Professional Documents
Culture Documents
Y. Marin-Felix1,2*, J.Z. Groenewald1, L. Cai3, Q. Chen3, S. Marincowitz2, I. Barnes4, K. Bensch1,5, U. Braun6, E. Camporesi7,8,9,
U. Damm10, Z.W. de Beer2, A. Dissanayake11,12, J. Edwards13, A. Giraldo1,2, M. Hernandez-Restrepo1,2, K.D. Hyde11,14,
R.S. Jayawardena11,12, L. Lombard1, J. Luangsa-ard15, A.R. McTaggart16, A.Y. Rossman17, M. Sandoval-Denis1,18, M. Shen19,
R.G. Shivas20, Y.P. Tan21,22, E.J. van der Linde23, M.J. Wingfield2, A.R. Wood24, J.Q. Zhang19, Y. Zhang19, and P.W. Crous1,2*
1
Westerdijk Fungal Biodiversity Institute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands; 2Department of Microbiology and Plant Pathology, Forestry and Agricultural
Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa; 3State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences,
Beijing 100101, PR China; 4Department of Genetics, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa; 5Botanische
Staatssammlung München, Menzinger Straße 67, D-80638 München, Germany; 6Martin-Luther-Universit€at, Institut für Biologie, Bereich Geobotanik und Botanischer
Garten, Herbarium, Neuwerk 21, D-06099 Halle (Saale), Germany; 7A.M.B. Gruppo Micologico Forlivese “Antonio Cicognani”, Via Roma 18, Forlì, Italy; 8A.M.B.
Circolo Micologico “Giovanni Carini”, C.P. 314, Brescia, Italy; 9Societa per gli Studi Naturalistici della Romagna, C.P. 144, Bagnacavallo (RA), Italy; 10Senckenberg
Museum of Natural History Görlitz, PF 300 154, 02806 Görlitz, Germany; 11Center of Excellence in Fungal Research, School of Science, Mae Fah Luang
University, Chiang Rai 57100, Thailand; 12Institute of Plant and Environment Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, PR
China; 13AgriBio Centre for AgriBiosciences, Department of Economic Development, Jobs, Transport and Resources, 5 Ring Road, LaTrobe University, Bundoora,
Victoria 3083, Australia; 14School of Science, Mae Fah Luang University, Chiang Rai 57100, Thailand; 15Microbe Interaction and Ecology Laboratory, Biodiversity
and Biotechnological Resource Research Unit (BBR), BIOTEC, NSTDA 113 Thailand Science Park Phahonyothin Rd., Khlong Nueng, Khlong Luang, Pathum Thani
12120, Thailand; 16Department of Plant and Soil Science, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa;
17
Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA; 18Faculty of Natural and Agricultural Sciences, Department of
Plant Sciences, University of the Free State, P.O. Box 339, Bloemfontein 9300, South Africa; 19Institute of Microbiology, P.O. Box 61, Beijing Forestry University,
Beijing 100083, PR China; 20Centre for Crop Health, Institute for Agriculture and the Environment, University of Southern Queensland, Toowoomba 4350,
Queensland, Australia; 21Department of Agriculture & Fisheries, Biosecurity Queensland, Ecosciences Precinct, Dutton Park, Queensland 4102, Australia;
22
Microbiology, Department of Biology, Utrecht University, Padualaan 8, 3584 CT Utrecht, The Netherlands; 23ARC – Plant Protection Research Institute,
Biosystematics Division – Mycology, P. Bag X134, Queenswood 0121, South Africa; 24ARC – Plant Protection Research Institute, P. Bag X5017, Stellenbosch
7599, South Africa
Abstract: Genera of Phytopathogenic Fungi (GOPHY) is introduced as a new series of publications in order to provide a stable platform for the taxonomy of
phytopathogenic fungi. This first paper focuses on 21 genera of phytopathogenic fungi: Bipolaris, Boeremia, Calonectria, Ceratocystis, Cladosporium, Colletotrichum,
Coniella, Curvularia, Monilinia, Neofabraea, Neofusicoccum, Pilidium, Pleiochaeta, Plenodomus, Protostegia, Pseudopyricularia, Puccinia, Saccharata, Thyrostroma,
Venturia and Wilsonomyces. For each genus, a morphological description and information about its pathology, distribution, hosts and disease symptoms are provided. In
addition, this information is linked to primary and secondary DNA barcodes of the presently accepted species, and relevant literature. Moreover, several novelties are
introduced, i.e. new genera, species and combinations, and neo-, lecto- and epitypes designated to provide a stable taxonomy. This first paper includes one new genus,
26 new species, ten new combinations, and four typifications of older names.
Studies in Mycology
Key words: DNA barcodes, Fungal systematics, Phytopathogenic fungi, Plant pathology, Taxonomy, Typifications.
Taxonomic novelties: New genus: Verkleyomyces Y. Marín & Crous; New species: Bipolaris saccharicola Y. Marín & Crous, Bi. variabilis Y. Marín, Y.P. Tan & Crous,
Boeremia trachelospermi Q. Chen & L. Cai, Calonectria ecuadorensis L. Lombard & Crous, Ca. longiramosa L. Lombard & Crous, Ca. nemoralis L. Lombard & Crous,
Ca. octoramosa L. Lombard & Crous, Ca. parvispora L. Lombard & Crous, Ca. tucuruiensis L. Lombard & Crous, Cladosporium chasmanthicola Bensch, U. Braun &
Crous, Cl. kenpeggii Bensch, U. Braun & Crous, Cl. welwitschiicola Bensch, U. Braun & Crous, Colletotrichum sydowii Damm, Curvularia pisi Y. Marín & Crous, Cu. soli
Y. Marín & Crous, Neofusicoccum italicum Dissanayake & K.D. Hyde, Nm. pistaciicola Crous, Nm. pruni Crous, Pilidium septatum Giraldo & Crous, Pleiochaeta carotae
Hern.-Rest., van der Linde & Crous, Plenodomus deqinensis Q. Chen & L. Cai, Protostegia eucleicola Crous, Saccharata leucospermi Crous, S. protearum Crous,
Thyrostroma franseriae Crous, Venturia phaeosepta Y. Zhang ter & J.Q. Zhang; New combinations: Coniella hibisci (B. Sutton) Crous, Monilinia mumeicola (Y.
Harada et al.) Sandoval-Denis & Crous, M. yunnanensis (M.J. Hu & C.X. Luo) Sandoval-Denis & Crous, Pseudopyricularia bothriochloae (Crous & Cheew.) Y.
Marín & Crous, Puccinia dianellae (Dietel) McTaggart & R.G. Shivas, Pu. geitonoplesii (McAlpine) McTaggart & R.G. Shivas, Pu. merrilliana (Syd. & P. Syd.)
McTaggart & R.G. Shivas, Pu. rhagodiae (Cooke & Massee) McTaggart & R.G. Shivas, Venturia martianoffiana (Thüm.) Y. Zhang ter & J.Q. Zhang, Verkleyomyces
illicii (X. Sun et al.) Y. Marín & Crous; Typification: Epitypification: Ceratophorum setosum Kirchn., Coniella musaiaensis var. hibisci B. Sutton, Helminthosporium
carpophilum Lev.; Lectotypification: Ceratophorum setosum Kirchn.
INTRODUCTION global trade in food and fibre (Crous et al. 2015b, 2016a). The
present project focused on genera of fungi that have members
Since the advent of molecular DNA techniques, many species of causing plant diseases (phytopathogenic), links to a larger
phytopathogenic fungi have been shown to represent species initiative called the “The Genera of Fungi project” based on
complexes or to be included in genera that are poly- or para- Clements & Shear (1931) (www.GeneraOfFungi.org, Crous et al.
phyletic (Crous et al. 2015b). Resolving these generic and spe- 2014a, 2015a, Giraldo et al. 2017), which aims to revise the
cies concepts is thus of the utmost importance for plant health and generic names of all currently accepted fungi (Kirk et al. 2013).
99
MARIN-FELIX ET AL.
Of the approximately 18 000 fungal genera that have thus far and/or novel species or typifications. Authors that wish to
been described, only around 8 000 are in current use. However, contribute to future issues of this project are encouraged to first
the majority of these were described before the DNA era. To contact Pedro Crous (p.crous@westerdijkinstitute.nl) before final
validate the application of these names, their type species need to submission, to ensure there is no potential overlap with activities
be recollected and designated as epi- or neotypes with a Myco- arising from other research groups. The genera chosen in the
Bank Typification (MBT) number to ensure traceability of the first paper were randomly selected, based on the fact that their
nomenclatural act (Robert et al. 2013). Furthermore, to move to a phylogenetic position was resolved, DNA data were available for
single nomenclature for fungi (Wingfield et al. 2012, Crous et al. those species known from culture, and novel species or typifi-
2015b), their sexual–asexual links also need to be confirmed. cations were available for inclusion.
The present initiative forms part of the activities of the Inter-
national Subcommission for the Taxonomy of Phytopathogenic
Fungi [Pedro Crous and Amy Rossman (co-chairs), of the In- MATERIAL AND METHODS
ternational Committee for the Taxonomy of Fungi (www.
fungaltaxonomy.org/)].
Isolates and morphological analysis
The aims of this project are to:
1. Establish a new website, www.plantpathogen.org, to host Descriptions of the new taxa and typifications are based on
a database that will link metadata to other databases such cultures obtained from the Westerdijk Fungal Biodiversity Insti-
as MycoBank, Index Fungorum, FacesofFungi, U.S. Na- tute, Utrecht, the Netherlands (CBS), the working collection of
tional Fungus Collections Databases, etc., and associated P.W. Crous (CPC), housed at the Westerdijk Institute, Herbarium
DNA barcodes (ITS, LSU and other loci as needed) to Mycologicum Academiae Sinicae (HMAS), BIOTEC Culture
GenBank (Schoch et al. 2014). Collection (BCC), the Queensland Plant Pathology Herbarium
2. Source type specimens and cultures of the type species of (BRIP), the Chinese General Microbiological Culture Collection
genera from fungaria and Biological Resource Centres Center (CGMCC), the Mae Fah Luang University Culture
(BRCs), and generate the required metadata as explained Collection (MFLUCC), and the Victorian Plant Pathogen Her-
below. barium (VPRI). For fresh collections, we followed the procedures
3. Recollect fresh material of the type species if not already previously described in Crous et al. (1991). Colonies were
available, and as far as possible derive DNA barcodes and transferred to different media, i.e. carnation leaf agar (CLA),
cultures from this material. cornmeal agar (CMA), 2 % malt extract agar (MEA), 2 % potato-
4. Designate type species, and type specimens of those dextrose agar (PDA), synthetic nutrient-poor agar (SNA),
species, for those genera where this has not been indi- oatmeal agar (OA), water agar (WA) (Crous et al. 2009c),
cated in the original publications. autoclaved pine needles on 2 % tap water agar (PNA) (Smith
5. Fix the application of the type species of generic names by et al. 1996), and incubated at different conditions depending
means of lecto-, neo-, or epitypification as appropriate, on the taxon to induce sporulation (requirements of media and
and at the same time deposit cultures in at least two Mi- conditions of incubations specified in each genus). Reference
crobial Biological Resource Centres (M-BRCs) from which strains and specimens are maintained at the BCC, CBS,
they would be widely available to the international CGMCC, HMAS and MFLUCC.
research community. Vegetative and reproductive structures were mounted in
6. Publish modern generic descriptions, and provide DNA clear lactic acid, Shear's mounting fluid and lactophenol cotton
barcodes for all accepted species, with reference to blue, either directly from specimens or from colonies sporu-
appropriate literature. lating on CLA, MEA, OA, PDA, PNA, or SNA. Sections of
Authors with new submissions should ensure that all new conidiomata were made by hand for examination purposes. For
species and typification events are registered in MycoBank (MB cultural characterisation, isolates were grown and incubated on
and MBT numbers), respectively. It is recommended that the different culture media and temperatures as stipulated for each
following issues are addressed in each genus: genus. Colour notations were rated according to the colour
1. Modern generic description, and phylogenetic placement charts of Rayner (1970). For some taxa, NaOH pot test was
of the type species of the genus. carried out on MEA cultures to detect the production of
2. Higher order phylogeny. metabolite E (Boerema et al. 2004). Taxonomic novelties were
3. New nomenclature merging asexual and sexual generic deposited in MycoBank (www.MycoBank.org; Crous et al.
names (see Rossman et al. 2013, Johnston et al. 2014). 2004b).
4. Description of novel taxa, with a reference collection (e.g.
fungarium), and MycoBank and GenBank sequence DNA isolation, amplification and analyses
accession numbers.
5. Name changes that result from the new phylogenetic Fungal DNA was extracted and purified directly from the colonies
placement. or host material according to the Wizard® Genomic DNA purifi-
6. Notes discussing the relevance and implications of the cation kit protocol (Promega, Madison, USA). Primers and pro-
phylogeny, and importance of the genus. tocols for the amplification and sequencing of gene loci can be
Authored generic contributions will be combined into scientific found in the bibliography related to the phylogeny presented for
papers to be published online in Studies in Mycology, and also each genus. Phylogenetic analyses consisted of Maximum-
placed in a database displayed on www.plantpathogen.org. Likelihood (ML), Bayesian Inference (BI), and Maximum Parsi-
Preference will be given to genera that include novel DNA data mony (MP). The ML was carried out using methods described by
100
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 1. Bipolaris spp. A–F. Disease symptoms. A. Symptoms caused by Bipolaris eragrostiellae (ex-type IMI 155931). B. Symptoms caused by Bipolaris gossypina (IMI
123377). C. Symptoms caused by Bipolaris halepensis (ex-type BPI 1103129). D. Symptoms caused by Bipolaris microstegii. E. Symptoms caused by Bipolaris musae-
sapientium (ex-type K (M) 181466). F. Symptoms caused by Bipolaris oryzae (ex-neotype MFLUCC 10-0715). G–L. Sexual morphs. G. Ascoma of Bipolaris luttrellii (IMI
345516). H–K. Asci. H. Bipolaris chloridis (ex-type IMI 213865). I. Bipolaris luttrellii (IMI 345516). J. Bipolaris maydis (CBS 241.92). K. Bipolaris microlaenae (IMI 338218). L.
Ascospores of Bipolaris maydis (CBS 241.92). M–Z. Asexual morphs. M–R. Conidiophores and conidia. M. Bipolaris setariae (BPI 880305B). N. Bipolaris zeae (ex-type IMI
202085). O. Bipolaris bicolor (CBS 690.96). P. Bipolaris heveae (CBS 241.92). Q. Bipolaris sorokiniana (ex-type CBS 110.14). R. Bipolaris zeicola (ex-type BPI 626668). S–Z.
Conidia. S. Bipolaris cookei (ex-type BPI 428852). T. Bipolaris costina (ex-type IMI 256417). U. Bipolaris crotonis (ex-type IMI 223682). V. Bipolaris gossypina (IMI 123377). W.
Bipolaris obclavata (ex-type IMI 331725). X. Bipolaris oryzae (ex-neotype MFLUCC 10-0715). Y. Bipolaris salviniae (DAR 35056). Z. Bipolaris sorokiniana (ex-type CBS 110.14).
Scale bars: A, N = 100 μm; B, E, F = 500 μm; C = 1 cm; G, H = 20 μm; I–L, O–Z = 10 μm; M = 50 μm. All pictures except for D taken from Manamgoda et al. (2014).
www.studiesinmycology.org 101
MARIN-FELIX ET AL.
102
GENERA OF PHYTOPATHOGENIC FUNGI
Table 1. (Continued).
Species Isolates1 GenBank accession numbers2 References
ITS gapdh tef1
Bi. woodii BRIP 12239T KX452458 KX452424 KX4524725 Tan et al. (2016)
Bi. zeae BRIP 11512IsoPT KJ415538 KJ415408 KJ415454 Tan et al. (2014)
Bi. zeicola FIP 532ET KM230398 KM034815 KM093752 Manamgoda et al. (2014)
1
AR, FIP: Isolates housed in Systematic Mycology and Microbiology Laboratory, United States Department of Agriculture, Agricultural Research Service, Beltsville, Maryland,
USA; Bi: Isolates housed in the Department of Plant Protection, Faculty of Agricultural Sciences and Engineering, University College of Agriculture and Natural Resources,
University of Tehran, Karaj, Iran (TUPP); ATCC: American Type Culture Collection, Virginia, USA; BRIP: Queensland Plant Pathology Herbarium, Brisbane, Australia; CBS:
Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands; ICMP: International Collection of Micro-organisms from Plants, Landcare Research, Private Bag 92170,
Auckland, New Zealand; MFLUCC: Mae Fah Luang University Culture Collection, Chiang Ria, Thailand. T, ET, IsoT, IsoLT, IsoPT, LT and NT indicate ex-type, ex-epitype, ex-isotype,
ex-isolectotype, ex-isoparatype, ex-lectotype and ex-neotype strains, respectively.
2
ITS: internal transcribed spacers and intervening 5.8S nrDNA; gapdh: partial glyceraldehyde-3-phosphate dehydrogenase gene; tef1: partial translation elongation factor
1-alpha gene.
