilex aquifolium, fruit Netherlands: Noord-

Holland Province, Aalsmeer

J.W. Veenbaas KU728517 KU728556 KU728593 KU728631

Dimorphosporicola tragani CBS 570.85ET; PD 84/500 Traganum nudatum var.

microphyll, leaf

Mauritania e KU728497 KU728536 KU728577 KU728616

Dothiora agapanthi CPC 20600ET Agapanthus sp., leaves South Africa: Western Cape



Dothiora bupleuricola CBS 112.75ET Bupleurum fruticosum,

leaf spot

France: Avignon, Roche des

Domes


Dothiora cannabinae CBS 737.71ET; ETH 2929 Daphne cannabina, twig India: Himalaya, Kumaon,

Chaubattia (Almora)

S.K. Bose AJ244243 DQ470984 e e

Dothiora ceratoniae CBS 290.72 Nerium oleander, dead

leaves

Italy: Sardegna, Cala Fuili W. Gams & J.A.

Stalpers

KU728500 KU728539 KU728580 KU728619

Dothiora ceratoniae CBS 441.72 Arbutus unedo, dead leaf Italy: Sardegna, Tacco di

Santa Barbara

W. Gams & J.A.

Stalpers

KU728501 KU728540 KU728581 KU728620

Dothiora ceratoniae CBS 477.69ET Ceratonia siliqua, leaves Spain: Mallorca, Can Pastilla H.A. van der Aa KF251151 KF251655 KF253111 KF252649

Dothiora elliptica CBS 736.71; ETH 7587 Vaccinium uliginosum,

twig

Switzerland: Tourbi�ere des

Ponts de Martel

L. Froidevaux KU728502 KU728541 e e

Dothiora laureolae CBS 744.71ET; ETH 7578 Daphne laureola, twig Italy: Sicilia, La Rocca

Busambra

L. Froidevaux KU728503 KU728542 e e

Dothiora maculans CBS 299.76 Populus tremuloides, leaf

litter

Canada: Rocky Mountains S. Visser KU728504 KU728543 KU728582 KU728621


litter

Canada: Alberta S. Visser KU728505 KU728544 KU728583 KU728622


litter

Canada: Alberta S. Visser KU728506 KU728545 KU728584 KU728623

Dothiora maculans CBS 686.70 Acer pseudoplatanus, leaf Netherlands: Utrecht

Province, Baarn


Dothiora oleae CBS 152.71 Olea europaea, rotting

fruit

Turkey: IzmireBornova S. Aksu KU728508 KU728547 KU728586 KU728625

Dothiora oleae CBS 235.57 Olea europaea, leaves Italy O. Verona KU728509 KU728548 KU728587 KU728626

Dothiora oleae CBS 472.69 Olea europaea, fallen

leaves, very old tree

Spain: Mallorca, Fornalutx

(ca 900 m)


Dothiora oleae CBS 615.72; ATCC 24520;

DSM 62123

Olea europaea, fallen leaf Greece R. Schneider KU728511 EU754148 KU728589 KU728628

(continued on next page)

Theyse

ldom

occu

ralone

1395

Table

1e

(con

tinued

)

Species

Culture

collectiona,b

Isolationso

urce

Loca

lity

Collector

GenBankacc

essionnumbers

c

ITS

LSU

tef1

tub2

Dothiora

phaeosp

erma

CBS870.71;ETH

7591

Loniceracoerulea

Switze

rland:Kt.

Graub€ unden,Celerina

L.Fro

idevaux

KU728512

KU728550

ee

Dothiora

phillyreae

CBS473.69ET

Phillyreaangu

stifolia,leaf

litter

Spain:Mallorca,ElArenal,

dunesbehindboulevard

H.A

.vanderAa

KU728513

EU754146

KU728590

KU728629

Dothiora

prunorum

CBS933.72ET

Prunusdom

estica

cv.

‘BelledeLouvain’,fruit

UK

eAJ244248

KU728551

ee

Dothiora

sorbi

CBS742.71;ETH

7563

Sorbusaria,tw

igSwitze

rland:Vaud,Ste

Cro

ix

L.Fro

idevaux

KU728514

KU728552

ee

Dothiora

sp.

CBS135.78;PD

77/922

Prunuslaurocerasu

sNeth

erlands:

Wageningen

ee

KU728553

ee

Dothiora

viburnicola

CBS274.72ET

Viburnum

tinus,deadleaf

Italy:Sard

egna,Tacc

odi

Santa

Barb

ara

W.Gams&

J.A.

Stalpers

KU728515

KU728554

KU728591

e

Pseudocamaropycnis

pini

CBS115589ET;HKUCC10098

Pinuselliotii,leaf

China:HongKong,Yung

ShueO

eKU728518

KU728557

KU728594

KU728632

aATCC:A

merica

nTypeCulture

Collection,V

A,U

SA;C

PC:C

ulture

collectionofPedro

Cro

us,

house

datCBS;D

SM:D

eutsch

eSammlungvonMikro

organismenundZellkulturenGmbH,B

raunsc

hweig,

Germ

any;ETH:SwissFederalInstitute

ofTech

nologyCulture

Collection,Zurich

,Switze

rland;HKUCC:TheUniversityofHongKongCulture

Collection,HongKong,China;IFO:Institute

forFerm

en-

tation,Osa

ka,Japan;MSCL:Micro

bialStrain

CollectionofLatvia,Facu

ltyofBiology,UniversityofLatvia,Latvia;PD:PlantPro

tectionService,nVW

A,DivisionPlant,W

ageningen,TheNeth

erlands.

bET:extypecu

lture.

cITS:intern

altransc

ribedsp

ace

rsandintervening5.8SnrD

NA;LSU:partial28SnrD

NA;tef1:partialtranslationelongationfactor1-alphagene;tub2:partialb-tubulingene.

1396 P. W. Crous, J. Z. Groenewald

cultures sporulating on PNA or OA at �1000 magnification,

with at least 30 measurements per structure, with extremes

given in brackets.

Results

Phylogenetic analyses

Based on the Blast results, the strains were divided into over-

view LSU phylogenies of Leotiomycetes and Dothideomycetes,

and subsequently multigene (ITS, tub2, tef1) species phyloge-

nies were generated for species belonging to the genera Coleo-

phoma and Dothiora, respectively.

The overview LSU/ITS phylogeny of Leotiomycetes consisted

of 46 sequences, including the outgroup sequence Neofusicoc-

cum umdonicola (GenBank KF766373, EU821904). A total of

1334 characters were included in the phylogenetic analyses;

245 characters were parsimony-informative, 155 were vari-

able and parsimony-uninformative, and 934 characters were

constant. A total of 391 equally most parsimonious trees

were obtained, the first of which is shown in Fig 1 (TL ¼ 970,

CI¼ 0.631, RI¼ 0.803, and RC¼ 0.507). In the Bayesian analysis,

the LSU partition had 112 unique site patterns and the ITS par-

tition 219 unique site patterns, and the analysis ran for 820 000

generations, resulting in 16 402 trees of which 12 302 trees

were used to calculate the posterior probabilities which are

mapped unto Fig 1. Both partitions were analysed with

MrBayes using dirichlet (1,1,1,1) state frequency distribution

and inverse gamma-shaped rate variation across sites

(GTR þ I þ G). The main difference between the Bayesian

and MP tree was the position of the Pezicula clade; in the

Bayesian tree this genus clustered sister to Coleophoma

whereas it was sister to the lineage containing Davidhawks-

worthia to Neofabraea in the parsimony analysis (data not

shown, see TreeBASE). The LSU region alone lacked sufficient

resolution to resolve the lineages in Dermateaceae and the

Coleophoma clade remainedwithout support in both the Bayes-

ian and MP analyses, therefore the LSU sequences were com-

bined with ITS sequences.

The overview LSU phylogeny of Dothideomycetes consisted

of 58 sequences, including the outgroup sequence Pseudo-

phloeospora eucalypti (GenBank HQ599593). A total of 819 char-

acters were included in the phylogenetic analyses; 206

characters were parsimony-informative, 62 were variable

and parsimony-uninformative, and 551 characters were con-

stant. A maximum of 1000 equally most parsimonious trees

were obtained, the first of which is shown in Fig 2 (TL ¼ 652,

CI¼ 0.612, RI¼ 0.916, and RC¼ 0.561). In the Bayesian analysis,

this partition had 230 unique site patterns in the analysis ran

for 1 750 000 generations, resulting in 35 002 trees of which

26 252 trees were used to calculate the posterior probabilities

which are mapped unto Fig 2. The LSU partition was analysed

with MrBayes using dirichlet (1,1,1,1) state frequency distribu-

tion and inverse gamma-shaped rate variation across sites

(GTR þ I þ G). The Bayesian and MP tree had the same overall

topology, with some rearrangements of species within fami-

lies (data not shown, see TreeBASE). Coleophoma-like isolates

occurred in four different families representing three different

orders in this phylogeny (see the Taxonomy section below).

3x-/100

0.55/-

1/100

1/100

1/100

1/83

1/100

1/1001/92

1/71

1/87

0.96/100

0.99/90

1/99

1/99

1/99

0.70/80

0.87/82

0.99/96

1/961/87

0.72/68

0.52/66

0.92/-

0.66/-

0.80/680.97/83

Phacidiaceae

Phac

idia

les

Hel

otia

les

Hemiphacidiaceae

Rutstroemiaceae

Dermateaceae

10 changes

Neofusicoccum umdonicola KF766373/EU821904Allantophomopsis cytisporea KJ663869/KJ663830

Scleromitrula shiraiana AY789407/AY789408

Bulgaria inquinans DQ470960/KJ663831

Phacidium lacerum KJ663882/KJ663841

Coleophoma sp. CBS 896.69

Sarcotrochila longispora KJ663877/KJ663836

Allantophomopsiella pseudotsugae KJ663868/KJ663829Potebniamyces pyri DQ470949/DQ491510

Phacidium trichophori KJ663895/KJ663854Phacidium pseudophacidioides KJ663893/KJ663852

Pezicula melanigena KR859003/KR859211Pezicula radicicola KR859029/KR859237

Heyderia abietis AY789296/AY789297Vestigium trifidum KC407777/KC407777

Coleophoma caliginosa CBS 124806Coleophoma eucalypticola CBS 124810

Davidhawksworthia ilicicola CBS 261.95Davidhawksworthia ilicicola CBS 734.94

Pseudofabraea citricarpa KR859075/KR859281

Coleophoma sp. CPC 20683

Coleophoma parafusiformis CBS 129169Coleophoma parafusiformis CBS 132692

Phlyctema vagabunda AY064705/AY064704

Neofabraea brasiliensis KR107002/KR107002

Coleophoma ericicola CBS 301.72

Phlyctema vincetoxici KF251710/KF251207Phlyctema vincetoxici KF251711/KF251208

Neofabraea kienholzii KR858873/KR859082Neofabraea malicorticis KR858877/KR859086

Coleophoma camelliae CBS 101376

Coleophoma coptospermatis CBS 251.39Coleophoma coptospermatis CPC 19864

Coleophoma proteae CBS 132532Coleophoma cylindrospora CBS 449.70Coleophoma cylindrospora CBS 502.76Coleophoma cylindrospora CBS 505.71Coleophoma cylindrospora CBS 592.70Coleophoma “empetri” FJ588252/FJ480116Coleophoma cylindrospora CBS 591.70Coleophoma “empetri” FJ588253/FJ480126

Coleophoma eucalyptorum CPC 19293Coleophoma eucalyptorum CPC 19865Coleophoma eucalyptorum CBS 131314

Coleophoma paracylindrospora CBS 109074Coleophoma paracylindrospora CBS 115328

Fig 1 e The first of 391 equally most parsimonious trees derived from the combined Leotiomycetes LSU/ITS alignment.