Type species: Bipolaris maydis (Y. Nisik. & C. Miyake) Shoe- Distribution: Worldwide.
maker. Neotype and ex-neotype culture: ATCC 48332, CBS
137271. Hosts: Mainly pathogens of grasses, but some also on non-grass
hosts, causing devastating diseases on cereal crops in the
DNA barcodes (genus): LSU, ITS. Poaceae, including rice, maize, wheat and sorghum and on
various other host plants. Moreover, this genus can occur on at
DNA barcodes (species): ITS, gapdh, tef1. Table 1. Fig. 2. least 60 other genera in Anacardiaceae, Araceae, Euphorbia-
ceae, Fabaceae, Malvaceae, Rutaceae and Zingiberaceae as
Ascomata pseudothecial, mostly globose to ellipsoidal, some- either saprobes or pathogens.
times flask-shaped or flattened on hard substrata, brown or
black, immersed, erumpent, partially embedded or superficial, Disease symptoms: Leaf spots, leaf blight, melting out, root rot,
free, smooth or covered with vegetative hyphae; ostiole central, and foot rot, among others.
papillate or with a sub-conical, conical, paraboloid or cylindrical
neck; ascomatal wall comprising pseudoparenchymatous cells of Notes: Species delimitation based on morphology alone is limited
equal thickness or slightly thickened at apex of the ascoma. since many species have overlapping characters. Moreover, the
Hamathecium comprising septate, filiform, branched pseudo- morphology of the sexual morph is of limited value due to diffi-
paraphyses. Asci bitunicate, clavate, cylindrical-clavate or culties to induce this morph in culture, or find it in nature. The
broadly fusoid, straight or slightly curved, thin-walled, fissituni- genus is morphologically similar to Curvularia, and distinguishing
cate, often becoming more or less distended prior to dehiscence, these genera can be problematic. Both genera contain species
short pedicellate, rounded at apex. Ascospores multiseriate, with straight or curved conidia, but in Bipolaris the curvature is
filiform or flagelliform, hyaline or sometimes pale yellow or pale continuous throughout the length of the conidium, while the
brown at maturity, septate, helically coiled within ascus, asco- conidia of Curvularia have intermediate cells inordinately
spore coiling moderate to strongly, often with a mucilaginous enlarged which contributes to their curvature. Moreover, conidia
sheath. Conidiophores single, sometimes arranged in small in Bipolaris are usually longer than in Curvularia. Another
groups, straight to flexuous or geniculate, pale to dark brown, morphological difference is the presence of stromata in some
branched, thick-walled, septate. Conidiogenous nodes smooth to species of Curvularia, a feature not observed in species of
slightly verruculose. Conidia canoe-shaped, fusoid or obclavate, Bipolaris. In order to properly delineate both genera, phyloge-
mostly curved, hyaline, pale or dark brown, reddish brown or pale netic studies using ITS, gapdh and tef1 sequences were recently
to deep olivaceous, thick-walled, smooth-walled, 3–14- performed (Manamgoda et al. 2014, 2015).
distoseptate, germinating by production of one or two germina-
tion tubes by polar cells; hila often slightly protruding or truncate, References: Ellis 1971, Sivanesan 1987 (morphology and
sometimes inconspicuous; septum ontogeny first septum median pathogenicity); Manamgoda et al. 2011, Tan et al. 2016
to sub-median, second septum delimits basal cell and third de- (morphology, phylogeny and pathogenicity); Manamgoda et al.
limits distal cell (adapted from Manamgoda et al. 2014). 2014 (morphology, phylogeny, pathogenicity and key of all
Bipolaris spp.).
Culture characteristics: Colonies on PDA white or pale grey
when young, brown or dark grey when mature, fluffy, cottony, Bipolaris saccharicola Y. Marín & Crous, sp. nov. MycoBank
raised or convex with papillate surface, margin lobate, undulate, MB820809. Fig. 3.
entire or sometimes rhizoid.
Etymology: Name refers to the host genus it was isolated from,
Optimal media and cultivation conditions: Sterilised Zea mays Saccharum.
leaves placed on 1.5 % WA or slide cultures of PDA under
near-ultraviolet light (12 h light, 12 h dark) at 25 °C to induce Hyphae hyaline to pale brown, branched, septate, thin-walled,
sporulation of the asexual morph, while for the sexual morph 2.5–5.5 μm. Conidiophores arising in smalls groups, septate,
Sach's agar with sterilised rice or wheat straw at 25 °C is straight or flexuous, smooth-walled, sometimes branched, cell
used. walls thicker than those of vegetative hyphae, mononematous,
www.studiesinmycology.org 103
MARIN-FELIX ET AL.
104
GENERA OF PHYTOPATHOGENIC FUNGI
semi- to macronematous, pale brown to brown, paler towards inconspicuous, slightly protuberant, flat, darkened, thickened,
apex, rarely swollen at base, up to 900 μm tall. Conidiogenous 3–6 μm diam. Chlamydospores and sexual morph not
cells smooth-walled, terminal or intercalary, subhyaline to pale observed.
brown or brown, subcylindrical to swollen, 10–27(–47) ×
4–8 μm. Conidia verruculose, curved, rarely straight, fusiform, Culture characteristics: Colonies on PDA reaching 90 mm diam
subhyaline to pale brown or brown, (2–)4–9(–11)-dis- within 1 wk, with sparse to moderate aerial mycelium giving a
toseptate, (30–)45–120 × 10.5–20(–21.5) μm; hila incon- cottony appearance, margin lobate; surface olivaceous grey to
spicuous, brown, slightly protuberant, flat, darkened, slightly iron-grey; reverse olivaceous black.
thickened, 2–4 μm. Chlamydospores and sexual morph not
observed. Material examined: Argentina, from leaf spots on Pennisetum
clandestinum, 28 Jul. 1986, col. M.N. Sisterna, isol. J.L. Alcorn
Culture characteristics: Colonies on PDA reaching 41–53 mm (holotype CBS H-23115, culture ex-type CBS 127716 = BRIP
diam after 1 wk, moderate aerial mycelium giving a cottony 15349). Brazil, from Pennisetum clandestinum, Apr. 1987, J.J.
appearance, margin lobate; surface olivaceous grey to oliva- Muchovej, CBS 127736 = BRIP 15702 = ATCC 62423.
ceous black; reverse olivaceous black.
Notes: Bipolaris variabilis can easily be distinguished based on
Material examined: Unknown country, unknown substratum, its highly variable conidial size, shape and septation. Hitherto,
1926, H. Atherton (holotype CBS H-23114, culture ex-type CBS this species has only been found on Pennisetum clandestinum
155.26 = MUCL 9693); Unknown country, from Saccharum in South America. Other species of Bipolaris can be found on
officinarum, unknown date, R.R. Nelson, CBS 324.64; CBS Pennisetum spp., i.e. Bi. bicolor, Bi. colocasiae, Bi. cynodontis,
325.64 = DSM 62597 = MUCL 18220 = MUCL 9694 = NRRL 5241. Bi. maydis, Bi. mediocris, Bi. sacchari, Bi. setariae, Bi. sor-
okiniana, Bi. stenospila, Bi. urochloae and Bi. zeae; however,
Notes: This species is closely related to Bi. maydis. However, Bi. only Bi. mediocris is restricted to that host (Manamgoda et al.
saccharicola can easily be distinguished by the absence of a 2014). Bipolaris mediocris and Bi. variabilis are morphologi-
sexual morph, longer conidiophores and verruculose, more cally similar, but Bi. variabilis produces smaller, verruculose
prominently curved conidia. Both species can be found on the conidia. Moreover, Bi. mediocris is characterised by much
same host, Saccharum officinarum. Other species of Bipolaris shorter conidiophores (up to 150 μm tall), and has only been
isolated from this host include Bi. cynodontis, Bi. sacchari, Bi. reported in Africa (Farr & Rossman 2017). Bipolaris variabilis is
setariae, Bi. stenospila and Bi. yamadae (Manamgoda et al. closely related to Bi. zeae, but the latter is characterised
2014). Bipolaris saccharicola is morphologically similar to Bi. by shorter conidiophores (up to 370 μm tall), and less septate
sacchari, but Bi. saccharicola can be distinguished by its much conidia that are less variable in shape than those of Bi.
longer and non-geniculate conidiophores and wider and more variabilis.
septate conidia.
Bipolaris yamadae (Y. Nisik.) Shoemaker, Canad. J. Bot. 37:
Bipolaris variabilis Y. Marín, Y.P. Tan & Crous, sp. nov. 884. 1959. Fig. 5.
MycoBank MB820810. Fig. 4. Basionym: Helminthosporium yamadae Y. Nisik., Rept. Ohara.
Inst. Agr. Research 4: 120. 1928.
Etymology: Name refers to the highly variable conidial Synonyms: Drechslera yamadai (Y. Nisik.) Subram. & B.L. Jain,
morphology. Curr. Sci. 35: 355. 1966.
Helminthosporium euphorbiae Hansf., Proc. Linn. Soc. London
Leaf spots brown to reddish, elongated, often confluent and 155: 49. 1943.
following veins, some with central part brown, 2.5 × 1–2 mm. Bipolaris euphorbiae (Hansf.) J.J. Muchovej & A.O. Carvalho,
Hyphae subhyaline to pale brown, branched, septate, thin- Mycotaxon 35: 160. 1989.
walled, 3–6 μm. Conidiophores arising in groups, septate, Drechslera euphorbiae (Hansf.) M.B. Ellis, Dematiaceous
straight or flexuous, sometimes geniculate at upper part, Hyphomycetes (Kew): 440. 1971.
smooth to verruculose, branched, cells walls thicker than those
of vegetative hyphae, mononematous, semi- to macro- Notes: Bipolaris euphorbiae was originally described in Hel-
nematous, pale brown to brown, paler towards apex, slightly minthosporium (Hansford 1943), then transferred to Drechslera
swollen at base, up to 1 600 μm tall. Conidiogenous cells (Ellis 1971), and finally placed in Bipolaris based on the bipolar
smooth-walled, terminal or intercalary, proliferating sympo- germination and hilum structure (Muchovej & Carvalho 1989).
dially, subhyaline or pale brown to brown, subcylindrical to In their revision of Bipolaris, Manamgoda et al. (2014) accepted
swollen, (6.5–)8–26(–35) × 5.5–11 μm. Conidia verruculose, this species in the genus despite the lack of molecular data. In
straight or slightly curved, globose, subglobose, ellipsoidal to the present study, the neotype strain of Bi. euphorbiae CBS
obclavate, pale brown to brown, apical and basal cells paler 127087 (=BRIP 16567; see Fig. 5), which was designated by
than middle cells being subhyaline to pale brown, (1–) Muchovej & Carvalho (1989), clustered with the ex-epitype
3–7(–9)-distoseptate, 13.5–77 × 10–19.5 μm; hila strain of Bi. yamadae. Both species are morphologically
Fig. 2. RAxML phylogram obtained from the combined ITS (478 bp), gapdh (472 bp) and tef1 (892 bp) sequences of all the accepted species of Bipolaris. The tree was rooted
to Curvularia buchlo€es CBS 246.49 and Curvularia subpapendorfii CBS 656.74. The novel species described in this study are shown in bold. RAxML bootstrap support (BS)
values above 70 % and Bayesian posterior probability scores 0.95 are shown at the nodes. GenBank accession numbers are indicated in Table 1. T, ET, IsoT, IsoLT, IsoPT, LT and
NT
indicate ex-type, ex-epitype, ex-isotype, ex-isolectotype, ex-isoparatype, ex-lectotype and ex-neotype strains, respectively. TreeBASE: S20877.
www.studiesinmycology.org 105
MARIN-FELIX ET AL.
Fig. 3. Bipolaris saccharicola (ex-type CBS 155.26). A–C. Conidiophores and conidia. D–H. Conidia. Scale bars: A–C = 20 μm; H applies to D–H = 10 μm.
similar differing only in the size of the structures that are usually Culture characteristics: Colonies on PDA reaching 30–65 mm
overlapping. Based on these data, we propose to reduce Bi. diam after 1 wk, cottony, with irregular margins; surface pale
euphorbiae to synonymy under Bi. yamadae. Moreover, we olivaceous grey to olivaceous grey; reverse olivaceous black.
emended the description of Bi. yamadae to include the
morphology of its new synonym, as well as the new host and Distribution: Brazil, Cuba, China, India, Japan, Sudan, Tanzania,
distribution records. USA (IA, ID, ND, WI).
Leaf spots on Panicum sp. ovoid, oblong, pale brown at margin Hosts: Panicum capillare, Pa. implicatum, Pa. maximum, Pa.
and pale brown at centre, with an irregular concentric zone. miliaceum, Euphorbia sp., Oryza sp., Saccharum sp., Setaria
Hyphae hyaline, branched, septate, anastomosing, thin-walled, plicata (Farr & Rossman 2017).
1.5–4.5 μm. Conidiophores arising singly or in small groups,
septate, rarely branched, straight or flexuous, sometimes Authors: Y. Marin-Felix, P.W. Crous & Y.P. Tan
geniculate at upper part, smooth walled, mononematous, semi-
to macronematous, olive-brown to pale brown, sometimes paler Boeremia Aveskamp et al., Stud. Mycol. 65: 36. 2010. Fig. 6.
towards apex, swollen at base, 40–650 × 3–10.5 μm. Con-
idiogenous cells smooth-walled, sometimes slightly verruculose, Classification: Dothideomycetes, Pleosporomycetidae, Pleo-
terminal or intercalary, subhyaline to pale brown or dark brown, sporales, Didymellaceae.
subcylindrical to slightly swollen, 7–30(–40) × 5.5–9.5 μm.
Conidia smooth-walled, straight or curved, ellipsoidal, cylindri- Type species: Boeremia exigua (Desm.) Aveskamp et al.
cal, fusiform or obclavate, sometimes obovoid, with rounded Representative strain: CBS 431.74.
ends, subhyaline to pale brown or olive-brown, (3–)5–7(–11)-
distoseptate, 27–100(–120) × 11.5–20 μm; hila 2.5–4.5 μm, DNA barcodes (genus): LSU, ITS.
non or slightly protuberant, flat, darkened; germination at both
ends. DNA barcodes (species): act, cal, rpb2, tef1, tub2. Table 2. Fig. 7.
106
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 4. Bipolaris variabilis (ex-type CBS 127716). A–C. Conidiophores and conidia. D–M. Conidia. Scale bars: A = 20 μm; B, C = 15 μm; H applies to D–H, M applies to
I–M = 5 μm.
Ascomata pseudothecial, subglobose. Asci cylindrical or sub- pseudoparenchymatous, multi-layered, outer wall brown pig-
clavate, 8-spored, biseriate. Ascospores ellipsoidal, 1-septate. mented. Conidiophores reduced to conidiogenous cells. Con-
Conidiomata pycnidial, variable in shape and size, mostly idiogenous cells phialidic, hyaline, smooth, ampulliform to
globose to subglobose, superficial or immersed into agar, solitary doliiform. Conidia variable in shape, hyaline, smooth- and thin-
or confluent; ostiole non-papillate or papillate, lined internally walled, mainly aseptate, but 1(–2)-septate larger conidia may
with hyaline cells when mature; conidiomatal wall be found (adapted from Aveskamp et al. 2010).
www.studiesinmycology.org 107
MARIN-FELIX ET AL.
Fig. 5. Bipolaris yamadae (CBS 127087). A–C. Conidiophores and conidia. D–G. Conidia. Scale bars: A–C = 20 μm; D–G = 10 μm.
Culture characteristics: Colonies on OA white to dull green, grey reported to have a sexual morph. Recently, Chen et al. (2015a)
olivaceous to olivaceous or smoke-grey, velvety, floccose to and Berner et al. (2015) further examined the phylogenetic re-
woolly, margin often regular, sometimes lobate and irregular lationships of taxa in Boeremia in two combined multilocus an-
scalloped. alyses, the first one based on LSU, ITS, tub2 and rpb2
sequences, and the second on ITS, act, cal, tef1 and tub2
Optimal media and cultivation conditions: OA or PNA at 25 °C sequences.
under near-ultraviolet light (12 h light, 12 h dark) to promote
sporulation. References: Boerema et al. 2004 (morphology and pathoge-
nicity); Aveskamp et al. 2010, Chen et al. 2015a (morphology
Distribution: Worldwide. and phylogeny); Berner et al. 2015 (morphology, pathogenicity
and phylogeny).
Hosts: Seed-borne pathogens of Phaseolus vulgaris (Fabaceae)
and noxious pathogens of Coffea arabica (Rubiaceae). Species Boeremia trachelospermi Q. Chen & L. Cai, sp. nov. Myco-
on more than 200 host genera including Amaryllidaceae, Bank MB818819. Fig. 8.
Apocynaceae, Araliaceae, Asteraceae, Caprifoliaceae, Cheno-
podiaceae, Crassulaceae, Fabaceae, Lamiaceae, Linaceae, Etymology: Named for the host genus from which the holotype
Oleaceae, Salicaceae, Solanaceae, Ulmaceae, Umbelliferae. was collected, Trachelospermum.
Disease symptoms: Leaf spots, stem lesions, black node, bulb Conidiomata pycnidial, solitary or aggregated, globose to sub-
rot, root rot, shoot dieback. globose, glabrous or with few hyphal outgrowths, superficial, with a
short neck, 75–255 × 60–225 μm; ostiole single, papillate or non-
Notes: The genus Boeremia was established by Aveskamp et al. papillate; conidiomatal wall pseudoparenchymatous 2–4-layered,
(2010) to accommodate phoma-like species that are morpho- 16.5–37 μm thick, composed of isodiametric cells. Conidiophores
logically similar and closely related to Ph. exigua. Taxa in this reduced to conidiogenous cells. Conidiogenous cells phialidic,
genus are characterised by having ostioles with a hyaline inner hyaline, smooth, ampulliform to doliiform, 4.5–12.5 × 4.5–6 μm.
layer of cells and producing aseptate and septate conidia Conidia variable in shape, mostly ovoid, ellipsoidal to cylindrical,
(Aveskamp et al. 2010). To date only Bo. lycopersici has been smooth- and thin-walled, hyaline, mainly aseptate, occasionally 1-
108
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 6. Boeremia spp. A. Symptoms of Boeremia lilacis (LC 8116) on Ocimum sp. B. Symptoms of Boeremia exigua var. rhapontica (ex-type CBS 113651) on Rhaponticum
repens. C. Symptoms of Boeremia lilacis (LC 5178) on Lonicera sp. D. Ostiole configuration of Boeremia exigua var. exigua (CBS 431.74). E. Section of young pycnidium of
Boeremia exigua var. pseudolilacis (ex-type CBS 101207). F. Conidia of Boeremia exigua var. pseudolilacis (ex-type CBS 101207). G. Conidia of Boeremia exigua var.
heteromorpha (ex-neotype CBS 443.94). Scale bars: D–E = 20 μm; F = 5 μm; G = 10 μm. Picture B taken from Berner et al. (2015); D–F from Aveskamp et al. (2010); G from
Chen et al. (2015a).
septate large conidia, 4.5–9.5 × 2.5–4.5 μm, with 1–8 guttules. Lectotype: France, litter of Platanus, Autumn. Desm., Pl. Crypt.
Conidial matrix cream-coloured. France Ed. 2 (2) # 372 (fide Rossman 1979); no culture or DNA
data available.