Bootstrap support values greater than 50 % and Bayesian posterior probabilities are given at the nodes (Bayesian posterior

probability/parsimony bootstrap). Thickened branches represent those branches present in the parsimony strict consensus

tree and the scale bar represents the number of changes. The branch to the outgroup node was shortened three times to

simplify layout of the tree. The families and orders are indicated with blocks of different colours and strains treated in the

present study are printed in bold face. The tree was rooted to Neofusicoccum umdonicola (GenBank KF766373, EU821904).


The overview LSU phylogeny of Dothideomycetes consisted

of 58 sequences, including the outgroup sequence P. eucalypti

(GenBank HQ599593). A total of 819 characters were included

in the phylogenetic analyses; 206 characters were

parsimony-informative, 62 were variable and parsimony-

uninformative, and 551 characters were constant. A maxi-

mum of 1000 equally most parsimonious trees were obtained,

the first of which is shown in Fig 2 (TL ¼ 652, CI ¼ 0.612,

RI ¼ 0.916, and RC ¼ 0.561). In the Bayesian analysis, this par-

tition had 230 unique site patterns in the analysis ran for

1 750 000 generations, resulting in 35 002 trees of which

26 252 trees were used to calculate the posterior probabilities

which are mapped unto Fig 2. The LSU partition was analysed

with MrBayes using dirichlet (1,1,1,1) state frequency distribu-

tion and inverse gamma-shaped rate variation across sites.

The Bayesian and MP tree had the same overall topology,

with some rearrangements of species within families (data

not shown, see TreeBASE). Coleophoma-like isolates occurred

in four different families representing three different orders

in this phylogeny (see the Taxonomy section below).

Pseudophloeospora eucalypti HQ599593 Kirschsteiniothelia maritima GU323203

Neocylindroseptoria pistaciae KF251656

Karstenula rhodostoma GU301821

Pseudocamaropycnis pini CBS 115589

Pseudoseptoria collariana KF251721 Pseudoseptoria obscura KF251722

Aureobasidium pullulans DQ470956 Aureobasidium proteae JN712557

Pleospora herbarum GU238160

Faurelina indica GU180654

Kalmusia ebuli JN644073

Lophium mytilinum EF596819

Endoconidioma populi HM185488

Camarosporium quaternatum DQ377884

Xenodidymella humicola GU238086

Mytilinidion rhenanum FJ161175 Mytilinidion scolecosporum FJ161186

Dothidea sambuci AY930108 Dothidea insculpta DQ247802

Delphinella strobiligena DQ470977 Sydowia polyspora DQ678058

Diphorphosporicola tragani CBS 570.85

Verrucoconiothyrium nitidae JN712516

Phaeodothis winteri GU301857 Bimuria novae-zelandiae AY016356

Montagnula anthostomoides GU205223 Montagnula aloes JX069847

Dothiora ceratoniae CBS 290.72 Dothiora ceratoniae CBS 441.72 Dothiora ceratoniae CBS 477.69

Neocamarosporium betae EU754179

Didymella exigua EU754155 Saccothecium sepincola GU301870

Dothiora sorbi CBS 742.71

Dothiora laureolae CBS 744.71 Dothiora cannabinae CBS 737.71

Neocamarosporium calvescens EU754131 Chaetosphaeronema hispidulum EU754145

Briansuttonomyces eucalypti CBS 114879 Briansuttonomyces eucalypti CBS 114887 Nothophoma gossypiicola GU238079

Dothiora maculans CBS 299.76 Dothiora maculans CBS 301.76 Dothiora maculans CBS 302.76 Dothiora maculans CBS 686.70

Dothiora elliptica CBS 736.71 Dothiora prunorum CBS 933.72 Dothiora phaeosperma CBS 870.71

Dothiora bupleuricola CBS 112.75 Dothiora sp. CBS 135.78 Dothiora viburnicola CBS 274.72 Dothiora phillyreae CBS 473.69 Dothiora oleae CBS 472.69 Dothiora oleae CBS 152.71 Dothiora oleae CBS 235.57 Dothiora oleae CBS 615.72 Dothiora agapanthi CPC 20600

25 changes

3x

3x

3x

3x

Mytilinidiaceae

Myt

ilini

-di

ales

Didymosphaeriaceae

Pleo

spor

ales

Dot

hide

ales

Pleosporaceae

Aureobasidiaceae

Didymellaceae

Dothideaceae

-/100

1/100

0.99/74

0.94/-

0.86/-

0.73/-

0.56/-

0.90/-

1/100

1/100

1/881/98

1/99

0.76/59

0.85/62

1/100

1/100

1/98

0.63/-

0.62/-

0.79/-

0.83/-

0.77/-

1/-

1/99

1/91

0.98/59

1/70

1/98

1/98

0.97/69

0.98/76

1/81

0.90/59

1/93

Fig 2 e The first of 1000 equally most parsimonious trees derived from the Dothideomycetes LSU alignment. Bootstrap support

values greater than 50 % and Bayesian posterior probabilities are given at the nodes (Bayesian posterior probability/parsi-

mony bootstrap). Thickened branches represent those branches present in the parsimony strict consensus tree and the scale

bar represents the number of changes. Some branches were shortened three times to simplify layout of the tree. The families

and orders are indicated with blocks of different colours and strains treated in the present study are printed in bold face. The

tree was rooted to Pseudophloeospora eucalypti (GenBank HQ599593).


The multigene (ITS, tef1, tub2) phylogeny of Coleophoma

s.str. consisted of 23 strains, including the two outgroup iso-

lates of Davidhawksworthia ilicicola (CBS 734.94 and CBS

261.95). A total of 1364 characters were included in the phylo-

genetic analyses; 436 characters were parsimony-informative,

118 were variable and parsimony-uninformative, and 810

characters were constant. Two equally most parsimonious

trees were obtained, the first of which is shown in Fig 3

(TL ¼ 1 393, CI ¼ 0.664, RI ¼ 0.770, and RC ¼ 0.511). The tree re-

solved twelve Coleophoma species, two of which were sterile

and therefore not named at the present time (see Taxonomy

section below).

20 changes

Davidhawksworthia ilicicola

Coleophoma sp. 1

Coleophoma sp. 2

Coleophoma ericicola

Co. proteae

Co. coptospermatis

Co. cylindrospora

Co. parafusiformis

Co. paracylindrospora

Co. camelliae

Co. eucalyptorum

100

75

100

100

55

90

61

70

100

100

99

100

65

CBS 896.69 Populus balsamifera Netherlands

CBS 261.95

CBS 734.94

CBS 301.72 Erica cinerea UK

CBS 124810 Eucalyptus globulus Australia

CBS 124806 Eucalyptus caliginosa Australia

CBS 132532 Protea caffra South Africa

CBS 449.70 Liriodendron tulipifera Netherlands

CPC 20683 Lauriade litter Netherlands

CBS 251.39 Thuja plicata UK

CPC 19864 Coptosperma littorale South Africa

CBS 502.76 Helleborus sp. Italy

CBS 505.71 Empetrum nigrum Germany

CBS 591.70 Vinca minor Netherlands

CBS 592.70 Hedera helix Netherlands

CBS 129169 Rhododendron sp. Latvia

CBS 132692 Rhododendron sp. Sweden

CBS 109074 Hypericum sp. New Zealand

CBS 115328 Amelanchier lamarckii Netherlands

CBS 101376 Camellia japonica New Zealand

CBS 131314 Eucalyptus piperita Australia

CPC 19293 Eucalyptus gummifera Australia

CPC 19865 Coptosperma littorale South Africa

3x

3x

Coleophoma eucalypticola

Coleophoma caliginosa

Fig 3 e The first of two equally most parsimonious trees derived from the Coleophoma s.str. combined (ITS, tef1, tub2)

alignment. Bootstrap support values greater than 50 % are given at the nodes. Thickened branches represent those branches

present in the parsimony strict consensus tree and the scale bar represents the number of changes. Some branches were

shortened three times to simplify layout of the tree. The species are indicated with blocks of different colours and extype

cultures are printed in bold face. The tree was rooted to sequences of Davidhawksworthia ilicicola (CBS 734.94 and CBS 261.95).


The multigene (ITS, tef1, tub2) phylogeny of Dothiora s.str.

consisted of 21 strains, including the outgroup Pseudoseptoria

obscura (GenBank KF251219, KF253175, and KF252708, respec-

tively). A total of 1181 characters were included in the phylo-

genetic analyses; 211 characters were parsimony-

informative, 253 were variable and parsimony-

uninformative, and 717 characters were constant. Three

equally most parsimonious trees were obtained, the first of

which is shown in Fig 4 (TL ¼ 816, CI ¼ 0.812, RI ¼ 0.804, and

RC ¼ 0.654). The tree resolved 13 Dothiora species (see the

Taxonomy section below).

Taxonomy

Results obtained in this study revealed isolates tentatively

identified as ‘Coleophoma spp.’ to cluster in diverse clades,

which explains the confusion in present literature. Taxa

are therefore treated in alphabetical order per family

below.

Dermateaceae, Helotiales, Leotiomycetes

Coleophoma H€ohn., Sber. Akad. Wiss. Wien, Math.-naturw. Kl.,

Abt. 1, 116: 637 (1907).

Synonyms: Basilocula Bub�ak, Annls. Mycol. 12: 210 (1914).

Rhabdostromellina H€ohn., Annls. Mycol. 15(5): 303 (1917).

Bactropycnis H€ohn., Hedwigia 62: 65 (1920).

Rhabdostromina Died., Annls. Mycol. 19: 297 (1921).

Xenodomus Petr., Annls. Mycol. 20: 206 (1922).

Ceuthosira Petr., Annls. Mycol. 22: 265 (1924).

Parafabraea Chen Chen et al., Fungal Biol. 120: 1291 (2016).

100

100

83

100

100

68

83

53

59

69

72

52

52

Dothiora viburnicola

Dothiora bupleuricola

Dothiora oleae

Dothiora phillyreae

Dothiora ceratoniae

Dothiora agapanthi

Dothiora maculans

Pseudoseptoria obscura KF251219/KF253175/KF252708

CBS 870.71 Lonicera coerulea Switzerland

CBS 736.71 Vaccinium uliginosum Switzerland

CBS 933.72 Prunus domestica UK

CBS 742.71 Sorbus aria Switzerland

CBS 274.72 Viburnum tinus Italy

CBS 737.71 Daphne cannabina India

CBS 744.71 Daphne laureola Italy

CBS 112.75 Bupleurum fruticosum France

CPC 20600 Agapanthus sp. South Africa

CBS 473.69 Phillyrea angustifolia Spain

CBS 152.71 Olea europaea Turkey

CBS 615.72 Olea europaea Greece

CBS 235.57 Olea europaea Italy

CBS 472.69 Olea europaea Spain

CBS 299.76 Populus tremuloides Canada

CBS 477.69 Ceratonia siliqua Spain

CBS 441.72 Arbutus unedo Italy

CBS 290.72 Nerium oleander Italy



CBS 686.70 Acer pseudoplatanus Netherlands 20 changes

3x

Dothiora phaeosperma

Dothiora elliptica

Dothiora prunorum

Dothiora sorbi

Dothiora cannabinae

Dothiora laureolae

Fig 4 e The first of three equally most parsimonious trees derived from the Dothiora s.str. combined (ITS, tef1, tub2) align-

ment. Bootstrap support values greater than 50 % are given at the nodes. Thickened branches represent those branches

present in the parsimony strict consensus tree and the scale bar represents the number of changes. The branch to the

outgroup node was shortened three times to simplify layout of the tree. The species are indicated with blocks of different

colours and extype cultures are printed in bold face. The tree was rooted to sequences of Pseudoseptoria obscura (GenBank

KF251219, KF253175, and KF252708, respectively).


For synonymy see Nag Raj (1978), Sutton (1980), Duan et al.

(2007).

Mycelium immersed, consisting of branched, septate, hyaline

to pale brown hyphae. Ascomata apothecial, sessile to subses-

sile, short-stalked, gregarious or confluent, clustering on

a basal stroma, partly immersed, medium to dark brown. Disc

turbinate, pale brown. Seta-like structures surrounding apoth-

ecia, rigid, pale brown, septate, cylindrical, straight or slightly

curved, slightly enlarged at truncate apex. Basal stroma subim-

mersed, composed of irregular, pale to medium brown cells.

Asci inoperculate, clavate to cylindrical-clavate, apex rounded,

short-pedicellate, base truncate, hyaline to pale brown, 8-

spored. Ascospores inequilateral, fusoid to ellipsoid, ends

rounded, straight or slightly curved, aseptate, thin-walled, hy-

aline, guttulate. Paraphyses numerous, cylindrical, slender,

wider at base, septate, apex round, hyaline to pale brown. Con-

idiomata pycnidial, separate, globose or flattened at the base,

black, immersed, unilocular; wall composed of brown, thick-

walled textura angularis; lowerwall often thicker thanupper re-

gion. Ostiole single, circular, not papillate. Paraphyses hyaline,

septate at the base, intermingled among conidiophores, cylin-

drical or long clavate, collapsing atmaturity.Conidiophores pale

brown at the base, hyaline above, branched, septate, smooth,

thin-walled, formed from the inner cells of the pycnidial

wall, sometimes confined to the base, or in short chains. Coni-

diogenous cells phialidic, determinate, discrete and ampulli-

form to lageniform, or integrated and subcylindrical, hyaline,


smooth, with prominent periclinal thickening, and collarette

minute. Conidia hyaline, aseptate, cylindrical, apex obtuse,

base acute, thin-walled, smooth, guttulate, straight (adapted

from Sutton 1980; Cheewangkoon et al. 2009).

Type species: Coleophoma crateriformis (Durieu & Mont.) H€ohn.

Notes: Presently there is no culture available of C. crateriformis.

TheculturederivedfromCBSH-10464isrepresentativeofaDothi-

chizaasexualmorphofaDothiorasp. (seebelow).Thismeans that

taxonomic conclusions drawn by De Gruyter et al. (2009), and

thus by default also Thambugala et al. (2014), are incorrect.

Parafabraea, the recently introduced genus for two species oc-

curring on Eucalyptus (Chen et al. 2016), was found in the pres-

ent study to represent the sexual morph of Coleophoma,

a genus hitherto not known from any sexual connections. Par-

afabraea is therefore reduced to synonymy under the older ge-

nus, Coleophoma.

Coleophoma caliginosa (Cheew. et al.) Crous, comb. nov.

MycoBank No.: MB816128

Basionym: Cryptosporiopsis caliginosaCheew. et al., Fungal Divers.

44: 93 (2010).

Synonym: Parafabraea caliginosa (Cheew. et al.) Chen Chen et al.,

Fungal Biol. 120: 1291 (2016).

Description and illustrations: Cheewangkoon et al. (2010).

Material examined: Australia: New South Wales, Northern Ta-

blelands, Mt Mackenzie Nature Reserve (290504S; 1515805E)

on leaves of Eucalyptus caliginosa, 1 Feb. 2007, B.A. Summerell

(holotype CBS H-20301, culture extype CPC 14048 ¼ CBS

124806, CPC 14049, 14050).

Coleophoma camelliae Crous, sp. nov. (Fig 5).


Etymology: Named after the host genus from which the type

strain was isolated, Camellia.

Conidiomata pycnidial, brown, erumpent, globose, to 300 mm

diam; wall of 2e6 layers of brown textura angularis. Paraphyses

intermingled among conidiophores, hyaline, subcylindrical,

0e1-septate, to 70 mm long, 2e5 mm diam, with clavate apical

Fig 5 e Coleophoma camelliae (CBS 101376). (A) Colony sporulatin

bars [ 10 mm.

part. Conidiophores hyaline, smooth, subcylindrical, 1e3-

septate, 15e30 � 3e4 mm. Conidiogenous cells hyaline, smooth,

subcylindrical to ampulliform, apical or lateral on conidio-

phores, 10e20 � 2.5e3 mm; tapering towards a truncate apex,

1e1.5 mmdiam, withminute periclinal thickening. Conidia sol-

itary, guttulate to granular, hyaline, smooth, subcylindrical,

apex obtuse, base tapered towards flattened scar, 0.5e1 mm

diam (12e)16e18(e20) � 2.5e3 mm.

Material examined: New Zealand: New Plymouth, Taranaki, on

rotting petals of Camellia japonica, coll. L. Mattson, isol. C.F. Hill

(holotype CBS H-22474, culture extype CBS 101376).

Culture characteristics: Colonies erumpent, spreading, with

moderate aerial mycelium, margins lobate, reaching 30 mm

diam after 2 wk on MEA, 70 mm diam on OA, and 60 mm

diam on PDA. On MEA surface mouse-grey, reverse mouse-

grey. On PDA surface mouse-grey, reverse olivaceous grey.

On OA surface mouse-grey.

Notes: Morphologically Coleophoma camelliae is similar to C.

empetri, which we regard as synonym of C. cylindrospora. Coleo-

phoma camelliae is therefore introduced as novel species based

on its distinct phylogeny.

Coleophoma coptospermatis Crous, sp. nov. (Fig 6).



strain was isolated, Coptosperma.

Conidiomata pycnidial, brown, immersed to superficial, glo-

bose, to 300 mmdiam; wall of 2e6 layers of brown textura angu-

laris. Paraphyses intermingled among conidiophores, hyaline,

subcylindrical, 0e1-septate, to 90 mm long, 4e6 mm diam, ta-

pering towards obtusely rounded apex. Conidiophores hyaline,

smooth, subcylindrical, 0e3-septate, 10e25 � 3e4 mm. Coni-

diogenous cells hyaline, smooth, subcylindrical to ampulliform

or doliiform, apical or lateral on conidiophores,

7e10 � 2.5e3.5 mm; tapering towards a truncate apex,

0.5e1 mmdiam, withminute periclinal thickening. Conidia sol-

itary, guttulate, hyaline, smooth, subcylindrical, apex obtuse,

base tapered towards flattened scar, 1.5e2 mm diam (16e)

18e25(e27) � 3(e3.5) mm.

g on OA. (B, C) Conidiogenous cells. (D) Conidia. Scale

Fig 6 e Coleophoma coptospermatis (CPC 19864). (A, D) Foliar disease symptoms. (B) Sporulation on PNA. (C, E) Conidiogenous

cells and paraphyses. (F) Conidia. Scale bars [ 10 mm.


Materials examined: South Africa: Western Cape Province,

Kirstenbosch, leaf spots on Coptosperma littorale, 11 Sep. 2011,

P.W. Crous (holotype CBS H-22475, culture extype CPC

19864).UK: England, Devon, Dartmoor, on seedling of Thuja pli-

cata, 1939, F.R. Peace, CBS 251.39.

Culture characteristics: Colonies flat, spreading, with moderate

aerial mycelium, margins lobate, reaching 50 mm diam after

2 wk. On MEA surface mouse-grey, reverse iron-grey. On

PDA surface mouse-grey, reverse iron-grey. On OA surface

dark mouse-grey.

Notes: Coleophoma coptospermatis, isolated from leaf spots on

Coptosperma littorale together with C. eucalyptorum, appears to

be closely related to an isolate from Thuja plicata in the UK

(Fig 3). However, we suspect that the latter may represent

a distinct species, but this matter can only be resolved once

more isolates become available. Based on the species of Coleo-

phoma recognised by Sutton (1980), C. coptospermatis is closest

to C. cylindrospora, although it has longer conidia.

Coleophoma crateriformis (Durieu & Mont.) H€ohn., Mitt. bot.

Inst. tech. Hochsch. Wien 2(3): 77 (1925) (Fig 7).

Basionym: Ascospora crateriformis Durieu & Mont., in Durieu,

Expl. Sci. Alg. 1(livr. 15): 590 (1849) [1846e1849].

For synonyms see Sutton (1980).

Conidiomata hypophyllous, rarely amphigenous, solitary, to

250 mm diam, rarely aggregated, subepidermal, erumpent

with papillate central ostiole; mature conidiomata appear

acervulus-like as the upper layers disintegrate, leaving almost

a cup-like conidioma; wall of brown, thick-walled textura

angularis, sides and bottom thick, becoming thinner towards

ostiole. Conidiophores lining the inner cavity, 0e2-septate, hya-

line, smooth. Conidiogenous cells integrated, short cylindrical or

irregularly cuboid, giving rise to solitary conidia; terminal cells

appearing as paraphyses on conidiophores, hyaline, smooth,

remaining sterile, becoming gelatinised, up to 17 � 5 mm. Con-

idia cylindrical, hyaline, smooth, apex obtuse, base narrowly

truncate, aseptate (11e)14e16(e17) � (2e)2.5e3(e3.5) mm,

encased in a mucoid mass.

Material examined: Corsica: Bastia, on leaf litter of Phillyrea me-

dia, 16 Apr. 1905, von H€ohnel (holotype FH 00304449). Spain:

Mallorca, El Arenal, dunes behind boulevard, on leaf litter of

Phillyrea angustifolia, 20 May 1969, H.A. van der Aa, CBS H-

10464.

Notes: Ascomata of aMycosphaerella sp.were also observed to be

present on the holotype (FH 00304449). A second specimen de-

posited at CBS (CBS H-10464) had conidia which were similar

in size (11e)14e15(e16) � 2.5e3(e3.5) mm. A culture (CBS

473.69)derivedfromthis specimen,however,wasofaDothichiza

asexualmorph that belongs toDothiora (Sivanesan 1984),which

also cooccurred on this material (see below).

Coleophoma cylindrospora (Desm.) H€ohn., Ber. dt. bot. Ges. 37:

114 (1919) (Fig 8).

Basionym: Sphaeropsis cylindrospora Desm., Annls. Sci. Nat., Bot.,

s�er. 3, 11: 227 (1849).

Synonyms: Phoma cylindrospora (Desm.) Sacc., Michelia 1(no. 5):

527 (1879).

Macrophoma cylindrospora (Desm.) Berl. & Voglino, Atti Soc.

Veneto-Trent. Sci. Nat. 10(1): 192 (1886).

Septoria empetri Rostr., Meddr Grønland, Biosc. 3: 574 (1888).