Culture characteristics: Colonies on OA, reaching 47–55 mm
diam after 1 wk, margin regular, floccose, white, dark grey near DNA barcodes (genus): LSU, ITS.
centre; reverse white to buff, dark grey near centre. Colonies on
MEA 40–60 mm diam after 1 wk, margin regular, woolly, pale DNA barcodes (species): cmdA, his3, tef1, tub2, and rpb2.
olivaceous grey; reverse concolourous. Colonies on PDA, Table 3. Fig. 11.
reaching 20–25 mm diam after 1 wk, margin regular, floccose,
compact, white to olivaceous; reverse white to buff, olivaceous Ascomata perithecial, solitary or in groups, globose to sub-
near centre. NaOH test negative. globose to ovoid, yellow to orange to red or red-brown to brown,
turning dark red to red-brown in KOH, rough-walled; ascomatal
Material examined: USA, on seedlings of Trachelospermum apex consisting of flattened, thick-walled hyphal elements with
jasminoides, 2014, W.J. Duan (holotype HMAS 246706, culture rounded tips forming a palisade, discontinuous with warty wall,
ex-type CGMCC 3.18222 = LC 8105). gradually becoming thinner towards ostiolar canal, and merging
with outer periphyses; ascomatal base consisting of dark
Notes: Boeremia trachelospermi represents the first report of brown-red, angular cells, merging with an erumpent stroma,
a Boeremia species on Trachelospermum (Apocynaceae). cells of outer wall layer continuing into pseudoparenchymatous
Phylogenetically, it forms a distinct lineage separate from Bo. cells of erumpent stroma. Asci 8-spored, clavate, tapering to a
diversispora, the Bo. exigua varieties, Bo. noackiana and Bo. long thin stalk. Ascospores aggregated in upper third of ascus,
sambuci-nigrae (Fig. 7), and morphologically it often pro- hyaline, smooth, fusoid with rounded ends, straight to sinuous,
duces longer conidiogenous cells and conidia than the other unconstricted, or constricted at septa. Megaconidiophores, if
taxa. present, borne on agar surface or immersed in agar; stipe
extensions mostly absent; conidiophores unbranched, termi-
Authors: Q. Chen & L. Cai nating in 1–3 phialides, or sometimes with a single subterminal
phialide; phialides straight to curved, cylindrical, seemingly
Calonectria De Not., Comm. Soc. crittog. Ital. 2(fasc. 3): 477. producing a single conidium, periclinal thickening and an
1867. Figs 9, 10. inconspicuous, divergent collarette rarely visible. Megaconidia
Synonyms: Cylindrocladium Morgan, Bot. Gaz. 17: 191. 1892. hyaline, smooth, frequently remaining attached to phialide,
Candelospora Rea & Hawley, Proc. R. Ir. Acad., Sect. B, Biol. multi-septate, widest in middle, bent or curved, with a truncated
Sci. 13: 11. 1912. base and rounded apical cell. Macroconidiophores consist of a
stipe, a penicillate arrangement of fertile branches, a stipe
Classification: Sordariomycetes, Hypocreomycetidae, Hypo- extension, and a terminal vesicle; stipe septate, hyaline or
creales, Nectriaceae. slightly pigmented at base, smooth or finely verruculose; stipe
extensions septate, straight to flexuous, mostly thin-walled,
Type species: Calonectria pyrochroa (Desm.) Sacc. Holotype: terminating in a thin-walled vesicle of characteristic shape.
Italy, leaves of Magnolia grandiflora, Daldini (as Ca. daldiniana); Conidiogenous apparatus with 0–1-septate primary branches,
www.studiesinmycology.org 109
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MARIN-FELIX
Table 2. DNA barcodes of accepted Boeremia spp.
Species Isolates1 GenBank accession numbers2 References
ITS act cal rpb2 tef1 tub2
ET AL.
Boeremia crinicola CBS 109.79 GU237737 KY484558 KY484571 KT389563 – GU237489 Aveskamp et al. (2010), Chen et al. (2015a), Berner et al. (2015)
Bo. diversispora CBS 102.80 GU237725 EU880861 KY484575 KT389565 KY484676 GU237492 Aveskamp et al. (2009b, 2010), Chen et al. (2015a), Berner et al. (2015)
Bo. exigua var. coffeae CBS 109183 GU237748 KY484560 KY484576 KT389566 KY484678 GU237505 Aveskamp et al. (2010), Chen et al. (2015a), Berner et al. (2015)
Bo. exigua var. exigua CBS 431.74 FJ427001 EU880854 KY484584 KT389569 KY484687 FJ427112 Aveskamp et al. (2009a, b), Chen et al. (2015a), Berner et al. (2015)
Bo. exigua var. forsythiae CBS 101213 GU237723 EU880868 KY484589 KT389571 KY484692 GU237494 Aveskamp et al. (2009b, 2010), Chen et al. (2015a), Berner et al. (2015)
Bo. exigua var. gilvescens CBS 101150 GU237715 KY484562 KY484591 KT389568 KY484694 GU237495 Aveskamp et al. (2010), Chen et al. (2015a), Berner et al. (2015)
Bo. exigua var. heteromorpha CBS 443.94NT GU237866 EU880869 KY484598 KT389573 KY484700 GU237497 Aveskamp et al. (2009b, 2010), Chen et al. (2015a), Berner et al. (2015)
Bo. exigua var. linicola CBS 116.76 GU237754 EU880880 KY484604 KT389574 KY484705 GU237500 Aveskamp et al. (2009b, 2010), Chen et al. (2015a). Berner et al. (2015)
Bo. exigua var. populi CBS 100167T GU237707 EU880885 KY484605 – KY484706 GU237501 Aveskamp et al. (2009b, 2010), Berner et al. (2015)
Bo. exigua var. pseudolilacis CBS 101207 T
GU237721 EU880874 KY484609 – KY484710 GU237503 Aveskamp et al. (2009b, 2010), Berner et al. (2015)
Bo. exigua var. rhapontica CBS 113651T KY484662 KY484566 KY484612 – KY484713 KY484760 Berner et al. (2015)
Bo. exigua var. viburni CBS 100354 GU237711 EU880889 KY484613 KT389577 – GU237506 Aveskamp et al. (2009b, 2010), Chen et al. (2015a), Berner et al. (2015)
Bo. foveata CBS 109176 GU237742 EU880892 KY484614 KT389578 KY484714 GU237508 Aveskamp et al. (2009b, 2010), Chen et al. (2015a), Berner et al. (2015)
Bo. hedericola CBS 367.91 GU237842 KY484568 KY484618 KT389579 KY484718 GU237511 Aveskamp et al. (2010), Chen et al. (2015a), Berner et al. (2015)
Bo. lilacis CBS 569.79 GU237892 EU880875 KY484619 – KY484721 GU237498 Aveskamp et al. (2009b, 2010), Berner et al. (2015)
Bo. lycopersici CBS 378.67 GU237848 EU880898 KY484623 KT389580 KY484726 GU237512 Aveskamp et al. (2009b, 2010), Chen et al. (2015a), Berner et al. (2015)
Bo. noackiana CBS 100353 GU237710 EU880881 KY484624 – KY484727 GU237514 Aveskamp et al. (2009b, 2010), Berner et al. (2015)
Bo. sambuci-nigrae CBS 629.68T GU237897 KY484570 KY484630 – KY484734 GU237517 Aveskamp et al. (2010), Berner et al. (2015)
Bo. strasseri CBS 126.93 GU237773 EU880904 KY484631 KT389584 KY484735 GU237518 Aveskamp et al. (2009b, 2010), Chen et al. (2015a), Berner et al. (2015)
Bo. telephii CBS 109175 GU237741 EU880906 KY484633 KT389585 KY484737 GU237520 Aveskamp et al. (2009b, 2010), Chen et al. (2015a), Berner et al. (2015)
Bo. trachelospermi CGMCC 3.18222T KY064028 – – KY064033 – KY064051 Present study
1
CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands; CGMCC: Chinese General Microbiological Culture Collection Center, Beijing, China. T and NT indicate ex-type and ex-neotype strains, respectively.
2
ITS: internal transcribed spacers and intervening 5.8S nrDNA; act: partial actin gene; cal: partial calmodulin gene; rpb2: partial RNA polymerase II second largest subunit gene; tef1: partial translation elongation factor 1-alpha gene; tub2: partial
β-tubulin gene.
GENERA OF PHYTOPATHOGENIC FUNGI
10.0
Fig. 7. Phylogenetic tree generated from a maximum parsimony analysis based on the combined LSU, ITS, tub2 and rpb2 sequences. Values above the branches represent
parsimony bootstrap support values (> 50 %). The novel species are shown in bold. The tree is rooted with Phoma herbarum CBS 615.75. GenBank accession numbers are
indicated in Table 2. T and NT indicate ex-type and ex-neotype strains, respectively. TreeBASE: S21048.
up to eight additional branches, mostly aseptate, each terminal terminating in 1–4 phialides; phialides cylindrical, straight to
branch producing 1–6 phialides; phialides cylindrical to allan- slightly curved, apex with minute periclinal thickening and
toid, straight to curved, or doliiform to reniform, hyaline, asep- marginal frill. Microconidia cylindrical, straight to curved,
tate, apex with minute periclinal thickening and inconspicuous rounded at apex, flattened at base, 1(–3)-septate, held in
divergent collarette. Macroconidia cylindrical, rounded at both asymmetrical clusters by colourless slime.
ends, straight or curved, widest at base, middle, or first basal
septum, 1- to multi-septate, lacking visible abscission scars, Culture characteristics: Colonies on MEA white to pale brick
held in parallel cylindrical clusters by colourless slime. Micro- when young, becoming pale brick to dark sepia when mature,
conidiophores consist of a stipe and a penicillate or sub- fluffy, cottony, effuse to convex with papillate surface, margin
verticillate arrangement of fertile branches; primary branches entire, undulate, lobate, or fimbriate, sometimes with abundant
0–1-septate, subcylindrical; secondary branches 0–1-septate, chlamydospores forming microsclerotia within medium.
www.studiesinmycology.org 111
MARIN-FELIX ET AL.
Fig. 8. Boeremia trachelospermi (ex-type CGMCC 3.18222). A, B. Colony on OA (front and reverse). C, D. Colony on MEA (front and reverse). E, F. Colony on PDA (front and
reverse). G. Pycnidia forming on OA. H. Pycnidia. I–K. Conidiogenous cells. L. Conidia. Scale bars: G = 200 μm; H = 50 μm; I–K = 5 μm; L = 10 μm.
Optimal media and cultivation conditions: CLA to induce sporu- Calonectria ecuadorensis L. Lombard & Crous, sp. nov.
lation of the asexual morph at 25 °C, while for the sexual morph MycoBank MB820849. Fig. 12.
sterile toothpicks placed on SNA is used at 20 °C.
Etymology: Name refers to Ecuador, the country where this
Distribution: Worldwide. fungus was collected.
Hosts: Soil-borne pathogens of forestry, agricultural and horti- Macroconidiophores consist of a stipe bearing a penicillate
cultural crops representing approximately 100 plant families and arrangement of fertile branches, and a stipe extension termi-
340 plant host species (Crous 2002, Lombard et al. 2010c). nating in a vesicle; stipe septate, hyaline, smooth,
55–70 × 6–10 μm; stipe extension septate, straight to flexuous,
Disease symptoms: Leaf spots, leaf and shoot blights, cutting rot, 130–280 μm long, 3–6 μm wide at apical septum, terminating in
stem cankers, damping-off and root rot. a clavate vesicle, 4–6 μm diam. Conidiogenous apparatus
45–90 μm wide, and 20–90 μm long; primary branches asep-
Notes: The genus Calonectria presently includes 151 species tate, 13–31 × 4–6 μm; secondary branches aseptate,
of which only Ca. hederae and Ca. pyrochroa are not sup- 13–23 × 4–5 μm; tertiary branches aseptate, 9–15 × 3–4 μm,
ported by ex-type cultures and supplementary DNA barcodes. each terminal branch producing 2–6 phialides; phialides dolii-
Species delimitation based on morphology alone is compli- form to reniform, hyaline, aseptate, 6–11 × 2–4 μm, apex with
cated by the large number of cryptic taxa recognised in this minute periclinal thickening and inconspicuous collarette. Mac-
genus (Lombard et al. 2016). The perithecia of several roconidia cylindrical, rounded at both ends, straight, (34–)
Calonectria spp. are morphologically similar. The 35–39(–44) × (3–)3.5–4.5(–5) μm (av. 37 × 4 μm), 1-septate,
cylindrocladium-like asexual morph, the life phase most lacking a visible abscission scar, held in parallel cylindrical
commonly found in nature, is extensively used for taxon clusters by colourless slime. Mega- and microconidia not
identification, although it is complicated by the morphological observed.
overlap of some cryptic species. For accurate species de-
limitation, phylogenetic inference of the cmdA, tef1 and tub2 Culture characteristics: Colonies moderately fast growing
(or combinations of these) is required. (35–55 mm diam) on MEA after 1 wk at room temperature;
surface rosy-buff to cinnamon with sparse white woolly aerial
References: Crous 2002 (morphology, pathogenicity and mycelium and abundant sporulation on aerial mycelium and
monograph); Lombard et al. 2010a–d, 2015, 2016 (morphology, colony surface; reverse rosy-buff to cinnamon to sepia with
phylogeny and key of Calonectria spp.); Alfenas et al. 2015 abundant chlamydospores throughout medium, forming
(morphology and phylogeny). microsclerotia.
112
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 9. Calonectria spp. A−H. Sexual morphs. A−D. Perithecia. A. Calonectria asiatica (ex-type CBS 114073). B. Calonectria braziliensis (ex-type CBS 230.51 × CBS 114257).
b Calonectria fujianensis (ex-type CBS 127201). D. Section through perithecium of Calonectria asiatica (ex-type CBS 114073). E−F. Asci. E. Calonectria crousiana (ex-type CBS
127198). F. Calonectria asiatica (ex-type CBS 114073). G−H. Ascospores. G. Calonectria fujianensis (ex-type CBS 127201). H. Calonectria acicola (ex-type CBS 114813).
I−AB. Asexual morphs. I−L. Macroconidiophores. I. Calonectria malesiana (ex-type CBS 112752). J. Calonectria macroconidialis (ex-type CBS 114880). K. Calonectria
spathulata (ex-type CBS 555.92). L. Calonectria ovata (CBS 111307). M−O. Conidiogenous apparatus. M. Calonectria brachiatica (ex-type CBS 123700). N. Calonectria
ecuadoriae (ex-type CBS 111406). O. Calonectria hurae (CBS 114551). P. Microconidiophore of Calonectria reteaudii (ex-type CBS 112144). Q. Megaconidia of Calonectria
hurae (CBS 114551). R, S. Macroconidia. R. Calonectria angustata (ex-type CBS 109065). S. Calonectria chinensis (ex-type CBS 114827). T. Microconidia of Calonectria
pteridis (ex-type CBS 111793). U−AB. Terminal vesicles of stipe extensions. U. Calonectria brassicae (ex-type CBS 111869). V. Calonectria rumohrae (CBS 109062). W.
Calonectria cylindrospora (CBS 119670). X. Calonectria hongkongensis (ex-type CBS 114828). Y. Calonectria chinensis (ex-type CBS 114827). Z. Calonectria humicola (ex-type
CBS 125251). AA. Calonectria mexicana (ex-type CBS 110918). AB. Calonectria spathulata (ex-type CBS 555.92). Scale bars: A−C = 500 μm; D−F = 100 μm; G, H, M−P,
R−AB = 10 μm; I−L, Q = 20 μm.
www.studiesinmycology.org 113
MARIN-FELIX ET AL.
Fig. 10. Disease symptoms associated with Calonectria spp. A−B. Root and collar rot of Pinus spp. C. Cutting rot of Eucalyptus sp. D. Calonectria leaf blight of Eucalyptus sp.
E. Calonectria leaf blight of Metrosideros thomasii. F. Calonectria leaf blight of Myrtus communis. G. Seedling blight of Drosera sp. H. Buxus blight. I. Root rot of Persea
americana. J. Potato tuber rot. K−L. Calonectria black rot of Arachis hypogaea.
Material examined: Ecuador, from soil, 20 Jun. 1997, M.J. clusters by colourless slime. Mega- and microconidia not
Wingfield (holotype CBS H-23134, culture ex-type CBS observed.
111706 = CPC 1636); ibid., culture CBS 114164 = CPC 1634.
Culture characteristics: Colonies moderately fast growing
Notes: Calonectria ecuadorensis can be distinguished from Ca. (35–70 mm diam) on MEA after 1 wk at room temperature;
ecuadoriae (Crous et al. 2006a) by its fewer branches in the surface amber with moderate white, woolly aerial mycelium and
conidiogenous apparatus. Also, the conidia of Ca. ecuadorensis moderate sporulation on the aerial mycelium and colony surface;
[(34–)35–39(–44) × (3–)3.5–4.5(–5) μm (av. 37 × 4 μm)] are reverse amber with abundant chlamydospores throughout the
smaller than those of Ca. ecuadoriae [(45–)48–55(–65) × (4–) medium, forming microsclerotia.
4.5(–5) μm (av. 51 × 4.5 μm); Crous et al. 2006a].
Material examined: Brazil, Amazon, from Eucalyptus sp., 1993,
Calonectria longiramosa L. Lombard & Crous, sp. nov. P.W. Crous & A.C. Alfenas (holotype CBS H-22759, culture ex-
MycoBank MB820843. Fig. 13. type CBS 116319 = CPC 3761); ibid., cultures CBS
116305 = CPC 3765.
Etymology: Name refers to the characteristic long fertile
branches of the conidiogenous apparatus in this fungus. Notes: Calonectria longiramosa is a new species in the Ca.
pteridis complex. This species is characterised by the long fertile
Macroconidiophores consist of a stipe bearing a penicillate branches of the conidiogenous apparatus distinguishing it from
arrangement of fertile branches, and a stipe extension termi- the other species in this complex (Alfenas et al. 2015).
nating in a vesicle; stipe septate, hyaline, smooth,
100–245 × 6–9 μm; stipe extension septate, straight to flex- Calonectria nemoralis L. Lombard & Crous, sp. nov. Myco-
uous, 155–310 μm long, 4–6 μm wide at apical septum, ter- Bank MB820850. Fig. 14.
minating in a clavate vesicle, 5–8 μm diam. Conidiogenous
apparatus 50–85 μm wide, and 60–140 μm long; primary Etymology: Name refers to the environment, a Eucalyptus
branches aseptate to 1-septate, 22–42 × 4–6 μm; secondary plantation, from where this fungus was collected.
branches aseptate, 15–35 × 3–6 μm; tertiary branches
aseptate, 12–30 × 3–6 μm; quaternary branches aseptate, Macroconidiophores consist of a stipe bearing a penicillate
11–19 × 3–6 μm each terminal branch producing 2–4 phia- arrangement of fertile branches, and a stipe extension termi-
lides; phialides elongate doliiform to allantoid, hyaline, asep- nating in a vesicle; stipe septate, hyaline, smooth,
tate, 8–16 × 2–4 μm, apex with minute periclinal thickening 40–165 × 6–8 μm; stipe extension septate, straight to flexuous,
and inconspicuous collarette. Macroconidia cylindrical, rounded 140–210 μm long, 3–5 μm wide at the apical septum, termi-
at both ends, straight to slightly curved, (57–) nating in a fusiform to ovoid vesicle, 7–9 μm diam. Con-
66–76(–84) × (3–)4.5–5.5(–6) μm (av. 71 × 5 μm), 1-septate, idiogenous apparatus 20–45 μm wide, and 40–55 μm long;
lacking a visible abscission scar, held in parallel cylindrical primary branches aseptate, 18–24 × 3–6 μm; secondary
114
Table 3. DNA barcodes of accepted Calonectria spp.
Species Isolates1 GenBank accession numbers2 References
tub2 cmdA tef1 his3 rpb2 ITS LSU
www.studiesinmycology.org
Calonectria acicola CBS 114812T DQ190590 GQ267359 GQ267291 DQ190693 KY653352 GQ280547 GQ280669 Crous et al. (2006a), Lombard et al. (2010c), present study
Ca. aconidialis CBS 136086T – KJ463017 KJ462785 KJ463133 – – – Lombard et al. (2015)
Ca. amazonica CBS 116250T KX784612 KX784555 KX784682 – KY653355 KY653241 KY653297 Lombard et al. (2016), present study
Ca. amazoniensis CBS 115440T KX784615 KX784558 KX784685 – KY653358 KY653244 KY653300 Lombard et al. (2016), present study
T
Ca. angustata CBS 109065 AF207543 GQ267361 FJ918551 DQ190696 KY653359 GQ280548 GQ280671 Crous & Kang (2001), Crous et al. (2006a),
Lombard et al. (2010c, d), present study
Ca. arbusta CBS 136079T KJ462904 KJ463018 KJ462787 KJ463135 – – – Lombard et al. (2015)
Ca. asiatica CBS 114073T AY725616 AY725741 AY725705 AY725658 – GQ280550 GQ280672 Crous et al. (2004c), Lombard et al. (2010c)
T
Ca. australiensis CBS 112954 DQ190596 GQ267363 GQ267293 DQ190699 KY653361 GQ280552 GQ280674 Crous et al. (2006a), Lombard et al. (2010c), present study
Ca. blephiliae CBS 136425T KF777246 – KF777243 – – KF777141 KF777197 Crous et al. (2013b)
Ca. brachiatica CBS 123700T FJ696388 GQ267366 GQ267296 FJ696396 – GQ280555 GQ280677 Lombard et al. (2009, 2010c)
Ca. brasiliana CBS 111484T KX784616 KX784559 KX784686 – KY653362 KY653245 KY653301 Lombard et al. (2016), present study
T
Ca. brasiliensis CBS 230.51 GQ267241 GQ267421 GQ267328 GQ267259 KY653364 GQ280624 GQ280746 Lombard et al. (2010c), present study
Ca. brassiana CBS 134855T KM395969 KM396056 KM395882 KM396139 – – – Alfenas et al. (2015)
T
Ca. brassicae CBS 111869 AF232857 GQ267382 FJ918567 DQ190720 KM232308 GQ280576 GQ280698 Crous et al. (1999, 2006a, b),
Lombard et al. (2009, 2010c), present study
Ca. brassicicola CBS 112841T KX784619 KX784561 KX784689 – – – – Lombard et al. (2016)
Ca. brevistipitata CBS 115671T KX784623 KX784565 KX784693 – KY653368 KY653248 KY653304 Lombard et al. (2016), present study
T
Ca. canadania CBS 110817 AF348212 AY725743 GQ267297 AF348228 KY653369 GQ280556 GQ280678 Kang et al. (2001), Crous et al. (2004c),
Lombard et al. (2010c), present study
Ca. candelabrum CPC 1675 FJ972426 GQ267367 FJ972525 FJ972476 – GQ280557 GQ280679 Lombard et al. (2010b, c)
Ca. cerciana CBS 123693T FJ918510 GQ267369 FJ918559 FJ918528 – GQ280559 GQ280681 Lombard et al. (2009, 2010c)
T
Ca. chinensis CBS 114827 AY725619 AY725747 AY725710 AY725661 KY653371 GQ280561 GQ280683 Crous et al. (2004c), Lombard et al. (2010c), present study
Ca. clavata CBS 114557T AF333396 GQ267377 GQ267305 DQ190623 KY653372 GQ280571 GQ280693 Schoch et al. (2001), Lombard et al. (2010c), present study
Ca. cliffordicola CBS 111812 T
KX784624 KX784566 KX784694 – KY653374 KY653249 KY653305 Lombard et al. (2016), present study
GENERA
Ca. colhounii CBS 293.79T DQ190564 GQ267373 GQ267301 DQ190639 KY653376 GQ280565 GQ280687 Crous et al. (2006a), Lombard et al. (2010c), present study
Ca. colombiana CBS 115127 T
FJ972423 GQ267455 FJ972492 FJ972442 – GQ280660 GQ280782 Lombard et al. (2010b, c)
OF PHYTOPATHOGENIC FUNGI
Ca. colombiensis CBS 112220T GQ267207 AY725748 AY725711 AY725662 – GQ280566 GQ280688 Crous et al. (2004c), Lombard et al. (2010c)
Ca. crousiana CBS 127198 T
HQ285794 – HQ285822 HQ285808 – – – Chen et al. (2011)
Ca. cylindrospora CBS 110666 FJ918509 GQ267423 FJ918557 FJ918527 KY653378 GQ280626 GQ280748 Crous et al. (2006a), Lombard et al. (2010c), present study
Ca. densa CBS 125261T GQ267232 GQ267444 GQ267352 GQ267281 – GQ280647 GQ280769 Lombard et al. (2010c)
Ca. duoramosa CBS 134656T KM395940 KM396027 KM395853 – – – – Alfenas et al. (2015)
115
T
Ca. ecuadoriae CBS 111406 DQ190600 GQ267375 GQ267303 DQ190705 KY653381 GQ280569 GQ280691 Crous et al. (2006a), Lombard et al. (2010c), present study
(continued on next page)
116
MARIN-FELIX
Table 3. (Continued).
Species Isolates1 GenBank accession numbers2 References
tub2 cmdA tef1 his3 rpb2 ITS LSU
ET AL.
Ca. ecuadorensis CBS 111706 T
KX784674 KX784604 KX784747 – KY653382 KY653252 KY653308 Lombard et al. (2016), present study
CBS 114164 KX784677 KX784607 KX784750 – KY653383 KY653253 KY653309
Ca. ericae CBS 114458T KX784629 KX784571 KX784699 – KY653385 KY653255 KY653311 Lombard et al. (2016), present study
Ca. eucalypti CBS 125275 T
GQ267218 GQ267430 GQ267338 GQ267267 – GQ280633 GQ280755 Lombard et al. (2010c)
Ca. eucalypticola CBS 134847T KM395964 KM396051 KM395877 KM396134 – – – Alfenas et al. (2015)
Ca. expansa CBS 136247 T
KJ462914 KJ463029 KJ462798 KJ463146 – – – Lombard et al. (2015)
Ca. floridana CBS 114692T KX784651 KX784588 KX784722 – – – – Lombard et al. (2016)
Ca. foliicola CBS 136641T KJ462916 KJ463031 KJ462800 KJ463148 – – – Lombard et al. (2015)
Ca. fujianensis CBS 127201T HQ285792 – HQ285820 HQ285806 – – – Chen et al. (2011)
Ca. glaeboicola CBS 134852 T
KM395966 KM396053 KM395879 KM396136 – – – Alfenas et al. (2015)
Ca. gordoniae CBS 112142T AF449449 GQ267381 GQ267309 DQ190708 KY653386 GQ280575 GQ280697 Crous et al. (2004c), Lombard et al. (2010c), present study
T
Ca. gracilipes CBS 111141 DQ190566 GQ267385 GQ267311 DQ190644 KY653387 GQ280579 GQ280701 Crous et al. (2004c), Lombard et al. (2010c), present study
Ca. gracilis CBS 111807T AF232858 GQ267407 GQ267323 DQ190646 KY653390 GQ280610 GQ280734 Crous et al. (2004c), Lombard et al. (2010c), present study
Ca. guangxiensis CBS 136092 T
KJ462919 KJ463034 KJ462803 KJ463151 – – – Lombard et al. (2015)
Ca. hainanensis CBS 136248T – KJ463036 KJ462805 KJ463152 – – – Lombard et al. (2015)
Ca. hawksworthii CBS 111870T AF333407 GQ267386 FJ918558 DQ190649 KY653391 GQ280580 GQ280702 Schoch et al. (2001), Lombard et al. (2010c), present study
Ca. henricotiae CBS 138102 T
JX535308 KF815157 – KF815185 – JX535322 – Gehesquiere et al. (2016)
Ca. hodgesii CBS 133609T KC491228 KC491222 KC491225 – – – – Alfenas et al. (2015)
Ca. hongkongensis CBS 114828T AY725622 AY725755 AY725717 AY725667 – GQ280581 GQ280703 Crous et al. (2004c), Lombard et al. (2010c)
Ca. humicola CBS 125251T GQ267233 GQ267445 GQ267353 GQ267282 – GQ280648 GQ280770 Lombard et al. (2010c)
Ca. hurae CBS 114551 AF333408 GQ267387 FJ918548 DQ190728 – GQ280583 GQ280705 Schoch et al. (2001), Lombard et al. (2010c, d)
Ca. ilicicola CBS 190.50T AY725631 AY725764 AY725726 AY725676 KM232307 GQ280605 GQ280727 Crous et al. (2004c), Lombard et al. (2010c)
T
Ca. indonesiae CBS 112823 AY725623 AY725756 AY725718 AY725668 KY653394 GQ280585 GQ280707 Crous et al. (2004c), Lombard et al. (2010c), present study
Ca. indonesiana CBS 112936T KX784631 KX784573 KX784701 – – – – Lombard et al. (2016)
Ca. indusiata CBS 144.36T GQ267239 GQ267453 GQ267332 GQ267262 KY653396 GQ280658 GQ280780 Lombard et al. (2010c), present study
Ca. insularis CBS 114558T AF210861 GQ267389 FJ918556 FJ918526 KY653398 GQ280587 GQ280709 Schoch et al. (1999), Lombard et al. (2010b, c), present study
Ca. kyotensis CBS 114525 T
AF348215 AY725750 AY725713 – – AF261741 – Crous et al. (2004c)
Ca. lageniformis CBS 111324T KX784632 KX784574 KX784702 – KY653400 KY653256 KY653312 Lombard et al. (2016), present study
T
Ca. lateralis CBS 136629 KJ462955 KJ463070 KJ462840 KJ463186 KY653402 KY653258 KY653314 Lombard et al. (2015), present study
Ca. lauri CBS 749.70T GQ267210 GQ267388 GQ267312 GQ267250 KY653403 GQ280584 GQ280706 Lombard et al. (2010c), present study
Ca. leguminum CBS 728.68 T
AF389837 GQ267391 FJ918547 DQ190654 – GQ280589 GQ280711 Crous et al. (2004c), Lombard et al. (2010c)
Ca. leucothoes CBS 109166T FJ918508 GQ267392 FJ918553 FJ918523 KY653404 GQ280590 GQ280712 Lombard et al. (2010b,c), present study
Ca. longiramosa CBS 116319T KX784635 KX784577 KX784705 – KY653406 KY653260 KY653316 Lombard et al. (2016), present study
Ca. machaerinae CBS 123183 T
KX784636 – KX784706 – KY653407 KY653261 KY653317 Lombard et al. (2016), present study
Ca. madagascariensis CBS 114572T DQ190572 GQ267394 GQ267314 DQ190658 KY653409 GQ280592 GQ280714 Crous et al. (2006a), Lombard et al. (2010c), present study
Ca. macroconidialis CBS 114880T AF232855 GQ267393 GQ267313 DQ190655 KY653410 GQ280591 GQ280713 Crous et al. (1999, 2006a),
www.studiesinmycology.org
GENERA
Ca. parakyotensis CBS 136085 T
– KJ463081 KJ462851 KJ463197 – – – Lombard et al. (2015)
Ca. parva CBS 110798T KX784646 KX784583 KX784716 – KY653425 KY653270 KY653326 Lombard et al. (2016), present study
OF PHYTOPATHOGENIC FUNGI
Ca. parvispora CBS 111465 T
DQ190607 KX784584 KX784717 – – – – Crous et al. (2006a), Lombard et al. (2016)
Ca. pauciramosa CBS 138824T FJ918514 GQ267405 FJ918565 FJ918531 KY653426 GQ280608 GQ280730 Lombard et al. (2010b, c), present study
T
Ca. penicilloides CBS 174.55 AF333414 GQ267406 GQ267322 GQ267257 KY653427 GQ280609 GQ280731 Schoch et al. (2001), Lombard et al. (2010c), present study
Ca. pentaseptata CBS 133349T JX855942 – JX855958 JX855946 – JX855950 JX855954 Crous et al. (2012a)
Ca. piauiensis CBS 134850 T
KM395973 KM396060 KM395886 KM396143 – – – Alfenas et al. (2015)
117
MARIN-FELIX
Table 3. (Continued).
Species Isolates1 GenBank accession numbers2 References
tub2 cmdA tef1 his3 rpb2 ITS LSU
ET AL.
Ca. pini CBS 123698 T
GQ267224 GQ267436 GQ267344 GQ267273 – GQ280639 GQ280761 Lombard et al. (2015)
Ca. polizzii CBS 123402 T
FJ972419 – FJ972488 FJ972438 – – – Lombard et al. (2010b, c)
Ca. plurilateralis CBS 111401T KX784648 KX784586 KX784719 – KY653430 KY653271 KY653327 Lombard et al. (2016), present study
T
Ca. pluriramosa CBS 136976 KJ462995 KJ463112 KJ462882 KJ463228 KY653431 KY653272 KY653328 Lombard et al. (2015), present study
Ca. propaginicola CBS 134815T KM395953 KM396040 KM395866 KM396123 – – – Alfenas et al. (2015)
Ca. pseudobrassicae CBS 134662 T
KM395936 KM396023 KM395849 KM396106 – – – Alfenas et al. (2015)
Ca. pseudocerciana CBS 134824T KM395962 KM396049 KM395875 KM396132 – – – Alfenas et al. (2015)
Ca. pseudocolhounii CBS 127195 T
HQ285788 – HQ285816 HQ285802 – – – Chen et al. (2011)
Ca. pseudoecuadoriae CBS 111402T KX784652 KX784589 KX784723 – KY653432 KY653273 KY653329 Lombard et al. (2016), present study
Ca. pseudohodgesii CBS 134818 T
KM395905 KM395991 KM395817 KM396079 – – – Alfenas et al. (2015)
Ca. pseudokyotensis CBS 137332T KJ462994 KJ463111 KJ462881 KJ463227 – – – Lombard et al. (2015)
Ca. pseudometrosideri CBS 134845 T
KM395909 KM395995 KM395821 KM396083 – – – Alfenas et al. (2015)
Ca. pseudomexicana CBS 130354T JN607281 – JN607496 JN607266 – – – Lombard et al. (2011)
Ca. pseudouxmalensis CBS 110924T KX784654 – KX784726 – KY653437 KY653276 KY653332 Lombard et al. (2016), present study
Ca. pseudonaviculata CBS 114417T GQ267214 GQ267409 GQ267325 GQ267258 KY653434 GQ280612 GQ280734 Lombard et al. (2010c), present study
Ca. pseudopteridis CBS 163.28T – KM396076 KM395902 – – – – Alfenas et al. (2015)
Ca. pseudoreteaudii CBS 123694T FJ918504 GQ267411 FJ918541 FJ918519 – GQ280614 GQ280736 Lombard et al. (2010c, d)
Ca. pseudoscoparia CBS 125257T GQ267229 GQ267441 GQ267349 GQ267278 – GQ280644 GQ280766 Lombard et al. (2010c)
T
Ca. pseudospathiphylli CBS 109165 FJ918513 GQ267412 FJ918562 AF348241 KY653435 GQ280615 GQ280737 Kang et al. (2001), Lombard et al. (2010c, d), present study
Ca. pseudospathulata CBS 134841T KM395983 KM396070 KM395896 KM396153 – – – Alfenas et al. (2015)
Ca. pseudovata CBS 134675 T
KM395946 KM396033 KM395859 KM396116 – – – Alfenas et al. (2015)
Ca. pteridis CBS 111793T DQ190578 GQ267413 FJ918563 DQ190679 KY653438 GQ280616 GQ280738 Crous et al. (2006a), Lombard et al. (2010c, d), present study
Ca. putriramosa CBS 111449 T
KX784656 KX784591 KX784728 – KY653440 KY653277 KY653333 Lombard et al. (2016), present study
Ca. queenslandica CBS 112146T AF389835 GQ267415 FJ918543 FJ918521 – GQ280618 GQ280740 Kang et al. (2001), Lombard et al. (2010c, d)
Ca. quinqueramosa CBS 134654 T
KM395942 KM396029 KM395855 KM396112 – – – Alfenas et al. (2015)
Ca. reteaudii CBS 112144T AF389833 GQ267417 FJ918537 DQ190661 KY653443 GQ280620 GQ280742 Kang et al. (2001), Lombard et al. (2010c, d), present study
Ca. robigophila CBS 134652 T
KM395937 KM396024 KM395850 KM396107 – – – Alfenas et al. (2015)
Ca. rumohrae CBS 111431T AF232871 GQ267419 FJ918549 DQ190675 KY653445 GQ280622 GQ280744 Crous et al. (1999), Lombard et al. (2010c), present study
T
Ca. seminaria CBS 136632 KJ462998 KJ463115 KJ462885 KJ463231 KY653446 KY653279 KY653335 Lombard et al. (2015), present study
Ca. silvicola CBS 135237T KM395978 KM396065 KM395891 KM396148 – – – Alfenas et al. (2015)
T
Ca. spathulata CBS 555.92 GQ267215 GQ267426 FJ918554 GQ267261 KY653449 GQ280630 GQ280752 Lombard et al. (2010c, d), present study
Ca. spathiphylli CBS 114540 AF348214 GQ267424 GQ267330 AF348230 KY653447 GQ280627 GQ280749 Kang et al. (2001), Lombard et al. (2010c), present study
Ca. sphaeropendunculata CBS 136081T KJ463003 KJ463120 KJ462890 KJ463236 – – – Lombard et al. (2015)
Ca. stipitata CBS 112513 T
KX784661 KX784596 KX784734 – KY653450 KY653280 KY653336 Lombard et al. (2016), present study
Ca. sulawesiensis CBS 125277T GQ267222 GQ267434 GQ267342 GQ267271 – GQ280637 GQ280759 Lombard et al. (2010c)
Ca. sumatrensis CBS 112829T AY725649 AY725771 AY725733 AY725696 – GQ280654 GQ280776 Crous et al. (2004c), Lombard et al. (2010c)
www.studiesinmycology.org
GENERA
OF PHYTOPATHOGENIC FUNGI
119
MARIN-FELIX ET AL.
branches aseptate, 11–19 × 3–5 μm, each terminal branch Material examined: Ecuador, from soil, 20 Jun. 1997, M.J.
producing 2–4 phialides; phialides elongate doliiform to reniform, Wingfield (holotype CBS H-23136, culture ex-type CBS
hyaline, aseptate, 6–14 × 2–4 μm, apex with minute periclinal 111423 = CPC 1650).
thickening and inconspicuous collarette. Macroconidia cylindri-
cal, rounded at both ends, straight, (44–)47–59(–71) × (3–) Notes: Calonectria octoramosa is a new species in the Ca.