Coleophoma empetri (Rostr.) Petr., Annls. Mycol. 27: 331 (1929).

Bactropycnis concentrica H€ohn., Hedwigia 62: 65 (1920).

Conidiomata pycnidial, brown, immersed to erumpent, glo-



subcylindrical, 0e1-septate, to 100 mm long, 3e6 mm diam,

with swollen apical part, fusoid, tapering towards obtusely

rounded apex. Conidiophores hyaline, smooth, subcylindrical,

1e6-septate, 15e45 � 3e4 mm. Conidiogenous cells hyaline,

smooth, subcylindrical to ampulliform, apical or lateral on co-

nidiophores, 5e10 � 3e4 mm; tapering towards a truncate

apex, 1e2 mmdiam, with minute periclinal thickening. Conidia

Fig 8 e Coleophoma cylindrospora (CBS 591.70). (A) Colony sporulating on PNA. (B, C) Conidiogenous cells and paraphyses. (D)

Conidia. Scale bars [ 10 mm.

Fig 7 e Coleophoma crateriformis (FH 00304449). (A) Conidiomata in vivo. (B, C) Conidiogenous cells (note dissolving paraphyses

in B). (D) Conidia. Scale bars [ 10 mm.


solitary, with large guttules, hyaline, smooth, subcylindrical,

apex obtuse, base tapered towards flattened scar, 0.5 mm

diam (15e)18e20(e22) � (2.5e)3 mm (based on CBS 592.70).

Materials examined: Germany: Kr. Wittmund, Knyphauser

Wald, leaf litter of Empetrum nigrum, 30 May 1971, W. Gams,

CBS H-10479, culture CBS 505.71. Italy: Val Molino near Bez-

zecca, on leaf of Helleborus sp., W. Gams, Jun. 1976, CBS

502.76. Netherlands: Province Gelderland, Putten, Schoven-

horst, leaf spot on Hedera helix, 13 May 1970, H.A. van der Aa,

culture CBS 592.70; Province Utrecht, Baarn, Cantonspark,

leaf spot on Vinca minor, 28 Apr. 1970, H.A. van der Aa, CBS

H-10471, culture CBS 591.70; Baarn, Groeneveld, decaying

leaves of Liriodendron tulipifera, 1 Mar. 1970, H.A. van der Aa,

CBS 449.70. Tyrol: on dead leaves of Hedera canariensis, 5 Aug.

1918, W. Pfaff (holotype of Bactropycnis concentrica, FH

00304451).


aerial mycelium,margins lobate, reaching 50e80mmdiam af-

ter 2 wk. On MEA surface dirty white, reverse cinnamon with

patches of mouse-grey. On PDA surface mouse-grey, with

patches of cinnamon, reverse iron-grey. On OA surface

mouse-grey.

Notes: Sutton (1980) retained C. cylindrospora (from Hedera helix,

conidia cylindrical with large guttules, 16.5e24 � 2.5e3 mm) as

distinct from C. empetri (from Empetrum nigrum, conidia cylin-

drical with small guttules, 12.5e18 � 2e3 mm). Strangely

enough, conidia of our isolate from Hedera helix (CBS 592.70)

fit the circumscription of C. cylindrospora, whereas conidia

from Empetrum nigrum (CBS 505.71) tend to be shorter, with

small guttules (12e)14e16(e19) � (2.5e)3 mm, fitting the cir-

cumscription of C. empetri. We therefore reduce C. empetri to

synonymy under the older name, C. cylindrospora, as they are

phylogenetically not distinguished.

Furthermore, examination of the holotype of Bactropycnis con-

centrica (Fig 9) found it to contain Phyllosticta concentrica, as well

as material of B. concentrica (conidia cylindrical with large gut-

tules, 20e24 � 3e3.5 mm), a small-spored Coleophoma sp. (con-

idia 9e11 � 2e2.5 mm), and a Colletotrichum sp. Bactropycnis

concentrica is thus regarded as additional synonym of C.

cylindrospora.

Coleophoma ericicola Crous, sp. nov. (Fig 10).



strain was isolated, Erica.

Conidiomata pycnidial, brown, immersed to erumpent, glo-



subcylindrical, 0e2-septate, to 30 mm long, 1.5e3 mm diam,

with obtusely rounded apex. Conidiophores hyaline, smooth,

subcylindrical, 0e1-septate, 7e15� 2e3 mm. Conidiogenous cells

hyaline, smooth, subcylindrical, apical or lateral on conidio-

phores, 5e10 � 1.5e2.5 mm; tapering towards a truncate

apex, 1e1.5 mm diam, with minute periclinal thickening. Con-

idia solitary, guttulate to granular, hyaline, smooth, subcylin-

drical (ends becoming swollen with age), apex obtuse, base

tapered towards flattened scar, 0.5 mm diam (8e)

10e12(e13) � 2(e2.5) mm.

Fig 9 e Bactropycnis concentrica (FH 00304451). (A) Conidiomata in vivo. (B, C) Conidiogenous cells and paraphyses. (D) Conidia.

Scale bars [ 10 mm.

Fig 10 e Coleophoma ericicola (CBS 301.72). (A, B) Colony sporulating on OA. (C, D) Conidiogenous cells and paraphyses. (E)



Material examined: UK: England, Cornwall, Bodmin Moor, on

leaf of Erica cinerea, 6 Sep. 1971, H.A. van der Aa (holotype

CBS H-22476, culture extype CBS 301.72).

Culture characteristics: Colonies flat, spreading, with sparse ae-

rial mycelium, margins feathery, reaching 30 mm diam after

2 wk on MEA, 6 mm diam on OA, and 40 mm diam on PDA.

On MEA surface and reverse iron-grey. On PDA surface isabel-

line to cinnamon, reverse sepia. On OA surface iron-grey.

Notes: A single species is known to occur on Erica, namely

C. ericae, which has significantly larger conidia, namely

16e22 � 2.5e3 mm (von H€ohnel 1920), being more similar to

those of C. cylindrospora. Based on its smaller conidia and

distinct phylogeny, C. ericicola is herewith introduced as new

species.

Coleophoma eucalypticola Crous, comb. et nom. nov.


Basionym: Neofabraea eucalypti Cheew. & Crous, Persoonia 23: 67

(2009).

Synonym: Parafabraea eucalypti (Cheew. & Crous) Chen et al.,

Fungal Biol. 120: 1291 (2016).

Description and illustrations: Cheewangkoon et al. (2009).

Material examined: Australia: Victoria, Otway, on Eucalyptus

globulus, 15 Feb. 2007, coll. I. Smith, isol. P.W. Crous (holotype

CBS H-20285, culture extype CPC 13755 ¼ CBS 124810, CPC

13756, 13757).

Notes: Parafabraea was recently described as a sexual

morph similar to Neofabraea and Pezicula, but being distinct

by having seta-like structures around its apothecia (Chen

et al. 2016). In the present study however, Parafabraea

was found to be the sexual morph of Coleophoma, which is

a much older, and well-established genus. Because the epi-

thet ‘eucalypti’ is occupied in Coleophoma (Yuan 1996), a new

name, eucalypticola, is introduced to accommodate this

fungus.

Coleophoma eucalyptorum Crous & Summerell, Persoonia 27:

137 (2011) (Fig 11).

Description and illustration: See Crous et al. (2011).

Materials examined: Australia: New South Wales, Blue Moun-

tains, Kurrajong Heights, on leaves of Eucalyptus piperita, 16

Nov. 2010, B.A. Summerell (holotype CBS H-20770, culture

extype CBS 131314); Northern Territory, Darwin, on leaves

of Eucalyptus gummifera, 9 Apr. 2011, P.W. Crous, CPC 19293.

South Africa: Western Cape Province, Kirstenbosch, leaf

Fig 11 e Coleophoma eucalyptorum (CPC 19865). (A, B) Conidiogenous cells and paraphyses. (C) Conidia. Scale bars [ 10 mm.


spots on Coptosperma littorale, 11 Sep. 2011, P.W. Crous, CPC

19865.

Notes: Coleophoma eucalyptorum was found to cooccur with C.

coptospermatis on the same leaf spots on Coptosperma littorale

in South Africa. Contrary to what was first believed, this spe-

cies appears to have a wider host range than only Eucalyptus.

Coleophoma paracylindrospora Crous, sp. nov. (Fig 12).


Etymology: Named after its morphological similarity to C.

cylindrospora.

Conidiomata pycnidial, brown, erumpent, globose, to 300 mm

diam; wall of 2e6 layers of brown textura angularis. Paraphyses

intermingled among conidiophores, hyaline, subcylindrical,

0e4-septate, to 100 mm long, 2e6 mm diam, branched or not,

with obtusely rounded apex. Conidiophores hyaline, smooth,

subcylindrical, branched, 1e3-septate, 7e25 � 3e4 mm. Coni-

diogenous cells hyaline, smooth, subcylindrical to allantoid,

apical or lateral on conidiophores, 7e15 � 2.5e3.5 mm; taper-

ing towards a truncate apex, 1e1.5 mm diam, with minute

periclinal thickening. Conidia solitary, guttulate to granular,

hyaline, smooth, cylindrical, apex obtuse, base tapered to-

wards flattened scar, 1e1.5 mm diam (15e)

17e20(e22) � (2.5e)3 mm.

Materials examined: Netherlands: Prov. Utrecht, Baarn, Park

Kasteel Groeneveld, on leaves of Amelanchier lamarckii, P.W.

Crous & G. Verkley, 16 Mar. 2004, CBS H-20230, culture CBS

Fig 12 e Coleophoma paracylindrospora (CBS 109074). (A) Colony s

and paraphyses. (F) Conidia. Scale bars [ 10 mm.

115328. New Zealand: Auckland, Great North Road, Western

Springs Garden, leaf spot on Hypericum sp., 7 Aug. 2000, C.F.

Hill (holotype CBS H-22477, culture extype CBS 109074).

Culture characteristics: Colonies spreading, surface folded, with

sparse to moderate aerial mycelium, margins lobate, reaching

40 mm diam after 2 wk on MEA, 80 mm diam on OA, and

60 mm diam on PDA. On MEA surface fuscous-black, dark

mouse-grey. On PDA surface mouse-grey, reverse iron-grey.

On OA surface mouse-grey.

Note: Coleophoma paracylindrospora is morphologically similar

to C. cylindrospora, and can only be distinguished based on

DNA phylogenetic data.

Coleophoma parafusiformis Crous, sp. nov. (Fig 13).


Etymology: Named after the Coleophoma fusiformis, to which it

has some resemblance.

Conidiomata pycnidial, brown, immersed to erumpent, globose

with central ostiole, to 250 mm diam; wall of 2e6 layers of

brown textura angularis. Paraphyses intermingled among co-

nidiophores, hyaline, subcylindrical, 0e2-septate, to 120 mm

long, 3e7 mm diam, with obtusely rounded apex. Conidiophores

hyaline, smooth, subcylindrical, branched, 0e3-septate,

13e35� 3e5 mm. Conidiogenous cells hyaline, smooth, subcylin-

drical, apical or lateral on conidiophores, 7e17 � 2.5e3.5 mm;

tapering towards a truncate apex, 1.5e2 mmdiam,withminute

porulating on OA. (BeE) Conidiophores, conidiogenous cells,

Fig 13 e Coleophoma parafusiformis (CBS 129169). (A) Colony sporulating on OA. (B, C) Conidiogenous cells and paraphyses. (D)



periclinal thickening. Conidia solitary, with large guttules, hy-

aline, smooth, cylindrical to fusoid, irregularly curved or

straight, apex obtuse, base tapered towards flattened scar,

2 mm diam (15e)17e20(e22) � (4e)5(e6) mm.