3.5–4.5(–6) μm (av. 53 × 4 μm), 1-septate, lacking a visible brassicae complex. It can be distinguished from other species in
abscission scar, held in parallel cylindrical clusters by colourless this complex by having eight levels of branching in its con-
slime. Mega- and microconidia not observed. idiogenous apparatus.
Culture characteristics: Colonies moderately fast growing Calonectria parvispora L. Lombard & Crous, sp. nov. Myco-
(35–55 mm diam) on MEA after 1 wk at room temperature; Bank MB820844. Fig. 16.
surface sienna with sparse buff to white, woolly aerial mycelium
with moderate sporulation on the aerial mycelium and colony Etymology: Name refers to the small macroconidia of this fungus.
surface; reverse sienna with abundant chlamydospores
throughout the medium, forming microsclerotia. Macroconidiophores consist of a stipe bearing a penicillate
arrangement of fertile branches, and a stipe extension terminating
Material examined: Brazil, from soil in Eucalyptus plantation, in a vesicle; stipe septate, hyaline, smooth, 36–152 × 7–9 μm;
1996, P.W. Crous (holotype CBS H-23135, culture ex-type CBS stipe extension septate, straight to flexuous, 137–277 μm long,
116249 = CPC 3533). 3–6 μm wide at the apical septum, terminating in a clavate vesicle,
4–8 μm diam. Conidiogenous apparatus 56–92 μm wide, and
Notes: Calonectria nemoralis is closely related to Ca. pseudo- 50–70 μm long; primary branches aseptate, 16–34 × 4–7 μm;
vata. The macroconidia of Ca. nemoralis [(44–) secondary branches aseptate, 11–20 × 4–6 μm; tertiary branches
47–59(–71) × (3–)3.5–4.5(–6) μm (av. 53 × 4 μm)] are smaller aseptate, 7–15 × 3–5 μm; quaternary branches and additional
than those of Ca. pseudovata [(55–)67–70(–80) × (4–)5 branches (–6) aseptate, 8–16 × 3–5 μm, each terminal branch
(–7) μm (av. 69 × 5 μm); Alfenas et al. 2015]. Furthermore, no producing 2–6 phialides; phialides doliiform to reniform, hyaline,
microconidiophores and microconidia were observed in Ca. aseptate, 7–12 × 3–5 μm, apex with minute periclinal thickening
nemoralis, although they are readily produced by Ca. pseudo- and inconspicuous collarette. Macroconidia cylindrical, rounded at
vata (Alfenas et al. 2015). both ends, straight, (24–)26–32(–36) × (3–)3.5–4.5(–5) μm (av.
29 × 4 μm), 1-septate, lacking a visible abscission scar, held in
Calonectria octoramosa L. Lombard & Crous, sp. nov. parallel cylindrical clusters by colourless slime. Mega- and
MycoBank MB820851. Fig. 15. microconidia not observed.
Etymology: Name refers to the eight levels of branching of the Culture characteristics. Colonies fast growing (50–75 mm
conidiogenous apparatus. diam) on MEA after 1 wk at room temperature; surface
umber to sepia with abundant buff to white, woolly aerial
Macroconidiophores consist of a stipe bearing a penicillate mycelium and abundant sporulation on the aerial mycelium
arrangement of fertile branches, and a stipe extension terminating and colony surface; reverse amber to sepia with abundant
in a vesicle; stipe septate, hyaline, smooth, 34–170 × 6–10 μm; chlamydospores throughout the medium, forming
stipe extension septate, straight to flexuous, 118–262 μm long, microsclerotia.
3–8 μm wide at the apical septum, terminating in a clavate
vesicle, 4–8 μm diam. Conidiogenous apparatus 58–128 μm Material examined: Brazil, from soil, Jun. 1998, A.C. Alfenas
wide, and 50–90 μm long; primary branches aseptate, (holotype CBS H-22765, culture ex-type CBS 111465 = CPC
14–31 × 5–8 μm; secondary branches aseptate, 1902). Colombia, La Paz, Rodal Seuiller, from soil, Jan. 1994,
10–23 × 4–6 μm; tertiary branches aseptate, 7–19 × 3–5 μm; P.W. Crous, CBS 116108 = CPC 726.
quaternary branches and additional branches (–8) aseptate,
8–14 × 3–5 μm, each terminal branch producing 2–6 phialides; Notes: Calonectria parvispora is a new species in the Ca. brassicae
phialides doliiform to reniform, hyaline, aseptate, 6–12 × 3–5 μm, complex (Lombard et al. 2009, Alfenas et al. 2015). The macro-
apex with minute periclinal thickening and inconspicuous collar- conidia of Ca. parvispora [(24–)26–32(–36) × (3–)
ette. Macroconidia cylindrical, rounded at both ends, straight, 3.5–4.5(–5) μm (av. 29 × 4 μm)] are smaller than those of Ca.
(32–)34–38(–39) × 4–5 μm (av. 36 × 4 μm), 1(–3)-septate, clavata [(44–)50–70(–80) × (4–)5–6 μm (av. 65 × 5 μm); Crous
lacking a visible abscission scar, held in parallel cylindrical clusters 2002], Ca. brachiatica [(37–)40–48(–50) × 4–6 μm (av.
by colourless slime. Mega- and microconidia not observed. 44 × 5 μm); Lombard et al. 2009], Ca. brassicae [(38–)
40–55(–65) × (3.5–)4–5(–6) μm (av. 53 × 4.5 μm); Crous 2002],
Culture characteristics: Colonies fast growing (60–75 mm diam) Ca. ecuadoriae [(45–)48–55(–65) × (4–)4.5(–5) μm (av.
on MEA after 1 wk at room temperature; surface cinnamon to 51 × 4.5 μm); Crous et al. 2006a], Ca. gracilipes [(35–)
brick with abundant white woolly aerial mycelium and abundant 40–48(–60) × 4–5(–6) μm (av. 45 × 4.5 μm); Crous 2002] and Ca.
sporulation on the aerial mycelium and colony surface; reverse gracilis [(40–)53–58(–65) × (3.5–)4–5 μm (av. 56 × 4.5 μm);
brick to sepia with abundant chlamydospores throughout the Crous 2002].
medium, forming microsclerotia.
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GENERA OF PHYTOPATHOGENIC FUNGI
0.02
Fig. 11. The Maximum Likelihood (ML) consensus tree inferred from the combined cmdA, tef1 and tub2 sequence alignments. Thickened lines indicate branches present in the
ML, Maximum parsimony (MP) and Bayesian consensus trees. Branches with ML-bootstrap (BS) & MP-BS = 100 % and posterior probabilities (PP) = 1.00 are in blue.
Branches with ML-BS & MP-BS 75 % and PP 0.95 are in green. The scale bar indicates 0.02 expected changes per site. The tree is rooted to Calonectria braziliensis
(CBS 230.51). Ex-type strains are indicated in bold. GenBank accession numbers are indicated in Lombard et al. (2010a, 2015, 2016) and Alfenas et al. (2015). TreeBASE:
S20877.
www.studiesinmycology.org 121
MARIN-FELIX ET AL.
Fig. 12. Calonectria ecuadorensis (ex-type CBS 111706). A, B. Macroconidiophores. C−E. Conidiogenous apparatus with conidiophore branches and doliiform to reniform
phialides. F−I. Clavate vesicles. J. Macroconidia. Scale bars: A, B = 50 μm; C−J = 10 μm.
122
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 13. Calonectria longiramosa (ex-type CBS 116319). A−C. Macroconidiophores. D−F. Conidiogenous apparatus with conidiophore branches and elongate doliiform to
allantoid phialides. G−J. Clavate vesicles. K. Macroconidia. Scale bars: A−C = 50 μm; D−K = 10 μm.
Calonectria tucuruiensis L. Lombard & Crous, sp. nov. Macroconidiophores consist of a stipe bearing a penicillate
MycoBank MB820845. Fig. 17. arrangement of fertile branches, and a stipe extension ter-
minating in a vesicle; stipe septate, hyaline, smooth,
Etymology: Name refers to Tucuruí, the region in Brazil from 35–105 × 6–9 μm; stipe extension septate, straight to flex-
which this fungus was collected. uous, 165– 290 μm long, 4–6 μm wide at the apical septum,
www.studiesinmycology.org 123
MARIN-FELIX ET AL.
Fig. 14. Calonectria nemoralis (ex-type CBS 116319). A, B. Macroconidiophores. C−D. Conidiogenous apparatus with conidiophore branches and doliiform to reniform
phialides. E. Macroconidia. F−I. Fusiform to ovoid vesicles. Scale bars: A, B = 50 μm; C−I = 10 μm.
terminating in a fusiform to ovoid to ellipsoid vesicle, 9 –12 μm 11–16 × 3–6 μm; quaternary branches aseptate,
diam. Conidiogenous apparatus 40–95 μm wide, and 8–14 × 3–4 μm each terminal branch producing 2–4 phia-
40–90 μm long; primary branches aseptate, lides; phialides elongate doliiform to reniform, hyaline, asep-
19–32 × 4–7 μm; secondary branches aseptate, tate, 8–17 × 3–5 μm, apex with minute periclinal
10–28 × 3–5 μm; tertiary branches aseptate, thickening and inconspicuous collarette. Macroconidia
124
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 15. Calonectria octoramosa (ex-type CBS 111423). A−C. Macroconidiophores. D−F. Conidiogenous apparatus with conidiophore branches and doliiform to reniform
phialides. G−J. Clavate vesicles. K. Macroconidia. Scale bars: A−C = 20 μm; D−K = 10 μm.
cylindrical, rounded at both ends, straight, (51–) Culture characteristics. Colonies fast growing (55–75 mm diam)
57–69(–71) × (4–)4.5–5.5( –6) μm (av. 63 × 5 μm), 1- on MEA after 1 wk at room temperature; surface cinnamon to
septate, lacking a visible abscission scar, held in parallel amber with sparse, buff to white, woolly aerial mycelium and
cylindrical clusters by colourless slime. Mega- and micro- abundant sporulation on the aerial mycelium and colony surface;
conidia not observed.
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MARIN-FELIX ET AL.
Fig. 16. Calonectria parvispora (ex-type CBS 111465). A−C. Macroconidiophores. D−F. Conidiogenous apparatus with conidiophore branches and doliiform to reniform
phialides. G−J. Clavate vesicles. K. Macroconidia. Scale bars: A−C = 20 μm; D−K = 10 μm.
reverse sienna to amber with abundant chlamydospores Type species: Ceratocystis fimbriata Ellis & Halst. Neotype: BPI
throughout the medium, forming microsclerotia. 595863.
Material examined: Brazil, Tucuruí, from leaves of Eucalyptus DNA barcodes (genus): 60S, LSU, mcm7.
tereticornis, 8 Aug. 1996, P.W. Crous (holotype CBS H-22777,
culture ex-type CBS 114755 = CPC 1403); ibid., CBS DNA barcodes (species): ITS, bt1, tef1, rpb2, ms204. Table 4.
116265 = CPC 3552.
Ascomata perithecial, scattered or gregarious, immersed,
Notes: Calonectria tucuruiensis is closely related to Ca. terricola partially embedded or superficial on the substrate; bases sub-
(Fig. 11). The macroconidia of Ca. tucuruiensis [(51–) globose to globose or obpyriform, brown to black, covered with
57–69(–71) × (4–)4.5–5.5(–6) μm (av. 63 × 5 μm)] are larger undifferentiated hyphae; ostiolar necks central, long, tapering
than those of Ca. terricola [(40–)43–49(–53) × (3–)4–5(–6) μm towards apex; ascomatal apex straight or undulate, unbranched
(av. 46 × 4.5 μm); Lombard et al. (2016)]. or branched, brown to black and becoming paler; ostiolar hyphae
divergent or convergent, non-septate, straight, tapering towards
Authors: L. Lombard & P.W. Crous apex, hyaline to light brown. Asci evanescent. Ascospores hy-
aline, 1-celled, ellipsoidal with gelatinous sheath which gives hat-
shaped impression, accumulating in white, creamy to yellow
Ceratocystis Ellis & Halst., New Jersey Agric. Coll. Exp. Sta.
masses at tips of necks. Conidiophores branched, straight or
Bull. 76: 14. 1890. Fig. 18.
Synonym: Rostrella Zimm., Meded. Lands Plantentuin 37: 24, flexuous, hyaline to pale brown. Conidiogenous cells endophia-
41. 1900. lidic, flask-shaped (lageniform) producing various shapes of
cylindrical conidia or tubular-form producing barrel-shaped
Classification: Sordariomycetes, Hypocreomycetidae, Micro- (doliiform) conidia, either lageniform alone or both forms pre-
ascales, Ceratocystidaceae. sent. Conidia hyaline, 1-celled, doliiform to cylindrical.
126
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 17. Calonectria tucuruiensis (ex-type CBS 114755). A−C. Macroconidiophores. D−F. Conidiogenous apparatus with conidiophore branches and elongate doliiform to
reniform phialides. G−J. Fusiform to ovoid to ellipsoid vesicles. K. Macroconidia. Scale bars: A−C = 50 μm; D−K = 10 μm.
Aleurioconidia (in some literature as chlamydospores) absent or Notes: Ceratocystis sensu lato included a heterogeneous
present, pale brown to dark brown, pyriform, ellipsoidal to group of fungi classified under this generic name due to similar
globose, singly or in chains. morphology resulting from convergent evolution, despite their
diverse ecological and biological features (Upadhyay 1981).
Culture characteristics: Colonies showing circular growth with The group has recently been divided into seven more narrowly
undulate margins, mycelium submerged to aerial, colour ranging defined homogeneous genera, supported by multigene phy-
from moderate yellowish brown to greyish or brownish olive logenies, morphological similarities and ecological commonality
when mature, releasing sweet fruity aroma. No growth on (Wingfield et al. 2013a, De Beer et al. 2014). The family
cycloheximide. Ceratocystidaceae includes nine genera, namely Ambrosiella,
Ceratocystis, Chalaropsis, Davidsoniella, Endoconidiophora,
Optimal media and cultivation conditions: 2 % MEA incubated at Huntiella, Thielaviopsis, Meredithiella and Phialophoropsis (De
25 °C. Addition of thiamin stimulates the development of sexual Beer et al. 2014, Mayers et al. 2015). Ceratocystis sensu
morph. stricto is now restricted to those species producing ascomata
with smooth bases, ascospores with hat-shaped sheaths, and
Distribution: Worldwide. thielaviopsis-like asexual morphs, which differentiate them from
other genera (De Beer et al. 2014). Within Ceratocystis,
Hosts: Herbaceous root crops, Ipomea batatas (sweet potato), morphological differences between species are insignificant
wounds or larval tunnels of woody angiosperms, Acacia, and phylogenies based on multiple gene regions are used to
Annona, Carya, Citrus, Coffea, Colocacia, Colophospermum, distinguish them from each other (Fourie et al. 2015). The ITS
Combretum, Corymbia, Cunninghamia, Dalbergia, Eucalyptus, region has been widely used for delimiting species of Cera-
Coffea, Mangifera, Platanus, Populus, Prosopis, Punica, Quer- tocystis (Schoch et al. 2012). However, discovery of multiple
cus, Rapanea, Saccharum, Schizolobium, Schotia, Styrax, ITS types within single species in the genus (Al Adawi et al.
Syzygium, Terminalia, Theobroma. Some known to be vectored 2013, Naidoo et al. 2013, Harrington et al. 2014) raised an
by flies (Diptera), non-specific ambrosia beetles (Scolytinae), or awareness that the ITS region alone should not be applied to
nitidulid beetles (Nitidulidae), but without specific insect delimit species in Ceratocystis, and that additional gene re-
associates. gions should also be considered. Loci such as bt1 and tef1 do
not provide good species resolution on their own, but provide
Disease symptoms: Root rot, cankers and vascular stain. strong support in combination with ITS (Fourie et al. 2015).
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MARIN-FELIX ET AL.
Fig. 18. A. Sweet potatoes (Ipomea batatas) infected with Ceratocystis fimbriata. B−O. Microscopic features of Ceratocystis fimbriata (CBS 114723 = CMW 14799) on 2 %
MEA. B. Ascomata with yellowish droplets of ascospores at tips of necks, with asexual state (white background). C. Young ascoma. D. Mature ascoma. E. Ostiolar hyphae. F, G.
Ascospores. H, I. Aleurioconidia. J. Conidiogenous cells producing aleurioconidia (black arrow) and cylindrical-shape conidia (white arrow). K–O. Conidia of various shapes in
chains. Scale bars: B = 500 μm; C, D = 100 μm; E = 50 μm; F, G, K–O = 10 μm; H = 50 μm; I, J = 25 μm.
128
Table 4. DNA barcodes of accepted Ceratocystis spp.
Species Isolates1 GenBank accession numbers2 References
ITS bt1 tef1 ms204 rpb2
www.studiesinmycology.org
Ceratocystis adelpha CBS 115169T DQ520637 KJ601509 KJ601516 – – Van Wyk et al. (2006), Fourie et al. (2015)
Ce. albifundus CBS 128992 DQ520638 EF070429 EF070400 – – Van Wyk et al. (2006, 2007)
Ce. atrox CBS 120518T NR_136981; EF070415 EF070431 EF070403 – – Van Wyk et al. (2007)
Ce. cacaofunesta CBS 115172 T
AY157953 KJ601512 KJ601519 – – Baker et al. (2003), Fourie et al. (2015)
Ce. caryae CBS 114716T NR_119530; AY907035; EF070424 EF070439 EF070412 – – Johnson et al. (2005), Van Wyk et al. (2007)
Ce. cercfabiensis CBS 139654 T *
KP727592; KP727593; KP727594 KP727618 KP727643 – – Liu et al. (2015a)
Ce. collisensis CBS 139679T KP727578 KP727614 KP727639 – – Liu et al. (2015a)
T
Ce. colombiana CBS 121792 NR_119483; AY177233 AY177225 EU241493 KJ601567 KJ601603 Marin et al. (2003), Van Wyk et al. (2010),
Fourie et al. (2015)
Ce. corymbiicola CBS 127215T NR_119830; HM071902 HM071914 HQ236453 – – Kamgan Nkuekam et al. (2012)
Ce. curvata CBS 122603T NR_137018; FJ151436 FJ151448 FJ151470 KJ601570 KJ601606 Van Wyk et al. (2011b), Fourie et al. (2015)
T
Ce. diversiconidia CBS 123013 FJ151440 FJ151452 FJ151474 KJ601571 KJ601607 Van Wyk et al. (2011b), Fourie et al. (2015)
Ce. ecuadoriana CBS 124020T FJ151432 FJ151444 FJ151466 KJ601573 KJ601609 Van Wyk et al. (2011b), Fourie et al. (2015)
T
Ce. eucalypticola CBS 124016 FJ236723 FJ236783 FJ236753 KJ601576 KJ601612 Van Wyk et al. (2012), Fourie et al. (2015)
Ce. ficicola MAFF 625119T NR_119410 KY685077 KY316544 KY685080 KY685082 Kajitani & Masuya (2011)
Ce. fimbriata CBS 114723 KC493160 KF302689 KJ631109 KJ601578 KJ601614 Luchi et al. (2013), Fourie et al. (2015)
Ce. fimbriatomima CBS 121786T EF190963 EF190951 EF190957 KJ601579 KJ601615 Van Wyk et al. (2009b), Fourie et al. (2015)
Ce. harringtonii CBS 119.78 EF070418 EF070434 EF070406 – – Van Wyk et al. (2007)
Ce. larium CBS 122512T NR_137016; EU881906 EU881894 EU881900 – – Van Wyk et al. (2009a)
T
Ce. mangicola CBS 114721 AY953382 EF433307 EF433316 KJ601582 KJ601618 Van Wyk et al. (2005), Van Wyk et al. (2011a),
Fourie et al. (2015)
Ce. manginecans CBS 121659T NR_119532; AY953383* EF433308 EF433317 KJ601584 KJ601620 Van Wyk et al. (2005, 2007), Fourie et al. (2015)
T
Ce. mangivora CBS 128340 FJ200262 FJ200275 FJ200288 KJ601587 KJ601623 Van Wyk et al. (2011a), Fourie et al. (2015)
T
Ce. neglecta CBS 121789 NR_137552; EF127990 EU881898 EU881904 KJ601588 KJ601624 Rodas et al. (2008), Van Wyk et al. (2009a),
Fourie et al. (2015)
GENERA
Ce. obpyriformis CBS 122511T EU245003 EU244975 EU244935 – – Heath et al. (2009)
Ce. papillata CBS 121793T NR_119486; AY233867 AY233874 EU241484 KJ601590 KJ601626 Van Wyk et al. (2010), Fourie et al. (2015)
OF PHYTOPATHOGENIC FUNGI
T
Ce. pirilliformis CBS 118128 NR_119452; AF427105 DQ371653 AY528983 KJ601594 KJ601630 Barnes et al. (2003), Van Wyk et al. (2004, 2006),
Fourie et al. (2015)
Ce. platani CBS 115162PT DQ520630 EF070425 EF070396 KJ601592 KJ601628 Van Wyk et al. (2006, 2007), Fourie et al. (2015)
Ce. polychroma CBS 115778T AY528970 AY528966 AY528978 – – Van Wyk et al. (2004)
Ce. polyconidia CBS 122289T EU245006 EU244978 EU244938 – – Heath et al. (2009)
Ce. smalleyi CBS 114724 T
NR_119529; AY907030; EF070420 EF070436 EF070408 – – Johnson et al. (2005), Van Wyk et al. (2007)
129
ITS: internal transcribed spacers and intervening 5.8S nrDNA; bt1: partial β-tubulin gene; tef1: partial translation elongation factor 1-alpha gene, ms204: partial guanine nucleotide-binding protein subunit beta-like protein gene; rpb2: partial RNA
The loci rpb2 and ms204 give stronger resolution than tef1 and
bt1, but also need to be used in combination with ITS (Fourie
CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands; MAFF: Ministry of Agriculture, Forestry and Fisheries, Tsukuba, Ibaraki, Japan. T and PT indicate ex-type and ex-paratype, respectively.
2014a, b, Wingfield et al. 2015, 2016a, b (genomes);
References
diales, Cladosporiaceae.
–
–
–
EU244931
KC691504
KC691506
EF408576
EF070409
KC691482
EF408569
EF070437
NR_119633; EF408555
KC691458
CBS 131280T
Ce. zambeziensis
130
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 19. Cladosporium spp. A–H. Sexual morphs. A. Ascomata on host tissue (arrows) of Cladosporium silenes (holotype CBS H-19874). B. Ascoma and asci of Cladosporium
herbarum (CPC 11600). C. Ostiole of Cladosporium macrocarpum (CBS 299.67). D, E. Asci of Cladosporium herbarum (CPC 11600). F, G. Ascospores of Cladosporium
herbarum (CPC 11600). H. Ascospores (arrow denotes mucoid appendage) of Cladosporium silenes (holotype CBS H-19874). I–O. Asexual morphs. I. Conidiophores of
Cladosporium halotolerans (ex-type CBS 119416). J. Fascicle of conidiophores of Cladosporium soldanellae (BPI 427476). K. Macronematous conidiophores and conidial
chains of Cladosporium cladosporioides (ex-neotype CBS 112388). L. Conidial chains, septa of secondary ramoconidia distinctly darkened of Cladosporium paracladosporioides
(ex-type CBS 171.54). M. CryoSEM of different types of conidia on aerial structures of Cladosporium exile (ex-type CBS 125987). Note a remarkable pattern of blastoconidium
formation (backwards) (arrow). N. Secondary ramoconidia, conidia and scars of Cladosporium perangustum (ex-type CBS 125996). O. Whorls of secondary ramoconidia and
conidia of Cladosporium scabrellum (ex-type CBS 126358). Scale bars: B, C, M, O = 5 μm; D–H, K, L = 10 μm; I = 100 μm; J = 50 μm; N = 2 μm. Pictures taken from Bensch
et al. (2012).
or nodulose, sometimes with unilateral swellings; conidiogenous verruculose, verrucose, echinulate, cristate; hila protuberant,
loci usually conspicuous, protuberant, composed of a central coronate, with a central convex dome and raised periclinal rim,
convex dome surrounded by a more or less raised periclinal rim thickened, refractive to darkened; microcyclic conidiogenesis
(coronate), thickened, refractive or barely to distinctly darkened; often occurring. In vitro: Stromata usually lacking. Co-
conidial formation holoblastic. Conidia solitary or catenate, in nidiophores usually solitary, arising terminally or laterally from
unbranched or branched acropetal chains, amero- to phrag- plagiotropous or ascending hyphae, often longer than in vivo.
mosporous, shape and septation variable, usually subglobose, Micronematous conidiophores, lacking in vivo, are often formed
ovoid, obovoid, ellipsoid, fusiform, limoniform to cylindrical, in culture. Conidial chains often longer than in vivo (species with
aseptate or with several transverse eusepta, rarely with a single solitary conidia are often capable of forming conidial chains in
longitudinal septum, subhyaline to usually pigmented, smooth, culture).
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MARIN-FELIX ET AL.
132
GENERA OF PHYTOPATHOGENIC FUNGI
Table 5. (Continued).
Species Isolates1 GenBank accession numbers2 References
ITS act tef1
ET
Cl. iridis CBS 138.40 EF679370 EF679523 EF679447 Schubert et al. (2007)
T
Cl. kenpeggii CBS 142613 KY646222 KY646225 KY646228 Present study
Cl. langeronii CBS 189.54NT DQ780379 EF101357 JN906990 Zalar et al. (2007), Bensch et al. (2012)
ET
Cl. licheniphilum CBS 125990 HM148111 HM148600 HM148355 Bensch et al. (2010)
Cl. limoniforme CBS 140484T KT600397 KT600592 KT600494 Bensch et al. (2015)
T
Cl. longicatenatum CBS 140485 KT600403 KT600598 KT600500 Bensch et al. (2015)
Cl. longissimum CBS 140485T DQ780352 EF101385 EU570259 Zalar et al. (2007), Dugan et al. (2008)
RS
Cl. lycoperdinum CBS 574.78C HM148115 HM148604 HM148359 Bensch et al. (2010)
Cl. macrocarpum CBS 121623NT EF679375 EF679529 EF679453 Schubert et al. (2007)
T
Cl. montecillanum CBS 140486 KT600406 KT600602 KT600504 Bensch et al. (2015)
Cl. myrtacearum CBS 126350ET HM148117 HM148606 HM148361 Bensch et al. (2010)
ET
Cl. ossifragi CBS 842.91 EF679381 EF679535 EF679459 Schubert et al. (2007)
Cl. oxysporum CBS 125991RS HM148118 HM148607 HM148362 Bensch et al. (2010)
T
Cl. paracladosporioides CBS 171.54 HM148120 HM148609 HM148364 Bensch et al. (2010)
Cl. parapenidielloides CBS 140487T KT600410 KT600606 KT600508 Bensch et al. (2015)
T
Cl. penidielloides CBS 140489 KT600412 KT600608 KT600510 Bensch et al. (2015)
Cl. perangustum CBS 125996T HM148121 HM148610 HM148365 Bensch et al. (2010)
T
Cl. phaenocomae CBS 128769 JF499837 JF499881 JF499875 Crous & Groenewald (2011)
Cl. phlei CBS 358.69ET JN906981 JN907000 JN906991 Bensch et al. (2012)
T
Cl. phyllactiniicola CBS 126352 HM148150 HM148639 HM148394 Bensch et al. (2010)
Cl. phyllophilum CBS 125992ET HM148154 HM148643 HM148398 Bensch et al. (2010)
T
Cl. pini-ponderosae CBS 124456 FJ936160 FJ936167 FJ936164 Schubert et al. (2009)
Cl. pseudiridis CBS 116463T EF679383 EF679537 EF679461 Schubert et al. (2007)
T
Cl. pseudochalastosporioides CBS 140490 KT600415 KT600611 KT600513 Bensch et al. (2015)
Cl. pseudocladosporioides CBS 125993T HM148158 HM148647 HM148402 Bensch et al. (2010)
T
Cl. psychrotolerans CBS 119412 DQ780386 EF101365 JN906992 Zalar et al. (2007), Bensch et al. (2012)
Cl. puyae CBS 274.80AT KT600418 KT600614 KT600516 Bensch et al. (2015)
T
Cl. ramotenellum CBS 121628 EF679384 EF679538 EF679462 Schubert et al. (2007)
Cl. rectoides CBS 125994T HM148193 HM148683 HM148438 Bensch et al. (2010)
Cl. rhusicola CBS 140492T KT600440 KT600637 KT600539 Bensch et al. (2015)
T
Cl. ruguloflabelliforme CBS 140494 KT600458 KT600655 KT600557 Bensch et al. (2015)
Cl. rugulovarians CBS 140495T KT600459 KT600656 KT600558 Bensch et al. (2015)
T
Cl. salinae CBS 119413 DQ780374 EF101390 JN906993 Zalar et al. (2007), Bensch et al. (2012)
Cl. scabrellum CBS 126358T HM148195 HM148685 HM148440 Bensch et al. (2010)
T
Cl. silenes CBS 109082 EF679354 EF679506 EF679429 Schubert et al. (2007)
Cl. sinuosum CBS 121629T EF679386 EF679540 EF679464 Schubert et al. (2007)
NT
Cl. soldanellae CBS 132186 JN906982 JN907001 JN906994 Bensch et al. (2012)
Cl. sphaerospermum CBS 193.54NT DQ780343 EF101380 EU570261 Zalar et al. (2007), Dugan et al. (2008)
T
Cl. spinulosum CBS 119907 EF679388 EF679542 EF679466 Schubert et al. (2007)
Cl. subcinereum CBS 140465T LN834433 LN834529 LN834617 Sandoval-Denis et al. (2016)
T
Cl. subinflatum CBS 121630 EF679389 EF679543 EF679467 Schubert et al. (2007)
Cl. subtilissimum CBS 113754T EF679397 EF679551 EF679475 Schubert et al. (2007)
T
Cl. subuliforme CBS 126500 HM148196 HM148686 HM148441 Bensch et al. (2010)
Cl. succulentum CBS 140466T LN834434 LN834618 LN834530 Sandoval-Denis et al. (2016)
T
Cl. tenellum CBS 121634 EF679401 EF679555 EF679479 Schubert et al. (2007)
Cl. tenuissimum CBS 125995ET HM148197 HM148687 HM148442 Bensch et al. (2010)
T
Cl. tuberosum CBS 140693 LN834417 LN834601 LN834513 Sandoval-Denis et al. (2016)
Cl. uredinicola ATCC 46649 AY251071 HM148712 HM148467 Braun et al. (2003), Bensch et al. (2010)
ET
Cl. variabile CBS 121635 EF679402 EF679556 EF679480 Schubert et al. (2007)
(continued on next page)
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MARIN-FELIX ET AL.
Table 5. (Continued).
Species Isolates1 GenBank accession numbers2 References
ITS act tef1
T
Cl. varians CBS 126362 HM148224 HM148715 HM148470 Bensch et al. (2010)
T
Cl. velox CBS 119417 DQ780361 EF101388 JN906995 Zalar et al. (2007), Bensch et al. (2012)
Cl. verrucocladosporioides CBS 126363T HM148226 HM148717 HM148472 Bensch et al. (2010)
T
Cl. versiforme CBS 140491 KT600417 KT600613 KT600515 Bensch et al. (2015)
Cl. welwitschiicola CBS 142614T KY646223 KY646226 KY646229 Present study
Cl. xanthochromaticum CBS 140691T LN834415 LN834599 LN834511 Sandoval-Denis et al. (2016)
Cl. xylophilum CBS 125997T HM148230 HM148721 HM148476 Bensch et al. (2010)
1
ATCC: American Type Culture Collection, Virginia, USA; CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands; CPC: Culture collection of Pedro Crous,
housed at Westerdijk Fungal Biodiversity Institute. T, ET, NT and RS indicate ex-type, ex-epitype, ex-neotype and reference strains, respectively.
2
ITS: internal transcribed spacers and intervening 5.8S nrDNA; act: partial actin gene; tef1: partial translation elongation factor 1-alpha gene.
Culture characteristics: Colonies on SNA often grey olivaceous Optimal media and cultivation conditions: For morphological
or olivaceous grey, reverse leaden-grey or black, flat, velvety examinations SNA incubated under continuous near-ultraviolet
with fluffy or cottony patches, margin irregular or undulate, aerial light at 25 °C proved to be best suited to promote sporulation.
mycelium loose diffuse or more abundantly formed, often with The sexual morph can be induced by inoculating plates of 2 %
abundant submerged mycelium. WA onto which autoclaved stem pieces of Urtica dioica
134
GENERA OF PHYTOPATHOGENIC FUNGI
(European stinging nettle) are placed. Inoculated plates have to differentiated conidiophores in most of the species (Bensch et al.
be incubated on the laboratory bench for 1 wk, after that period 2012, 2015). Morphologically similar genera have been treated
they have to be further incubated at 10 °C in the dark for 1–2 mo in Crous et al. (2007b).
to stimulate sexual morph development. Members of Cladosporiaceae: Cladosporium, Graphiopsis,
Neocladosporium, Rachicladosporium, Toxicocladosporium,
Distribution: Worldwide. Verrucocladosporium.
Hosts: Asparagaceae, Asteraceae, Fabaceae, Myrtaceae, References: Braun et al. 2003 (sexual morph); Crous et al.
Orchidaceae, Poaceae and many other hosts, including fungi 2007a, b (cladosporium-like genera); Schubert et al. 2007
and insects. (morphology, phylogeny Cl. herbarum complex); Zalar et al.
2007 (morphology, phylogeny Cl. sphaerospermum com-
Disease symptoms: Leaf spots, leaf blight, discolourations, ne- plex); Bensch et al. 2010 (morphology, phylogeny Cl. clado-
crosis, or shot-hole symptoms, on stems and fruits, but also sporioides complex); Bensch et al. 2012 (morphology,
saprobic, endophytic or isolated from numerous substrates and phylogeny and key of all Cladosporium species); Bensch et al.
environments, e.g. indoor environments, salterns and human 2015 (morphology, additions to the three species complexes);
and animal infections. Sandoval-Denis et al. 2016 (morphology, phylogeny of clinical
samples).
Notes: The monophyletic genus Cladosporium is well charac-
terised by the coronate structure of its conidiogenous loci and Cladosporium chasmanthicola Bensch, U. Braun & Crous, sp.
conidial hila, consisting of a central convex dome surrounded nov. MycoBank MB819978. Fig. 21.
by a raised periclinal rim (David 1997, Braun et al. 2003). At
the moment it comprises about 200 species. Cladosporium Etymology: Epithet composed of the name of the host genus,
was previously extremely heterogeneous and encompassed Chasmanthe, and -cola, dweller.
772 names assigned to this genus (Dugan et al. 2004).