Materials examined: Latvia: Riga, on Rhododendron sp., I. Apine,

CBS 129169¼MSCL 1028. Sweden: Uppsala, on leaf spot of Rho-

dodendron sp., Nov. 2010, O. Pettersson (holotype CBS H-22478,

culture extype CBS 132692).

Culture characteristics: Colonies erumpent, folded, spreading,

with moderate aerial mycelium, margins lobate to feathery,

reaching 20e30 mm diam after 2 wk. On MEA surface dark

mouse-grey, reverse greyish sepia. On PDA surface greyish se-

pia, reverse isabelline. On OA surface honey.

Notes: Wu et al. (1996) introduced C. fusiformis as a novel spe-

cies on Rhododendron in the UK, distinguishing it from the

other Coleophoma spp. on Rhododendron on the basis that it

had fusiform conidia, and was regarded to be a pathogen of

this host. Conidia of C. fusiformis are fusiform to cylindrical,

21e25 � 4e4.5 mm, thus larger than that of C. parafusiformis,

and also much more prominently tapered, whereas conidia

of C. parafusiformis are also more irregular in shape. Further-

more, in C. fusiformis the paraphyses dissolve at maturity,

but this is not the case in C. parafusiformis. The second species

known to occur on Rhododendron, C. empetri (¼C. cylindrospora,

see above), differs in having conidia that are more cylindrical,

and slightly narrower (15e)18e20(e22) � (2.5e)3 mm.

Coleophoma proteae Crous, Persoonia 28: 163 (2012).

Description and illustration: See Crous et al. (2012).

Material examined: South Africa: Gauteng Province, Roode-

poort, Walter Sisulu National Botanical Gardens, on leaves of

Protea caffra, 5 Jul. 2011, P. Crous, M.K. Crous & M. Crous (holo-

type CBS H-20962, culture extype CBS 132532).

Note: Coleophoma proteae is associated with a leaf spot disease

on Protea caffra in South Africa, and has thus far not been re-

ported on any other host (Crous et al. 2012).

Davidhawksworthia Crous, gen. nov.


Etymology: Named after David L. Hawksworth, in recognition

to his many significant contributions to fungal taxonomy.

Colonies giving rise to spreading, hyaline, septate hyphae that

tend to becomepigmented, forming chains of chlamydospore-

like structures. Conidiophores dimorphic, thin-walled. Macroco-

nidiophores erect, basal part hyaline or pale brown, smooth.

Microconidiophores penicillate, similar in morphology. Macroco-

nidiogenous cells hyaline, smooth, apical, phialidic, clavate,

with apical opening and collarette, or arising from a mother

cell that gives rise to several ampulliform to doliiform phia-

lides. Macroconidia aseptate, cylindrical with obtuse ends and

a flattened hilum at base, hyaline, smooth, granular, straight,

frequently aggregated in cylindrical packets.

Type species: Davidhawksworthia ilicicola Crous.

Davidhawksworthia ilicicola Crous, sp. nov. (Fig 14).


Etymology: Named after the host genus from which it was iso-

lated, Ilex.

Colonies giving rise to spreading, hyaline, septate hyphae (on

SNA), 3e4 mm diam, but hyphae tend to become pigmented

on MEA, with chains of chlamydospore-like structures. Conid-

iophores dimorphic. Macroconidiophores erect, basal part hya-

line or pale brown, smooth, to 200 mm tall, 3e4 mm diam.

Microconidiophores penicillate, similar in morphology, to

100 mm tall. Macroconidiogenous cells hyaline, smooth, apical,

phialidic, clavate, 20e30 � 3e4 mm, with apical opening and

collarette, or arising from a mother cell that gives rise to sev-

eral ampulliform to doliiform phialides, 5e14 � 3e4 mm. Mac-

roconidia aseptate, cylindrical with obtuse ends and a flattened

hilum at base, 1 mm diam, hyaline, smooth, granular, straight,

frequently aggregated in cylindrical packets (17e)

18e20(e22) � 3(e3.5) mm.

Materials examined: Netherlands: Prov. Noord-Holland, Aals-

meer, fruit of Ilex aquifolium, Jan. 1995, J.W. Veenbaas (holotype

CBS H-22479, culture extype CBS 734.94); Aalsmeer, fruit of Ilex

aquifolium, Apr. 1995, J.W. Veenbaas, CBS 261.95.

Culture characteristics: Colonies flat, folded, spreading, with

moderate aerial mycelium, margins smooth, even, reaching

Fig 14 e Davidhawksworthia ilicicola (CBS 734.94). (A) Colony sporulating on OA. (B) Microconidiophores and conidia. (C)

Macro- and microconidiophores and conidia. (DeF) Macroconidiogenous cells and macroconidia. (G) Macroconidia. Scale

bars [ 10 mm.


30e50 mm diam after 2 wk. On MEA surface mouse-grey, re-

verse olivaceous grey. On PDA surface mouse-grey, reverse

pale mouse-grey. On OA surface dark mouse-grey.

Notes: Davidhawksworthia is reminiscent of Cylindrodendrum

(Lombard et al. 2014, 2015), but can be distinguished in that

the conidia are aseptate, and formed on phialides that fre-

quently arise from a mother cell. Furthermore, on SNA it

also develops penicillate microconidiophores, which are

never observed in Cylindrodendrum.

Dothideaceae, Dothideales, Dothideomycetes

Dothiora Fr., Summa veg. Scand., Section Post. (Stockholm): 418

(1849).

Synonyms: Stigmea Bonord., Abh. naturforsch. Ges. (Halle) 8: 79

(1864).

Dothichiza Lib. ex Roum., Fungi Selecti Galliaei Exs.: no. 627

(1880).

Dothiora subgen. Metadothis Sacc., Syll. Fung. (Abellini) 8: 766

(1889).

Metadothis (Sacc.) Sacc., Syll. Fung. (Abellini) 10: 857 (1892).

Leptodothiora H€ohn., Ber. dt. bot. Ges. 36: 311 (1918).

Keisslerina Petr., Annls. Mycol. 17: 74 (1920) [1919].

Coleonaema H€ohn., in Weese, Mitt. bot. Inst. tech. Hochsch. Wien

1(3): 95 (1924).

Jaapia Kirschst., Krypt.-Fl. Brandenburg (Leipzig) 7(3): 444 (1938).

Cylindroseptoria Quaedvl., Verkley & Crous, Stud. Mycol. 75: 358

(2013).

Synonyms from Thambugala et al. (2014), with the addition of

Coleonaema, Cylindroseptoria, and Dothichiza.

Ascostromata immersed to erumpent, pulvinate to globose,

black, multiloculate; wall of dark brown textura angularis.

Locules globose to subglobose, broadly rounded or papillate

with central ostiole. Pseudoparaphyses absent. Asci 8- or

more spored, bitunicate, fissitunicate, oblong to clavate, ped-

icellate, with a small ocular chamber. Ascospores biseriate to

multiseriate, septate, constricted at the primary median sep-

tum, at times with a vertical septum, hyaline, rarely pale

brown, obovate to ellipsoid to fusoid, often inequilateral or

slightly curved, smooth, at times with a thin mucoid sheath.

Conidiomata pycnidial, separate, or aggregated in a stroma.

Conidiophores reduced to conidiogenous cells lining the inner

cavity, hyaline, smooth, ampulliform to doliiform, phialidic.

Conidia aseptate, hyaline, smooth, subcylindrical to ovoid or

oblong. Hyphae becoming brown, verruculose, and con-

stricted at septa, giving rise to a Hormonema-like synasexual

morph.

Notes: The genus Dothiora, including its type species D. pyreno-

phora, contains numerous species that have been linked to

Dothichiza asexual morphs via cultural studies (Froidevaux

1972; Sivanesan 1984), several also producing Hormonema-

like asexual morphs in culture. In the present study, several

species of Dothiora with Dothichiza asexual morphs clustered

with extype strains of Coleonaema and Cylindroseptoria in

a well-supported clade. Although no strains of the type spe-

cies Dothiora pyrenophora or Dothichiza populea are presently

known from culture, Dothiora appears the oldest name pres-

ently available for this clade, and hence we allocate these

taxa to it. Further collections would be required, however, to

designate an epitype for Dothiora pyrenophora, and fix the ap-

plication of this name. Both Dothiora and Dothichiza are in

need of revision, and very little information is currently avail-

able about their phylogeny. Several species of Dothiora are de-

scribed below, although only the Dothichiza or Hormonema-like

morphs can be observed in culture.

Fig 15 e Dothiora agapanthi (CPC 20600). (A, B) Colony sporulating on SNA. (C) Section through conidioma. (D) Conidia. Scale

bars [ 10 mm.


Dothiora agapanthi Crous, sp. nov. (Fig 15).



lated, Agapanthus.

Conidiomata separate, erumpent, pycnidial, globose with long

neck, brown, to 250 mm diam, with central ostiole, exuding

a creamy conidial mass; wall of 3e6 layers of brown textura

angularis. Conidiophores reduced to conidiogenous cells lining

the inner cavity, hyaline, smooth, ampulliform to doliiform,

5e7 � 5e6 mm, with central phialidic locus. Conidia hyaline,

smooth, guttulate, subcylindrical, apex obtuse, tapering to

a truncate hilum (8e)10e12(e13) � 3(e3.5) mm. Hyphae becom-

ing brown, verruculose, and constricted at septa, giving rise to

a Hormonema-like synasexual morph.

Material examined: South Africa: Western Cape Province, Kirst-

enbosch, on leaves of Agapanthus sp., May 2012, P.W. Crous

(holotype CBS H-22480, culture extype CPC 20600).


rial mycelium, margins feathery, covering dish after 2 wk. On

MEA, PDA, and OA and reverse iron-grey.

Notes: This fungus was originally isolated as a hyphomycete

(from the Hormonema-like morph), and its pycnidial

Fig 16 e Dothiora bupleuricola (CBS 112.75). (A, B) Colonies sporu

cells. (E) Conidia. Scale bars [ 10 mm.

conidiomata were only observed in culture. No species of

Dothiora or Dothichiza have thus far been reported from

Agapanthus.

Dothiora bupleuricola Crous, sp. nov. (Fig 16).



lated, Bupleurum.





the inner cavity, hyaline, smooth, globose to allantoid,



a truncate hilum (8e)9e10(e12) � 2(e2.5) mm.

Material examined: France: Avignon, Roche des Domes, on leaf

spot of Bupleurum fruticosum, Feb. 1975, H.A. van der Aa (holo-

type CBS H-22481, culture extype CBS 112.75).


rial mycelium, margins feathery, reaching 60 mm diam after

2 wk. On MEA, PDA, and OA surface fuscous black, reverse

iron-grey.

lating on PNA and PDA, respectively. (C, D) Conidiogenous


Notes: No species of Dothiora or Dothichiza have thus far been

reported from Bupleurum. Kabatiella bupleuri occurs on dead

flowers of Bupleurum gibraltarium in Spain, and has a Hormo-

nema-like growth in culture (Bills et al. 2012), but is morpholog-

ically and phylogenetically quite distinct.

Dothiora ceratoniae (Quaedvl., Verkley & Crous) Crous, comb.

nov.

MycoBank no.: MB816138

Basionym: Cylindroseptoria ceratoniaeQuaedvl., Verkley & Crous,

Stud. Mycol. 75: 358 (2013).

Description and illustration: See Quaedvlieg et al. (2013).

Materials examined: Italy: Sardegna, Cala Fuili, on dead leaves

of Nerium oleander, 10 May 1971, W. Gams & J. Stalpers, CBS

290.72; Sardegna, Tacco di Santa Barbara, on dead leaf ofArbu-

tus unedo, 10 May 1971, W. Gams & J. Stalpers, CBS 441.72.

Spain: Mallorca, Can Pastilla, on leaves of Ceratonia siliqua, 24

May 1969, H.A. van der Aa (holotype CBS H-21300, culture

extype CBS 477.69).

Notes: Cylindroseptoria ceratoniae is the type species of the ge-

nus Cylindroseptoria (Quaedvlieg et al. 2013), which is shown

to be a synonym of Dothiora. A new combination is herewith

introduced in Dothiora to accommodate this taxon.

Dothiora maculans (Ellis & Everh.) Crous, comb. nov. (Fig 17).


Basionym: Phyllosticta maculans Ellis & Everh., Proc. Acad. Nat.

Sci. Philad. 45: 157 (1893).

Synonym: Coleophomamaculans (Ellis & Everh.) Petr., in Petrak &

Sydow, Feddes Repert., Beih. 42: 471 (1927).

Conidiomata pycnidial, solitary, to 300 mm diam on OA, up to

150 mm on PNA, with central ostiole. Conidiogenous cells could

have 1e2 loci, and are aggregated in pseudochains, encased

in a thick, persistent mucoid layer. Conidia hyaline, smooth,

subcylindrical to oblong, guttulate, apex obtuse, tapering to

a truncate hilum (7e)10e12(e13) � (2.5e)3(e3.5) mm. Hormo-

nema-like synasexual morph with ampulliform to doliiform

phialidic conidiogenous cells, 5e7 � 5e6 mm (based on CBS

301.76).

Fig 17 e Dothiora maculans (CBS 301.76). (A, B) Colonies sporula

diogenous cells. (F) Conidia. Scale bars [ 10 mm.

Materials examined: Canada: Alberta, leaf litter of Populus trem-

uloides, May 1976, S. Visser, CBS 301.76; Alberta, leaf litter of P.

tremuloides, May 1976, S. Visser, CBS 302.76; Rocky Mountains,

leaf litter of P. tremuloides, Feb. 1976, S. Visser, CBS 299.76.

Netherlands: Prov. Utrecht, Baarn, leaf of Acer pseudoplatanus,

May 1974, H.A. van der Aa, CBS 686.70.

Culture characteristics: Colonies flat, spreading, surface folded,

with sparse aerial mycelium, margins feathery, covering

dish after 2 wk. On MEA, PDA, and OA surface and reverse

iron-grey.

Notes: The type specimen of ‘Phyllosticta’ maculans was de-

scribed from leaves of Populus monilifera collected in the USA

(conidia 10e14 � 3e3.5 mm), which fit well with the morphol-

ogy of the present cultures studied here, and thus we believe

these cultures to be representative for the name. Dothiora

sphaeroides (asexual morph: Dothichiza tremulae, conidia ob-

long, 4e10 � 2.5e3.5 mm) is known from Populus tremula and

P. tremuloides (Froidevaux 1972), but has smaller conidia.

Dothiora oleae (DC.) Crous, comb. nov. (Fig 18).


Basionym: Sphaeria oleae DC., in de Candolle & Lamarck, Fl.

franc., Edn 3 (Paris) 5/6: 136 (1815).

Synonyms: Coleonaema oleae (DC.) H€ohn., in Weese, Mitt. bot.

Inst. tech. Hochsch. Wien 1(3): 95 (1924).

Coleophoma oleae (DC.) Petr. & Syd., Beih. Reprium nov. Spec. Regni

veg. 42(1): 469 (1927) [1926].

Description and illustration: See Duan et al. (2007).

Materials examined: Greece: on fallen leaf of Olea europaea, Aug.

1972, R. Schneider, CBS 615.72 ¼ ATCC 24520 ¼ DSM 62123.

Italy: on leaves of Olea europaea, Mar. 1957, O. Verona, CBS

235.57. Spain: Mallorca, Fornalutx (ca 900 m) on fallen leaves

ofOlea europaea, 26 May 1969, H.A. van der Aa, CBS 472.69. Tur-

key: Izmir-Bornova, on rotting fruit of Olea europaea, 24 Nov.

1970, S. Aksu, CBS 152.71.

Culture characteristics: Colonies flat to erumpent, spreading,

with sparse aerial mycelium, margins lobate, reaching

40 mm diam after 2 wk. On MEA surface iron-grey, reverse

ting on PNA and OA, respectively. (C) Mycelium. (D, E) Coni-

Fig 18 e Dothiora oleae (CBS 615.72). (A, B) Colonies sporulating on OA and SNA, respectively. (C, D) Conidia. Scale

bars [ 10 mm.


olivaceous grey. On PDA surface iron-grey, reverse olivaceous

grey with diffuse isabelline pigment. On OA surface iron-grey.

Notes: Duan et al. (2007) resurrected the genus Coleonaema to

accommodate the fungus occurring on olive leaves, on the ba-

sis that it had a different conidiomatal development (more cu-

pulate conidiomata) to Coleophoma s.str., and dissolving

hyphal elements in its conidiomata (persistent paraphyses

in Coleophoma). In the present study we found Coleonaema to

cluster in the Dothiora clade, and hence a new combination

is herewith proposed.

Dothiora phillyreae Crous, sp. nov. (Fig 19).



lated, Phillyrea.

Conidiomata solitary or aggregated in a stroma, brown, im-

mersed in media (SNA), or superficial (OA), brown, to 300 mm

Fig 19 e Dothiora phillyreae (CBS 473.69). (A) Conidiomata in vivo

diogenous cells. (G) Conidia. Scale bars [ 10 mm.

diam, with central ostiole that bursts open to render the con-

idioma more acervular in appearance; wall of 3e6 layers of

brown textura angularis. Conidiophores reduced to conidioge-

nous cells lining the inner cavity, hyaline, smooth, aseptate,

ampulliform to broadly ellipsoid or doliiform,

5e10� 5e7 mm, holoblastic with apical locus, inconspicuously

phialidic. Conidia solitary, hyaline, smooth, subcylindrical to

oblong, guttulate, apex obtuse, tapering to a truncate hilum,

1 mm diam (8e)10e11(e12) � (2.5e)3(e3.5) mm. Colonies also

sporulating on superficial hyphae, forming a Hormonema-like

asexual morph, with hyphae becoming brown, verruculose,

constricted at septa, forming chlamydospore-like cells up to

8 mm diam; older conidia become brown and verruculose, up

to 15 mm long, 5 mm diam.

Material examined: Spain: Mallorca, El Arenal, dunes behind

boulevard, on leaf litter of Phillyrea angustifolia, 20 May 1969,

H.A. van der Aa (holotype CBS H-22482, culture extype CBS

473.69).

. (B) Colony sporulating on SNA. (CeF) Hyphae and coni-

Fig 20 e Dothiora viburnicola (CBS 274.72). (A, B) Colonies sporulating on SNA. (C, D) Hyphae giving rise to conidiogenous cells.

(E) Conidiogenous cells. (F) Conidia. Scale bars [ 10 mm.


Culture characteristics: Colonies flat, spreading, surface folded,

with sparse aerial mycelium, margins lobate, reaching

60 mm diam after 2 wk. On MEA, PDA, and OA surface and re-

verse fuscous-black.

Notes: ThiscultureofDothiora phillyreaewasderived fromaspec-

imen (CBS H-10464) of Coleophoma crateriformis, and incorrectly

assumed to represent the latter fungus, withwhich it cooccurs.

No species of Dothiora or Dothichiza are known from Phillyrea,

and hence this taxon is herewith described as new.

Dothiora prunorum (C. Dennis & Buhagiar) Crous, comb. nov.


Basionym: Aureobasidium prunorum C. Dennis & Buhagiar,

Trans. Br. Mycol. Soc. 60: 572 (1973).

Synonym: Hormonema prunorum (C. Dennis & Buhagiar) Herm.-

Nijh., Stud. Mycol. 15: 170 (1977).

Material examined: UK, fruit of Prunus domestica, cv. ‘Belle de

Louvain’, 1972, C. Dennis (extype CBS 933.72).

Dothiora viburnicola Crous, sp. nov. (Fig 20).



lated, Viburnum.



Fig 21 e Pseudocamaropycnis pini (CBS 115589). (AeD) Conidiopho



the inner cavity, hyaline, smooth, ampulliform to doliiform,



a truncate hilum (6.5e)8e10(e13) � (2e)2.5(e3) mm.

Material examined: Italy: Sardegna, Tacco di Santa Barbara, on

dead leaf of Viburnum tinus, May 1971, W. Gams & J.A. Stalpers

(holotype CBS H-22483, culture extype CBS 274.72).

Note: Dothiora viburnicola needs to be compared to Dothichiza

viburni (conidia ellipsoid-elongate, 6e8 � 2e3 mm; Karsten

1890), although conidia of the latter species are shorter.

Mytilinidiaceae, Mytilinidiales, Dothideomycetes

Pseudocamaropycnis Crous, gen. nov.


Etymology: Named after the genus Camaropycnis, which it mor-

phologically resembles.

Conidiomata erumpent, black, elongated, lens-shaped, opening

by irregular rupture. Paraphyses intermingled among conidio-

phores, hyaline, septate, branched, subcylindrical. Conidio-

phores hyaline, smooth, subcylindrical, septate, thin-walled,

branched. Conidiogenous cells hyaline, smooth, terminal and

lateral, subcylindrical, phialidic with minute periclinal thick-

ening, apex truncate. Conidia solitary, hyaline, smooth, cylin-

drical, straight, biguttulate.

res and conidiogenous cells. (E) Conidia. Scale bars[ 10 mm.


Type species: Pseudocamaropycnis pini Crous.

Pseudocamaropycnis pini Crous, sp. nov. (Fig 21).



lated, Pinus.

Conidiomata erumpent, black, elongated, lens-shaped, to

500 mm diam, opening by irregular rupture. Paraphyses inter-

mingled among conidiophores, hyaline, septate, branched,

subcylindrical, to 70 mm long, 1.5e2 mmdiam. Conidiophores hy-

aline, smooth, subcylindrical, 0e2-septate, branched,

10e25 � 2e3 mm. Conidiogenous cells hyaline, smooth, terminal

and lateral, subcylindrical, phialidic with minute periclinal

thickening, apex truncate, 1.5 mmdiam, 7e17� 2e2.5 mm. Con-

idia solitary, hyaline, smooth, cylindrical, straight, biguttulate

(5e)6e7(e8) � 1.5e2 mm.

Material examined: China: Hong Kong, Yung Shue O, on needles

of Pinus elliotii, 7 Jul. 2003, Q.S.Y. Yeung (holotype CBS H-22484,

culture extype CBS 115589).


aerial mycelium, margins lobate, reaching 20 mm diam after

2 wk. On MEA surface pale mouse-grey, reverse purplish

grey. On PDA surface pale mouse-grey, reverse mouse-grey.