Heuchert et al. (2005) examined Cladosporium spp. dwelling Leaf spots solitary, distributed over leaf surface, amphigenous,
on other fungi, and Schubert (2005) provided a comprehensive ellipsoid, 1–2 mm diam, pale brown with dark red-brown margin,
treatment of foliicolous species. Crous et al. (2007a) encom- some spots also associated with uredinia of Uromyces kenta-
passed a series of papers dealing with a reassessment and niensis. On SNA: Mycelium loosely branched, filiform, narrowly
new circumscription of Cladosporium s. str. and treatments of cylindrical-oblong or irregular in outline due to swellings and
several cladosporioid genera. Bensch et al. (2012) published a constrictions, 0.5–4 μm wide, septate, subhyaline or pale
taxonomic monograph of the genus Cladosporium which can olivaceous or olivaceous brown, almost smooth, verruculose,
be consulted for further information on the history and many distinctly verrucose or irregularly rough-walled. Conidiophores
other aspects of this genus. solitary, formed terminally or laterally from hyphae, straight or
Species delimitation in Cladosporium based on morphology somewhat flexuous, macro- and micronematous; macro-
alone is limited since many species have overlapping char- nematous conidiophores cylindrical, sometimes geniculate, often
acters. Some key differential features have been identified and irregular in outline due to lateral outgrowths, swellings and
detailed in a series of monographic papers (Schubert et al. constrictions (not connected with conidiogenesis), mostly un-
2007, Zalar et al. 2007, Bensch et al. 2010, 2012). The branched, 20–100(–140) × 3.5–5(–6) μm, up to 6 μm wide at
most relevant differential morphological traits are the shape, the base, 1–6-septate, septa sometimes in short succession, not
width and complexity of conidiophores, the presence of constricted at septa, pale olivaceous or pale to medium oliva-
ramoconidia, and the formation and ornamentation of conidia. ceous brown, smooth, walls slightly thickened; micronematous
However, given the overlapping of these features, and the conidiophores shorter, narrower and paler than macronematous
need for standardisation using special culture media and ones, 15–30(–80) × 2–3 μm, 0–2-septate, subhyaline or pale
scanning electron microscopy procedures, the use of a mo- olivaceous. Conidiogenous cells integrated, terminal and inter-
lecular approach should be mandatory for correct identification calary, 8–24 μm long, short cylindrical or often irregular in outline
of the species in this complex fungal group (Sandoval-Denis due to lateral prolongations and shoulders and numerous con-
et al. 2016). idiogenous loci often crowded at or towards the apex, up to eight
Three different species complexes are recognised within the loci in terminal cells, 1–3 loci in intercalary cells, loci conspic-
genus, mainly based on morphology, and used for practical uous, subdenticulate, 1–2 μm diam. Ramoconidia commonly
purposes. The Cl. cladosporioides species complex is charac- formed, subcylindrical or irregular due to numerous loci at the
terised by mainly narrowly cylindrical or cylindrical-oblong, non- distal end, 15–33 × 3–4.5 μm, 0–1(–3)-septate, base broadly
nodulose, mostly non-geniculate conidiophores and conidia with truncate, 2.5(–3.5) μm wide. Conidia numerously formed,
a quite variable surface ornamentation ranging from smooth to especially small terminal and intercalary conidia, in branched
irregularly verrucose-rugose or rough-walled (reticulate or chains, branching in all directions with 1–3 conidia in the terminal
embossed stripes under SEM); the Cl. herbarum species unbranched part of the chain; terminal conidia very small, ovoid
complex includes species mainly having nodulose co- or obovoid, very pale, subhyaline or pale olivaceous brown,
nidiophores, with conidiogenesis confined to swellings, and 2.5–4.5 × 2–2.5(–3) μm (av. ± SD: 3.4 ± 0.6 × 2.2 ± 0.3), apex
verruculose, verrucose or echinulate conidia; and the Cl. rounded; intercalary conidia ovoid, limoniform, ellipsoid or
sphaerospermum complex is most remarkable due to forming irregular due to lateral outgrowths, 4–10.5 × (2–)3–3.5(–4) μm
numerous globose or subglobose terminal and intercalary con- (av. ± SD: 7.2 ± 2.0 × 3.1 ± 0.5), aseptate, with 1–4 distal hila;
idia with variable surface ornamentation and often poorly secondary ramoconidia ellipsoid, subcylindrical or irregular in
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MARIN-FELIX ET AL.
Fig. 21. Cladosporium chasmanthicola (ex-type CBS 142612). A–H. Conidiophores and conidial chains. Scale bars = 10 μm; C applies to C–G.
outline due to numerous hila crowded at or towards the distal on Chasmanthe aethiopica, 25 Sep. 2012, A.R. Wood (holotype
end, sometimes located on lateral shoulders or lateral pro- CBS H-23117, culture ex-type CBS 142612 = CPC 21300).
longations, those formed on micronematous conidiophores
shorter and narrower, (5–)8–23 × (2.5–)3–4.5 μm (av. ± SD: Note: Cladosporium chasmanthicola is closely related to Cl.
13.3 ± 5.4 × 3.5 ± 0.6), 0–1(–3)-septate, very pale olivaceous or acalyphae, but the latter species has much longer and narrower
pale olivaceous brown, smooth, walls unthickened, with (2–) conidiophores (150–430 × 3–4 μm) and smooth to loosely
3–6(–7) distal scars; hila conspicuous, 0.5–2 μm diam, verruculose, irregularly verruculose-rugose or rough-walled
darkened-refractive and somewhat thickened; conidia some- conidia (Bensch et al. 2010).
times germinating.
Cladosporium kenpeggii Bensch, U. Braun & Crous, sp. nov.
Culture characteristics: Colonies on PDA reaching 28–35 mm MycoBank MB819979. Fig. 22.
diam after 2 wk, olivaceous grey, grey olivaceous with several
smoke-grey patches of dense, felty aerial mycelium, reverse Etymology: Named after Dr Ken Pegg (Agri-Science and Bio-
leaden-grey to olivaceous grey, powdery, margin white, broad, security Queensland, Australia), the collector of the species, who
glabrous, colony centre somewhat folded and wrinkled, growth celebrates his 80th birthday this year.
flat. Colonies on MEA attaining 29–35 mm diam, whitish, smoke-
grey to pale olivaceous grey, reverse greyish sepia or olivaceous On SNA: Superficial mycelium sparingly formed, unbranched,
grey, velvety; margin glabrous, to somewhat feathery, radially occasionally branched, 2.5–3.5 μm wide, septate, without
furrowed, colony centre elevated, wrinkled and folded; aerial swellings and constrictions, pale olivaceous brown, almost
mycelium abundant, covering large parts of the colony surface, smooth to verruculose. Conidiophores macronematous, solitary,
dense, fluffy. Colonies on OA reaching 20–28 mm diam, oliva- arising mostly terminally, rarely laterally from hyphae, narrowly
ceous grey with patches of smoke-grey, grey olivaceous or cylindrical-oblong, usually unbranched, non-nodulose, some-
glaucous-grey towards margins, reverse leaden-grey to iron- times slightly geniculate towards the apex,
grey, fluffy-felty; margin glabrous, undulate, colony centre 15–100(–150) × 2.5–4 μm, 0–2(–5)-septate, pale to medium
somewhat elevated; aerial mycelium loose, diffuse to dense and olivaceous brown, smooth or minutely verruculose, walls
fluffy in a few spots. On all media without prominent exudates, unthickened or slightly thickened. Conidiogenous cells inte-
sporulation profuse. grated, mainly terminally, narrowly cylindrical-oblong, 16–60 μm
long, with (1–)2–3(–4) distal conidiogenous loci, crowded at or
Material examined: South Africa, Western Cape Province, Cape towards the apex, sometimes slightly geniculate due to sympo-
Town, Brackenfell, Bracken Nature Reserve, isol. from leaf spots dial proliferation, conidiogenous loci conspicuous, 1–2 μm diam,
136
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 22. Cladosporium kenpeggii (ex-type CBS 142613). A. Part of the colony on SNA. B–H. Conidiophores and conidial chains. Note the microcyclic conidiogenesis in C,
forming a secondary conidiophore at a still attached conidium with giving rise to secondary conidia and the germinating conidia in C and G. Scale bars = 10 μm; C applies to C,
D; E applies to E–G.
Fig. 23. Cladosporium welwitschiicola (ex-type CBS 142614). A–G. Conidiophores and conidial chains. H. Conidial chain. Scale bars = 10 μm; A applies to A–C; E applies to E, F.
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GENERA OF PHYTOPATHOGENIC FUNGI
thickened and darkened-refractive, sometimes cells germinating. and somewhat wider with a narrower base and intercalary conidia
Ramoconidia frequently formed, (17–)25–55 × 3–4(–5) μm, are shorter and narrower (Bensch et al. 2012).
0–1(–2)-septate, base broadly truncate, 2–4 μm wide, Cladosporium maracuja, described from Passiflora in Brazil in
unthickened, somewhat darkened-refractive. Conidia numerous, 1935, is morphologically quite similar in having smooth, catenate,
formed in branched chains, branching in all directions, up to eight 0–1-septate conidia and short conidiophores but since it is only
conidia in the terminal unbranched part of the chain; small ter- known from the type specimen it is kept separate. The conidia of
minal conidia obovoid or ellipsoid, 4.5–6 × (2–)2.5–3(–3.5) μm this species are shorter and wider and the conidiophores wider
(av. ± SD: 5.0 ± 0.5 × 2.7 ± 0.5), apex rounded; intercalary in vivo.
conidia ovoid or ellipsoid, 5.5–15 × (2–)2.5–3.5 μm (av. ± SD:
8.9 ± 3.2 × 3.0 ± 0.4), aseptate, with 1–2 distal hila, attenuated Cladosporium welwitschiicola Bensch, U. Braun & Crous, sp.
towards apex and base; secondary ramoconidia subcylindrical or nov. MycoBank MB819980. Fig. 23.
cylindrical, 14.5–35 × 3–4(–5) μm (av. ± SD:
22.4 ± 5.8 × 3.8 ± 0.6), 0–1(–2)-septate, with 2–3 distal hila, Etymology: Epithet composed of the name of the host genus,
pale olivaceous or pale olivaceous brown, smooth, walls slightly Welwitschia, and -cola, dweller.
thickened; hila conspicuous, subdenticulate, 1–2 μm diam,
somewhat thickened and darkened-refractive; microcyclic con- On SNA: Superficial mycelium abundantly formed, filiform to
idiogenesis occurring, conidia often germinating, often with more cylindrical-oblong, unbranched or loosely branched, (0.5–)
than one germination tube, tubes sometimes even branched, 1–4 μm wide, sometimes slightly swollen or constricted, septate,
filiform or irregular in outline. subhyaline, pale olivaceous or pale olivaceous brown, surface
ornamentation variable, smooth or almost so, asperulate, verru-
Culture characteristics: Colonies on PDA attaining 35–47 mm culose or sometimes even verrucose, walls unthickened, some-
diam after 2 wk, olivaceous to olivaceous grey, dull green towards times forming ropes of several hyphae. Conidiophores
margins, reverse iron-grey, greyish blue towards margins, pow- macronematous, solitary, erect, straight or slightly flexuous,
dery to fluffy, margin feathery, growth flat, aerial mycelium loose, terminally or laterally formed from hyphae, narrowly cylindrical-
diffuse, dense, fluffy and high in a few spots, pale olivaceous grey, oblong, non-nodulose, occasionally once geniculate towards the
sporulation profuse, without prominent exudates. Colonies in MEA apex due to sympodial proliferation, 25–90 × (2.5–)
reaching 39–48 mm diam, grey olivaceous, reverse iron-grey, 3–4.5(–5.5) μm, 0–3(–4)-septate, not constricted at septa, pale
velvety, margin white, broad, feathery, colony centre elevated, to medium olivaceous brown, smooth, sometimes verruculose or
wrinkled and folded, radially furrowed, aerial mycelium loose, irregularly rough-walled towards the base, walls thickened. Con-
diffuse to denser and fluffy, several small but prominent exudates idiogenous cells integrated, usually terminal, cylindrical,
formed, sporulation profuse. Colonies on OA grey olivaceous 12.5–42 μm long, with 2–4 conidiogenous loci crowded at the
when sporulating profusely, whitish or smoke-grey due to aerial apex, conspicuous, subdenticulate, 1–2 μm diam, somewhat
mycelium, reverse lead-grey or iron-grey, some parts with a cin- thickened and darkened-refractive. Ramoconidia not observed.
namon margin (both on top and reverse), powdery to fluffy-felty, Conidia catenate, in branched chains, branching in all directions,
aerial mycelium forming high strains, growth flat, without exudates. (1–)2–5(–6) conidia in the terminal unbranched part of the chain;
small terminal conidia obovoid, ellipsoid, 4–5 × 2.5–3.5 μm
Material examined: Australia, New South Wales, Upper Dungay, (av. ± SD: 4.6 ± 0.6 × 3.0 ± 0.4), rugulose, broadly rounded at the
28°150 S 153°210 E, isol. from leaves of Passiflora edulis, 20 apex; intercalary conidia ellipsoid, limoniform or fusiform, some-
Oct. 1999, K.G. Pegg & J. Dawes, FP 24737 (holotype BRIP times irregular in outline due to surface ornamentation, slightly to
26701a, isotype CBS H-23118, culture ex-type CBS distinctly attenuated towards apex and base, 5–11 × (2.5–)
142613 = CPC 19248 = BRIP 26701a). 3–3.5(–4) μm (av. ± SD: 7.4 ± 1.9 × 3.2 ± 0.4), 0–1-septate, with
1–3 distal hila, rugulose to distinctly rugose; secondary ramoco-
Notes: The smooth conidia formed in long branched chains and nidia ellipsoid or subcylindrical, often 3–4 formed at the apex of
the frequently formed ramoconidia remind one of Cl. cladospor- conidiophores, 8.5–21 × 3–4(–4.5) μm (av. ± SD:
ioides and Cl. iranicum. However, compared with Cl. cladospor- 14.6 ± 3.6 × 3.5 ± 0.4), 0–2(–3)-septate, mostly 1-septate,
ioides, Cl. kenpeggii possesses much shorter macronematous septum median or somewhat in the lower half, pale to medium
conidiophores, micronematous conidiophores are not formed and olivaceous brown or dingy brown, smooth or almost so to rugu-
the conidia are very often germinating and forming secondary lose, walls somewhat thickened; hila conspicuous, 0.5–2 μm
conidiophores. In Cl. iranicum the conidia also germinate quite diam; microcyclic conidiogenesis not occurring.
often, but the conidiophores are longer, ramoconidia are shorter
Fig. 24. Colletotrichum spp. A–AA. Asexual morphs. A–C. Conidiomata. A. Colletotrichum acutatum (ex-type CBS 112996). B. Colletotrichum destructivum (ex-type CBS
136228). C. Colletotrichum cymbidiicola (ex-type IMI 347923). D. Seta of Colletotrichum torulosum (ex-type CBS 128544). E. Tip of a seta of Colletotrichum gloeosporioides (ex-
type CBS 112999). F. Basis of a seta of Colletotrichum gloeosporioides (ex-type CBS 112999). G–K. Conidiogenous cells. G. Colletotrichum brasiliense (ex-type CBS 128501).
H. Colletotrichum scovillei (ex-type CBS 126529). I. Colletotrichum tofieldiae (CBS 495.85). J. Colletotrichum petchii (ex-type CBS 378.94). K. Colletotrichum gloeosporioides
(ex-type CBS 112999). L–R. Appressoria. L. Colletotrichum americae-borealis (CBS 136855). M. Colletotrichum graminicola (ex-epitype CBS 130836). N. Colletotrichum
gloeosporioides (ex-type CBS 112999). O. Colletotrichum laticiphilum (ex-type CBS 112989). P. Colletotrichum phormii (ex-type CBS 118194). Q. Colletotrichum liriopes (ex-type
CBS 119444). R. Colletotrichum truncatum (ex-type CBS 151.35). S–AA. Conidia of the ex-type strains of the name-giving species of nine Colletotrichum species complexes. S.
Colletotrichum dematium (ex-type CBS 125.25). T. Colletotrichum acutatum (ex-type CBS 112996). U. Colletotrichum truncatum (ex-type CBS 151.35). V. Colletotrichum
gloeosporioides (ex-type CBS 112999). W. Colletotrichum graminicola (ex-epitype CBS 130836). X. Colletotrichum boninense (ex-type CBS 123755). Y. Colletotrichum
destructivum (ex-type CBS 136228). Z. Colletotrichum orbiculare (ex-type CBS 570.97). AA. Colletotrichum gigasporum (ex-type CBS 133266). A–C, E–H, K. from Anthriscus
stem. D, I, J, L–AA. from SNA. Scale bars: A = 200 μm; B applies to B, C = 100 μm; G applies to D–AA = 10 μm. A–AA Pictures taken by U. Damm; A, H, O–P, T from Damm
et al. (2012b); B, L, Y from Damm et al. (2014); C, D, G, J, X from Damm et al. (2012a); I, Q–S, U from Damm et al. (2009); Z from Damm et al. (2013).