On OA surface dark mouse-grey.

Notes: Based on its conidiophores and conidia, Pseudocamaro-

pycnis is morphologically similar to Camaropycnis (on

branches of Pinus and Libocedrus), but can be distinguished

by having conidiomata immersed in pine needles, and not

short-stipitate as in the latter (Sutton 1980). Similarly, its

conidiomata also distinguish it from Coleophoma s.str.

Pleosporaceae, Pleosporales, Dothideomycetes

Briansuttonomyces Crous, gen. nov.


Etymology: Named after Dr B.C. Sutton, in acknowledgement of

his valuable contributions to the taxonomy of coelomycetous

fungi.

Conidiomata erumpent, eutromatic, brown, globose, with cen-

tral ostiole; wall of 3e8 layers of medium brown textura angu-

laris. Conidiogenous cells lining inner cavity, hyaline, smooth,

thin-walled, ampulliform to globose, phialidic with periclinal

thickening, and minute collarette. Conidia solitary, hyaline,

Fig 22 e Briansuttonomyces eucalypti (CBS 114887). (AeC) C

smooth, guttulate to granular, cylindrical with obtuse ends,

(0e)1-septate, mostly straight.

Type species: Briansuttonomyces eucalypti Crous.

Briansuttonomyces eucalypti Crous, sp. nov. (Fig 22).



lated, Eucalyptus.

Colonies poorly sporulating on MEA, sterile on SNA, PDA, and

OA. Conidiomata erumpent, eutromatic, brown, globose, to

350 mm diam, with central ostiole; wall of 3e8 layers of me-

dium brown textura angularis. Conidiogenous cells lining inner

cavity, hyaline, smooth, ampulliform to globose,

4e7 � 4e11 mm, phialidic with periclinal thickening, and min-

ute collarette. Conidia solitary, hyaline, smooth, guttulate to

granular, cylindrical with obtuse ends, (0e)1-septate, mostly

straight (14e)17e21(e22) � 2.5(e3) mm.

Material examined: South Africa: Western Cape Province, Gra-

bouw, on Eucalyptus leaf litter, 1 Feb. 1990, P.W. Crous (holo-

type CBS H-22485, culture extype CBS 114879, 114887).

Culture characteristics: Colonies flat, folded, spreading, with

moderate aerial mycelium, margins smooth, reaching

60mmdiam after 2 wk. OnMEA surface purplish grey, reverse

mouse-grey. On PDA surface and reverse fuscous-black. On

OA surface purplish grey.

Notes: A specimen of Briansuttonomyceswas sent to B.C. Sutton

in IMI in 1991. At the time he commented that this fungus was

best placed in Coleophoma, pending further study. Given the

phylogenetic backbone generated for Coleophoma in the pres-

ent study, we are now able to treat this fungus. Although

Briansuttonomyces is morphologically Coleophoma-like, the con-

idia are 1-septate, and the conidiomata lack paraphyses.

Based on these differences and its distinct phylogeny, this

fungus is herewith introduced as a new genus.

Pleosporaceae, Pleosporales, Dothideomycetes

Dimorphosporicola Crous, gen. nov.


Etymology: Named after its dimorphic conidia.

Conidiomata pycnidial, erumpent, globose, pale brown, with

several dark brown ostioles per conidioma; wall of 2e3 layers

onidiogenous cells. (D) Conidia. Scale bars [ 10 mm.


of pale brown textura angularis. Conidiophores reduced to coni-

diogenous cells, hyaline, smooth, lining the inner cavity,

ampulliform to doliiform, phialidic with minute collarette, at

times with percurrent proliferation. Paraphyses intermingled

among conidiogenous cells, hyaline, smooth, subcylindrical,

aseptate. Conidia dimorphic. Macroconidia cylindrical, straight

or slightly curved, with obtuse ends, guttulate, hyaline, asep-

tate, smooth. Microconidia hyaline, smooth, ellipsoid, apex ob-

tuse, base truncate, aseptate.

Type species: Dimorphosporicola tragani Crous.

Dimorphosporicola tragani Crous, sp. nov. (Fig 23).



lated, Traganum.

Conidiomata pycnidial, erumpent, globose, pale brown, to

300 mmdiam, with several dark brown ostioles per conidioma;

wall of 2e3 layers of pale brown textura angularis. Conidiophores

reduced to conidiogenous cells, hyaline, smooth, lining the in-

ner cavity, ampulliform to doliiform, phialidic with minute

collarette, at times with percurrent proliferation,

5e7 � 4e6 mm. Paraphyses intermingled among conidiogenous

cells, hyaline, smooth, subcylindrical, aseptate, to 30 mm long,

3e4 mm diam. Conidia dimorphic. Macroconidia cylindrical,

straight or slightly curved, with obtuse ends, guttulate, hya-

line, aseptate, smooth (15e)17e21(e25) � 3.5e4(e5) mm.Micro-

conidia hyaline, smooth, ellipsoid, apex obtuse, base truncate,

aseptate, 3e7 � 3e4 mm.

Material examined: Mauritania: on leaf of Traganum nudatum

var. microphyllum, unknown collection date and collector (ho-

lotype CBS H-10512, culture extype CBS 570.85).


aerial mycelium, margins smooth, even, reaching 70 mm

diamafter 2 wk. OnMEA surface isabelline, reverse cinnamon.

On PDA surface vinaceous-buff, reverse rosy-buff. On OA sur-

face rosy-buff.

Notes: Dimorphosporicola tragani was identified as a species of

Coleophoma based on its pycnidial conidiomata, cylindrical

conidia, and the presence of paraphyses. As member of the

Fig 23 e Dimorphosporicola tragani (CBS 570.85). (A) Colony spor

microconidia. (E) Macroconidia. Scale bars [ 10 mm.

Pleosporaceae, D. tragani is distinct from Coleophoma by having

conidiogenous cells that can also proliferate percurrently,

and having dimorphic conidia.

Discussion

The aim of the present study was to resolve the phylogeny of

the genus Coleophoma, listed as incertae sedis, Pezizomycotina in

Index Fungorum and MycoBank. Previously, coelomycetous

fungi with pycnidial conidiomata having paraphyses, and hy-

aline, cylindrical conidia were treated as members of Coleo-

phoma. It is therefore not surprising that recent studies

revealed Coleophoma to be polyphyletic (Quaedvlieg et al.

2013; Tanaka et al. 2015). Via convergent evolution these char-

acters were found to have evolved in several lineages in the

Dothideomycetes, namely Dothideaceae (Dothideales), Mytilinidia-

ceae (Mytilinidiales), Didymellaceae, Didymosphaeriaceae, Pleospor-

aceae (Pleosporales), and Dermateaceae (Helotiales, Leotiomycetes).

A recent phylogenetic study on Phoma-like genera (De

Gruyter et al. 2009) incorporated strain CBS 473.69, which

was isolated from a specimen (CBS H-10464) corresponding

to the type species of Coleophoma, Coleophoma crateriformis.

The morphology of this isolate, however, was never con-

firmed. A subsequent revision of Dothideaceae by

Thambugala et al. (2014) assumed that this isolate was cor-

rectly identified, and based on herbarium specimens and

a few cultures, revised the family, thus further perpetuating

this mistake. In the latter study, two sequences of Dothiora

were linked to this incorrectly identified Coleophoma species

(now Dothiora phillyreae), but this matter was left unresolved.

An examination of older literature revealed that Dothiora is

the sexual morph of Dothichiza (Froidevaux 1972; Sivanesan

1984). In this study we have confirmed this association, al-

though it should be stressed that the type species of respec-

tively Dothiora (Dothiora pyrenophora), and Dothichiza

(Dothichiza populea) still wait to be recollected to definitively re-

solve this issue. Notwithstanding this fact, however, this clade

appears to be monophyletic, to which we apply the older

name, Dothiora. A further point of confusion lies in the fact

that Dothiora also has a Hormonema-like synasexual morph

(De Hoog & Yurlova 1994; Petrini & Petrini 2010; Crous et al.

ulating on OA. (B, C) Conidiogenous cells. (D) Macro- and


2015), which is commonly observed in culture, but also in na-

ture. For instance, the newly described Dothiora agapanthi, was

originally isolated as a hyphomycetous fungus from itsHormo-

nema-likemorph.Dothiora thus has a hyphomycetous and coe-

lomycetous morph, but which clearly also play a role in its

ecology. One of the more commonly known species that

now belong to this genus is Dothiora oleae, a fungus with a con-

fused taxonomy, which commonly occurs on olive leaves

(Duan et al. 2007).

Although there is no available culture of the type species of

Coleophoma, C. crateriformis (on leaf litter of Phillyrea media, Cor-

sica), other species exhibiting morphology typical of Coleo-

phoma cluster together in a well-defined clade in

Dermateaceae (Helotiales). We therefore prefer to apply the

name Coleophoma to this clade, at least tentatively, pending

cultures and sequence data retrieved from C. crateriformis,

the type species of this genus. Coleophomawas also for the first

time linked to a sexual genus, Parafabraea (Chen et al. 2016),

which is herein reduced to synonymy under the former. The

genus clearly contains a mixture of saprobes, as well as foliar

pathogens, such as Coleophoma eucalyptorum (Crous et al. 2011),

Coleophoma proteae (Crous et al. 2012), and Coleophoma copto-

spermatis (present study). Coleophoma fusiformis was described

as a foliar pathogen of Rhododendron in the UK (Wu et al. 1996),

and therefore it is interesting to note the presence of yet an-

other foliar pathogen of this host in Latvia and Sweden, Coleo-

phoma parafusiformis. The description of the genus

Davidhawksworthia from Ilex in the Netherlands is also inter-

esting, in that although it is Cylindrodendrum-like in morphol-

ogy (Nectriaceae; Lombard et al. 2014, 2015), it also clusters in

Dermateaceae.

Several other Coleophoma-like genera are also described as

new in this study. These include Pseudocamaropycnis (Mytilini-

diaceae) (on Pinus needles, Hong Kong), and two genera in the

Pleosporaceae, namely Dimorphosporicola (on Traganum leaves,

Mauritania), and Briansuttonomyces (on Eucalyptus leaves,

South Africa). Although these genera share cylindrical conidia

as a synapomorphy, they are distinguishable from Coleophoma

s.str. based on a set of other characters linked to their conidio-

mata, conidia, conidiogenesis or paraphyses. In spite of all the

genera dealt with here that were previously identified as Coleo-

phoma based on morphology, some taxa were also allied to

a group of Phoma-like species related to Nothophoma gossypii-

cola (Didymellaceae, Pleosporales, Dothideomycetes) (see Chen

et al. 2015), which will be treated elsewhere.

Conflicts of interest

The authors report no conflicts of interest. The authors alone

are responsible for the content and writing of the paper.

Acknowledgements

We are grateful to Arien van Iperen (cultures) and Mieke

Starink-Willemse (DNA isolation, amplification, and sequenc-

ing) for their technical assistance. Genevieve Tocci (Harvard

University Herbaria) is also thanked for assistance and the

loan of specimens.

r e f e r e n c e s

Bianchinotti MV, Rajchenberg M, 2004. Coleophoma gevuinae comb.nov., a foliar pathogen on Gevuina avellana (Proteaceae). Sydo-wia 56: 217e221.

Bills GF, Gonz�alez Men�endez V, Platas G, 2012. Kabatiella bupleurisp. nov. (Dothideales), a pleomorphic epiphyte and endophyteof the Mediterranean plant Bupleurum gibraltarium (Apiaceae).Mycologia 104: 962e973.

Carbone I, Kohn LM, 1999. A method for designing primer sets forspeciation studies in filamentous ascomycetes. Mycologia 91:553e556.

Cheewangkoon R, Groenewald JZ, Summerell BA, Hyde KD,Toanun C, Crous PW, 2009. Myrtaceae, a cache of fungal bio-diversity. Persoonia 23: 55e85.

Cheewangkoon R, Groenewald JZ, Verkley GJM, Hyde KD,Wingfield MJ, Gryzenhout M, Summerell BA, Denman S,Toanun C, Crous PW, 2010. Re-evaluation of Cryptosporiopsiseucalypti and Cryptosporiopsis-like species occurring on Euca-lyptus leaves. Fungal Diversity 44: 89e105.

Chen C, Verkley GJM, Sun G, Groenewald JZ, Crous PW, 2016.Redefining common endophytes and plant pathogens in Neo-fabraea, Pezicula, and related genera. Fungal Biology 120:1291e1322.

Chen Q, Jiang JR, Zhang GZ, Cai L, Crous PW, 2015. Resolving thePhoma enigma. Studies in Mycology 82: 137e217.

Crous PW, Gams W, Stalpers JA, Robert V, Stegehuis G, 2004.MycoBank: an online initiative to launch mycology into the21st century. Studies in Mycology 50: 19e22.

Crous PW, Schoch CL, Hyde KD, Wood AR, Gueidan C, de Hoog GS,Groenewald JZ, 2009a. Phylogenetic lineages in the Capno-diales. Studies in Mycology 64: 17e47.

Crous PW, Summerell BA, Shivas RG, Burgess TI, Decock CA,Dreyer LL, Granke LL, Guest DI, Hardy GESt J, Hausbeck MK,Huberli D, Jung T, Koukol O, Lennox CL, Liew ECY, Lombard L,McTaggart AR, Pryke JS, Roets F, Saude C, Shuttleworth LA,Stukely MJC, Vanky K, Webster BJ, Windstam ST,Groenewald JZ, 2012. Fungal planet description sheets:107e127. Persoonia 28: 138e182.

Crous PW, Summerell BA, Shivas RG, Romberg M, Mel’nik VA,Verkley GJM, Groenewald JZ, 2011. Fungal planet descriptionsheets: 92e106. Persoonia 27: 130e162.

Crous PW, Verkley GJM, Groenewald JZ, Samson RA (eds), 2009b.Fungal Biodiversity. CBS Laboratory Manual Series. Centraal-bureau voor Schimmelcultures, Utrecht, Netherlands.

Crous PW, Wingfield MJ, Le Roux JJ, Richardson DM, Strasberg D,Shivas RG, Alvarado P, Edwards J, Moreno G, Sharma R,Sonawane MS, Tan YP, Alt�es A, Barasubiye T, Barnes CW,Blanchette RA, Boertmann D, Bogo A, Carlavilla JR,Cheewangkoon R, Daniel R, de Beer ZW, de Jes�us Y�a~nez-Morales M, Duong TA, Fern�andez-Vicente J, Geering ADW,Guest DI, Held BW, Heykoop M, Hubka V, Ismail AM, Kajale SC,Khemmuk W, Kola�r�ık M, Kurli R, Lebeuf R, L�evesque CA,Lombard L, Magista D, Manj�on JL, Marincowitz S, Mohedano JM,Nov�akov�a A, Oberlies NH, Otto EC, Paguigan ND, Pascoe IG,P�erez-Butr�on JL, Perrone G, Rahi P, Raja HA, Rintoul T,Sanhueza RMV, Scarlett K, Shouche YS, Shuttleworth LA,Taylor PWJ, Thorn RG, Vawdrey LL, Solano-Vidal R, Voitk A,Wong PTW, Wood AR, Zamora JC, Groenewald JZ, 2015. Fungalplanet description sheets: 371e399. Persoonia 35: 264e327.

De Gruyter J, Aveskamp MM, Woudenberg JHC, Verkley GJM,Groenewald JZ, Crous PW, 2009. Molecular phylogeny of Phomaand allied anamorph genera: towards a reclassification of thePhoma complex. Mycological Research 113: 508e519.

De Hoog GS, Gerrits van den Ende AHG, 1998. Molecular diag-nostics of clinical strains of filamentous Basidiomycetes. My-coses 41: 183e189.

http://refhub.elsevier.com/S1878-6146(16)30051-4/sref1
































































































De Hoog GS, Yurlova NA, 1994. Conidiogenesis, nutritional phys-iology and taxonomy of Aureobasidium and Hormonema. Antonievan Leeuwenhoek 65: 41e54.

Duan JX, Liu XZ, Wu WP, 2007. Reinstatement of Coleonaema forColeophoma oleae and further notes on the genus Coleophoma.Fungal Diversity 26: 187e204.

Froidevaux L, 1972. Contribution �a l’�etude des Dothiorac�ees(Ascomyc�etes). Nova Hedwigia 23: 679e734.

Glass NL, Donaldson G, 1995. Development of primer sets de-signed for use with PCR to amplify conserved genes from fil-amentous ascomycetes. Applied and Environmental Microbiology61: 1323e1330.

Gomes RR, Glienke C, Videira SIR, Lombard L, Groenewald JZ,Crous PW, 2013. Diaporthe: a genus of endophytic, saprobic andplant pathogenic fungi. Persoonia 31: 1e41.

Groenewald JZ, Nakashima C, Nishikawa J, Shin H-D, Park J-H,Jama AN, Groenewald M, Braun U, Crous PW, 2013. Speciesconcepts in Cercospora: spotting the weeds among the roses.Studies in Mycology 75: 115e170.

H€ohnel F von, 1907. Fragmente zur Mykologie: IV. Mitteilung (Nr.156 bis 168). Sitzungsberichte der Kaiserlichen Akademie der Wis-senschaften Mathematisch-Naturwissenschaftliche Klasse, Abtei-lung I 116: 615e647.

H€ohnel F von, 1920. Fungi imperfecti. Beitr€age zur Kenntnis der-selben. Hedwigia 62: 56e89.

Karsten PA, 1890. Sphaeropsideae hucusque in Fennia observa-tae. Acta Societatis pro Fauna et Flora Fennica 6: 1e86.

Katoh K, Standley DM, 2013. MAFFT multiple sequence alignmentsoftware version 7: improvements in performance and us-ability. Molecular Biology and Evolution 30: 772e780.

Lombard L, van der Merwe NA, Groenewald JZ, Crous PW, 2014.Lineages in Nectriaceae: re-evaluating the generic status ofIlyonectria and allied genera. Phytopathologia Mediterranea 53:340e357.

Lombard L, van der Merwe NA, Groenewald JZ, Crous PW, 2015.Generic concepts in Nectriaceae. Studies in Mycology 80:189e245.

Nag Raj TR, 1978. Genera coelomycetum. XIV. Allelochaeta, Basilo-cula, Ceuthosira, Microgloeum, Pycnidiochaeta and Xenodomus.Canadian Journal of Botany 56: 687e707.

Nylander JAA, 2004. MrModeltest V. 2. Program Distributed by theAuthor. Evolutionary Biology Centre, Uppsala University.

O’Donnell K, Cigelnik E, 1997. Two divergent intragenomic rDNAITS2 types within a monophyletic lineage of the fungus Fusa-rium are nonorthologous. Molecular Phylogenetics and Evolution7: 103e116.

O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC, 1998. Multipleevolutionary origins of the fungus causing Panama disease ofbanana: concordant evidence from nuclear and mitochondrialgene genealogies. Proceedings of the National Academy of Sciencesof the United States of America 95: 2044e2049.

Petrini LE, Petrini O, 2010. Schimmelpilze und deren BestimmungVol. 3. Auflage. J. Cramer, Germany, p.170.

Polashock JJ, Caruso FL, Oudemans PV, McManus PS, Crouch JA,2009. The North American cranberry fruit rot fungal commu-nity: a systematic overview using morphological and phylo-genetic affinities. Plant Pathology 58: 1116e1127.

Quaedvlieg W, Verkley GJ, Shin HD, Barreto RW, Alfenas AC,Swart WJ, Groenewald JZ, Crous PW, 2013. Sizing up Septoria.Studies in Mycology 75: 307e390.

Rayner RW, 1970. A Mycological Colour Chart. CommonwealthMycological Institute and British Mycological Society, Kew,Surrey, UK.

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A,H€ohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP, 2012.MrBayes 3.2: efficient Bayesian phylogenetic inference andmodel choice across a large model space. Systematic Biology 61:539e542.

Sivanesan A, 1984. The Bitunicate Ascomycetes and Their Anamorphs.J. Cramer 701.

Smith H, Wingfield MJ, Crous PW, Coutinho TA, 1996. Sphaeropsissapinea and Botryosphaeria dothidea endophytic in Pinus spp.and Eucalyptus spp. in South Africa. South African Journal ofBotany 62: 86e88.

Sutton BC, 1980. The Coelomycetes. Fungi Imperfecti with Pycnidia,Acervuli and Stromata. Commonwealth Mycological Institute,Kew, Surrey, England.

Swofford DL, 2003. PAUP*. Phylogenetic Analysis Using Parsimony(*and Other Methods), V. 4.0b10. Sinauer Associates, Sunder-land, Massachusetts.

Tamura K, Dudley J, Nei M, Kumar S, 2007. MEGA4: MolecularEvolutionary Genetics Analysis (MEGA) software version 4.0.Molecular Biology and Evolution 24: 1596e1599.

Tanaka K, Hirayama K, Yonezawa H, Sato G, Toriyabe A, Kudo H,Hashimoto A, Matsumura M, Harada Y, Kurihara Y,Shirouzu T, Hosoya T, 2015. Revision of the Massarineae (Pleo-sporales, Dothideomycetes). Studies in Mycology 82: 75e136.

Thambugala KM, Ariyawansa HA, Li Y-M, Boonmee S,Hongsanan S, Tian Q, Singtripop C, Bhat DJ, Camporesi E,Jayawardena R, Liu Z-Y, Xu J-C, Chukeatirote E, Hyde KD, 2014.Dothideales. Fungal Diversity 68: 105e158.

Vilgalys R, Hester M, 1990. Rapid genetic identification andmapping of enzymatically amplified ribosomal DNA fromseveral Cryptococcus species. Journal of Bacteriology 172:4238e4246.

White TJ, Bruns T, Lee S, Taylor J, 1990. Amplification and directsequencing of fungal ribosomal RNA genes for phylogenetics.In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds), PCR Pro-tocols: a guide to methods and applications. Academic Press, SanDiego, California, pp. 315e322.

Wu W, Sutton BC, Gange AC, 1996. Coleophoma fusiformis sp. nov.from leaves of Rhododendron, with notes on the genus Coleo-phoma. Mycological Research 100: 942e947.

Yuan Z-Q, 1996. Fungi and associated tree diseases in MelvilleIsland, Northern Territory, Australia. Australian SystematicBotany 9: 337e360.













































































































































they seldom occur alone - knaw · coleophoma coptospermatis cbs 251.39 thuja plicata, seedling uk:...

Documents