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GENERA OF PHYTOPATHOGENIC FUNGI
Culture characteristics: Colonies on PDA reaching up to 78 mm inamyloid, refractive ring at the apex. Ascospores uni- to
diam after 2 wk, olivaceous grey, fawn at margins, reverse biseriate, aseptate, hyaline, smooth-walled, cylindrical, oval,
mouse-grey, vinaceous-buff at margins, fluffy; margins feathery, fusiform or rhomboid, straight or curved, one end ± acute and
growth low convex. Colonies on MEA reaching up to 80 mm one end rounded or both ends rounded. Conidiomata acervular,
diam, smoke-grey, pale olivaceous grey to olivaceous grey, conidiophores and setae formed on cushions of pale to medium
reverse iron-grey, fluffy; margin feathery. Colonies on OA brown, roundish to angular cells, but very variable in culture,
reaching up to 72 mm diam, smoke-grey and pale olivaceous ranging from sporodochia-like aggregations of conidiophores
grey, reverse iron-grey, fluffy. On all three media aerial mycelium directly on hyphae to closed conidiomata that open by rupture.
abundantly formed covering large parts of the colony, loose to Setae may or may not be present, straight, pale to dark brown,
dense, high, fluffy; without prominent exudates, sporulation sometimes hyaline towards the tip, smooth-walled, verruculose
profuse. to verrucose, 1–8-septate, base cylindrical, conical or slightly
inflated, tip ± rounded to ± acute. Conidiophores hyaline to pale
Material examined: Namibia, isol. from dead leaf of Welwitschia brown, simple or septate, branched or unbranched, smooth-
mirabilis, 1 Oct. 2010, M.J. Wingfield (holotype CBS H-23119, walled, sometimes verruculose. Conidiogenous cells entero-
culture ex-type CBS 142614 = CPC 18648). blastic, hyaline to pale brown, smooth-walled, discrete, cylin-
drical, ellipsoidal, doliiform or ampulliform, collarette usually
Notes: With its rugulose or distinctly rugose conidia and rela- distinct, periclinal thickening visible to conspicuous, sometimes
tively short conidiophores, Cl. welwitschiicola reminds one of Cl. extending to form new conidiogenous loci (percurrent) or sur-
exasperatum and Cl. verrucocladosporioides, but the latter two rounded by a gelatinous coating. Conidia hyaline, smooth-
species differ in forming ramoconidia and in having longer and walled, aseptate, cylindrical, clavate, fusiform, sometimes
slightly wider small, intercalary and secondary ramoconidia. ellipsoidal to ovoid, straight or curved, apex rounded to acute,
Phylogenetically, it is closest to Cl. gamsianum and Cl. pseu- sometimes with a filiform appendage, base rounded to truncate,
docladosporioides, but these species are easily distinguishable sometimes with a prominent hilum. Appressoria single or in
in having smooth and narrower conidia (Bensch et al. 2012). small groups, pale to dark brown, with a globose, elliptical,
clavate, navicular or irregular outline and an entire, undulate or
Authors: K. Bensch, U. Braun, J.Z. Groenewald & P.W. Crous lobate edge.
Colletotrichum Corda, in Sturm, Deutschl. Fl., 3 Abt. (Pilze Culture characteristics: Colonies on PDA flat, with an entire to
Deutschl.) 3: 41, tab. 21. 1831. Figs 24, 25. irregular margin, grey to dark in centre, aerial mycelium, if pre-
Synonyms: Glomerella Spauld. & H. Schrenk, Science, N.Y. 17: sent, sparse to cottony, white, buff or pale olivaceous green in
751. 1903. colour. Reverse first white, with age turning grey to black,
For additional synonyms see Sutton (1980). olivaceous green or smoke-grey, concentric rings can be
observed. Conidia in mass orange, salmon, pink, white or pale
Classification: Sordariomycetes, Hypocreomycetidae, Glomer- grey. Colonies on SNA flat, with an entire, erose, dentate or
ellales, Glomerellaceae. undulate margin, aerial mycelium, if present, hyaline, white,
honey colour, iron-grey, greenish black or dark olivaceous.
Type species: Colletotrichum lineola Corda. Holotype: PRM Reverse hyaline, honey, pale olivaceous grey to iron-grey. Col-
155463. Epitype and ex-epitype culture: CBS H-20362, CBS onies on OA flat, with an entire to umbonate margin, aerial
125337. mycelium, if present, white, buff, rosy-buff, very pale glaucous,
hyaline or honey coloured. Reverse buff, rosy-buff, flesh, pale
DNA barcodes (genus): ITS. luteous, honey coloured, smoke-grey or olivaceous grey. Conidia
in mass salmon, saffron, orange, white or rosy-buff.
DNA barcodes (species): act, ApMat, apn2, cal, chs-1, gapdh,
gs, his3, sod2, tub2. Tables 6, 7. Fig. 26. Optimal media and cultivation conditions: For morphological
examinations of the asexual morphs SNA amended with double
Ascomata solitary or gregarious, globose to subglobose, dark autoclaved stems of Anthriscus sylvestris (wild chervil) and
brown to black, ostiole periphysate; ascomatal wall composed autoclaved filter paper placed onto the agar surface and incu-
of pale to medium brown flattened cells of textura angularis. bated under near-ultraviolet light with a 12 h photoperiod at
Hamathecium composed of hyaline, septate paraphyses, 20 °C for 10 d proved to be best suited to promote sporulation of
branched at the bases, rounded at the tips. Asci 8-spored, most of the species, while for other species, culturing on OA or
unitunicate, cylindrical to subfusoid, short pedicellate, with an PDA incubated under the same conditions is more suitable.
Fig. 25. A–F. Disease symptoms caused by Colletotrichum spp. A. Anthracnose on fruit of Cucurbita maxima cv. Red Hokkaido caused by Colletotrichum coccodes. B. Leaf
spot of red clover caused by Colletotrichum utrechtense. C. Anthracnose on bean hypocotyl caused by Colletotrichum lindemuthianum. D. Leaf spot of Paphiopedilum sp.
caused by Colletotrichum arxii. E. Anthracnose on strawberry fruit caused by Colletotrichum nymphaeae. F. Leaf spot of Mahonia aquifolium caused by Colletotrichum godetiae.
G–R. Sexual morphs of Colletotrichum spp. G, H. Ascomata. G. Colletotrichum petchii (ex-type CBS 378.94). H. Colletotrichum karstii (CBS 127597). I. Peridium in cross
section of Colletotrichum karstii (CBS 127597). J. Outer surface of peridium of Colletotrichum constrictum (ex-type CBS 128504). K–N. Ascospores. K. Colletotrichum salicis
(ex-type CBS 607.94). L. Colletotrichum constrictum (ex-type CBS 128504). M. Colletotrichum cymbidiicola (ex-type IMI 347923). N. Colletotrichum parsonsiae (ex-type CBS
128525). O–Q. Asci. O. Colletotrichum cymbidiicola (ex-type IMI 347923). P. Colletotrichum salicis (ex-type CBS 607.94). Q. Colletotrichum constrictum (ex-type CBS 128504).
R. Paraphyses of Colletotrichum salicis (ex-type CBS 607.94). G, K, M, O–R. from Anthriscus stem. H–J, L, N. from SNA. Scale bars: G = 100 μm; H = 50 μm; I applies to
I–R = 10 μm. A–R Pictures taken by U. Damm; E from Cannon et al. (2012); G–J, L–O, Q from Damm et al. (2012a); K, P, R from Damm et al. (2012b).
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Table 6. DNA barcodes of accepted Colletotrichum spp. except for species in the Col. graminicola and caudatum complexes.
Species Isolates1 GenBank accession numbers2 References
ITS gapdh chs-1 his3 act tub2 cal gs sod2 ApMat
ET AL.
Colletotrichum abscissum COAD 1877T KP843126 KP843129 KP843132 KP843138 KP843141 KP843135 – – – – Crous et al. (2015d)
Col. acerbum CBS 128530T JQ948459 JQ948790 JQ949120 JQ949450 JQ949780 JQ950110 – – – – Damm et al. (2012b)
Col. acutatum CBS 112996 T
JQ005776 JQ948677 JQ005797 JQ005818 JQ005839 JQ005860 – – – – Damm et al. (2012b)
Col. aenigma ICMP 18608T JX010244 JX010044 JX009774 – JX009443 JX010389 JX009683 JX010078 JX010311 KM360143 Weir et al. (2012)
Col. aeschynomenes ICMP 17673T JX010176 JX009930 JX009799 – JX009483 JX010392 JX009721 JX010081 JX010314 – Weir et al. (2012)
Col. agaves CBS 118190 DQ286221 – – – – – – – – – Farr et al. (2006)
Col. alatae ICMP 17919T JX010190 JX009990 JX009837 – JX009471 JX010383 JX009738 JX010065 JX010305 KC888932 Weir et al. (2012)
Col. alienum ICMP 12071 T
JX010251 JX010028 JX009882 – JX009572 JX010411 JX009654 JX010101 JX010333 KM360144 Weir et al. (2012)
Col. americae-borealis CBS 136232T KM105224 KM105579 KM105294 KM105364 KM105434 KM105504 – – – – Damm et al. (2014)
Col. annellatum CBS 129826 T
JQ005222 JQ005309 JQ005396 JQ005483 JQ005570 JQ005656 JQ005743 – – – Damm et al. (2012a)
Col. anthrisci CBS 125334T GU227845 GU228237 GU228335 GU228041 GU227943 GU228139 – – – – Damm et al. (2009)
Col. antirrhinicola CBS 102189 T
KM105180 KM105531 KM105250 KM105320 KM105390 KM105460 – – – – Damm et al. (2014)
Col. aotearoa ICMP 18537T JX010205 JX010005 JX009853 – JX009564 JX010420 JX009611 JX010113 JX010345 KC888930 Weir et al. (2012),
Sharma et al. (2015)
T
Col. aracearum CGMCC 3.14983 KX853167 KX893586 KX893578 KX893582 Hou et al. (2016)
Col. arxii CBS 132511 T
KF687716 KF687843 KF687780 KF687858 KF687802 KF687881 KF687819 KF687756 – – Liu et al. (2014)
Col. asianum ICMP 18580T FJ972612 JX010053 JX009867 – JX009584 JX010406 FJ917506 JX010096 JX010328 FR718814 Prihastuti et al. (2009),
Silva et al. (2012),
Weir et al. (2012)
Col. australe CBS 116478T JQ948455 JQ948786 JQ949116 JQ949446 JQ949776 JQ950106 – – – – Damm et al. (2012b)
Col. beeveri CBS 128527T JQ005171 JQ005258 JQ005345 JQ005432 JQ005519 JQ005605 JQ005692 – – – Damm et al. (2012a)
Col. bidentis COAD 1020T KF178481 KF178506 KF178530 KF178554 KF178578 KF178602 – KF178627 – – Damm et al. (2013)
Col. bletillum CGMCC 3.15117T JX625178 KC843506 – – KC843542 JX625207 – – – – Tao et al. (2013)
Col. boninense CBS 123755T JQ005153 JQ005240 JQ005327 JQ005414 JQ005501 JQ005588 JQ005674 – – – Damm et al. (2012a)
Col. brasiliense CBS 128501T JQ005235 JQ005322 JQ005409 JQ005496 JQ005583 JQ005669 JQ005756 – – – Damm et al. (2012a)
Col. brassicola CBS 101059 T
JQ005172 JQ005259 JQ005346 JQ005433 JQ005520 JQ005606 JQ005693 – – – Damm et al. (2012a)
Col. brevisporum BCC 38876T JN050238 JN050227 KF687760 – JN050216 JN050244 – – – – Noireung et al. (2012)
Col. brisbanense CBS 292.67 T
JQ948291 JQ948621 JQ948952 JQ949282 JQ949612 JQ949942 – – – – Damm et al. (2012b)
Col. bryoniicola CBS 109849T KM105181 KM105532 KM105251 KM105321 KM105391 KM105461 – – – – Damm et al. (2014)
Col. cairnsense BRIP 63642 T
KU923672 KU923704 KU923710 KU923722 KU923716 KU923688 – – – – De Silva et al. (2017)
Col. camelliae CGMCC 3.14925T KJ955081 KJ954782 – – KJ954363 KJ955230 KJ954634 KJ954932 – KJ954497 Liu et al. (2015b)
T
Col. camelliae-japonicae CGMCC3.18118 KX853165 KX893584 KX893576 KX893580 Hou et al. (2016)
Col. carthami SAPA100011T AB696998 – – – – AB696992 – – – – Damm et al. (2012b),
Uematsu et al. (2012)
Col. changpingense MFLUCC 15-0022 KP683152 KP852469 KP852449 – KP683093 KP852490 – – – – Jayawardena et al. (2016a)
Col. chlorophyti IMI 103806 T
GU227894 GU228286 GU228384 GU228090 GU227992 GU228188 – – – – Damm et al. (2009)
Col. chrysanthemi SAPA100010 AB696999 AB696993 – – – – Uematsu et al. (2012),
Damm et al. (2012b)
www.studiesinmycology.org
Col. circinans CBS 221.81T GU227855 GU228247 GU228345 GU228051 GU227953 GU228149 – – – – Damm et al. (2009)
Col. citri CBS 134233 T
KC293581 KC293741 – – KC293621 KC293661 KC293701 KC293781 – – Huang et al. (2013)
Col. citricola CBS 134228T KC293576 KC293736 KC293792 – KC293616 KC293656 KC293696 KC293776 – – Huang et al. (2013)
Col. clidemiae ICMP 18658 T
JX010265 JX009989 JX009877 – JX009537 JX010438 JX009645 JX010129 JX010356 KC888929 Weir et al. (2012)
Col. cliviae CBS 125375T GQ485607 GQ856756 GQ856722 JX560963 GQ856777 GQ849440 – – – – Yang et al. (2009),
Cannon et al. (2012)
Col. coccodes CBS 369.75T HM171679 HM171673 JX546681 JX546779 HM171667 JX546873 – – – – Liu et al. (2011, 2013a)
Col. colombiense CBS 129818 T
JQ005174 JQ005261 JQ005348 JQ005435 JQ005522 JQ005608 JQ005695 – – – Damm et al. (2012a)
Col. conoides CGMCC 3.17615T KP890168 KP890162 KP890156 KP890144 KP890174 KP890150 Diao et al. (2017)
Col. constrictum CBS 128504 T
JQ005238 JQ005325 JQ005412 JQ005499 JQ005586 JQ005672 JQ005759 – – – Damm et al. (2012a)
Col. cordylinicola ICMP 18579T JX010226 JX009975 JX009864 – HM470235 JX010440 HM470238 JX010122 JX010361 JQ899274 Weir et al. (2012)
Col. cosmi CBS 853.73 T
JQ948274 JQ948604 JQ948935 JQ949265 JQ949595 JQ949925 – – – – Damm et al. (2012b)
Col. costaricense CBS 330.75T JQ948180 JQ948510 JQ948841 JQ949171 JQ949501 JQ949831 – – – – Damm et al. (2012b)
Col. curcumae IMI 288937 T
GU227893 GU228285 GU228383 GU228089 GU227991 GU228187 – – – – Damm et al. (2009)
Col. cuscutae IMI 304802T JQ948195 JQ948525 JQ948856 JQ949186 JQ949516 JQ949846 – – – – Damm et al. (2012b)
Col. cymbidiicola IMI 347923 T
JQ005166 JQ005253 JQ005340 JQ005427 JQ005514 JQ005600 JQ005687 – – – Damm et al. (2012a)
Col. dacrycarpi CBS 130241T JQ005236 JQ005323 JQ005410 JQ005497 JQ005584 JQ005670 JQ005757 – – – Damm et al. (2012a)
Col. dematium CBS 125.25 T
GU227819 GU228211 GU228309 GU228015 GU227917 GU228113 – – – – Damm et al. (2009)
Col. destructivum CBS 136228T KM105207 KM105561 KM105277 KM105347 KM105417 KM105487 – – – – Damm et al. (2014)
Col. dracaenophilum CBS 118199 T
DQ286209, JX546707 JX519230 JX546756 JX519238 JX519247 – – – – Cannon et al. (2012),
JX519222 Farr et al. (2006)
Col. endophytica MFLUCC 13–0418T KC633854 KC832854 – – KF306258 – KC810018 – – – Manamgoda et al. (2013)
Col. euphorbiae CBS 134725T KF777146 KF777131 KF777128 KF777134 KF777125 KF777247 – – – – Crous et al. (2013b)
Col. excelsum-altitudum CGMCC 3.15130 T
HM751815 KC843502 – – KC843548 JX625211 – – – – Tao et al. (2013)
Col. fioriniae CBS 128517T JQ948292 JQ948622 JQ948953 JQ949283 JQ949613 JQ949943 – – – – Damm et al. (2012b)
GENERA
Col. fructi CBS 346.37 T
GU227844 GU228236 GU228334 GU228040 GU227942 GU228138 – – – – Damm et al. (2009)
Col. fructicola ICMP 18581T JX010165 JX010033 JX009866 – FJ907426 JX010405 FJ917508 JX010095 JX010327 JQ807838 Weir et al. (2012)
OF PHYTOPATHOGENIC FUNGI
Col. fructivorum CBS 133125 T
JX145145 – – – – JX145196 – – – JX145300 Doyle et al. (2013)
Col. fuscum CBS 133701T KM105174 KM105524 KM105244 KM105314 KM105384 KM105454 – – – – Damm et al. (2014)
Col. fusiforme MFLUCC 12–0437T KT290266 KT290255 KT290253 – KT290251 KT290256 – – – – Ariyawansa et al. (2015a)
Col. gigasporum CBS 133266 T
AM982797, KF687715 KF687822 KF687761 KF687844 – FN557442, KF687866 – – – – Rakotoniriana et al. (2013),
Liu et al. (2014)
143
MARIN-FELIX
Table 6. (Continued).
Species Isolates1 GenBank accession numbers2 References
ITS gapdh chs-1 his3 act tub2 cal gs sod2 ApMat
ET AL.
Col. gloeosporioides CBS 112999T JQ005152 JQ005239 JQ005326 JQ005413 JQ005500 JQ005587 JQ005673 JX010085 JX010365 JQ807843 Weir et al. (2012)
Col. godetiae CBS 133.44T JQ948402 JQ948733 JQ949063 JQ949393 JQ949723 JQ950053 – – – – Damm et al. (2012b)
Col. grevilleae CBS 132879 T
KC297078 KC297010 KC296987 KC297056 KC296941 KC297102 KC296963 KC297033 – – Liu et al. (2013b)
Col. grossum CGMCC3.17614T KP890165 KP890159 KP890153 KP890141 KP890171 KP890147 Diao et al. (2017)
Col. guajavae IMI 350839T JQ948270 JQ948600 JQ948931 JQ949261 JQ949591 JQ949921 – – – – Damm et al. (2012b)
Col. guizhouensis CGMCC 3.15112T JX625158 KC843507 – – KC843536 JX625185 – – – – Tao et al. (2013)
Col. hebeiense MFLUCC13–0726T KF156863 KF377495 KF289008 – KF377532 KF288975 – – – – Yan et al. (2015)
Col. hemerocallidis CBS 130642T JQ400005 JQ400012 JQ399998 – JQ399991 JQ400019 KJ781319 – – – Yang et al. (2012)
Col. henanense CGMCC 3.17354 T
KJ955109 KJ954810 – – KM023257 KJ955257 KJ954662 KJ954960 – KJ954524 Liu et al. (2015b)
Col. higginsianum IMI 349061T KM105184 KM105535 KM105254 KM105324 KM105394 KM105464 – – – – Damm et al. (2014)
Col. hippeastri CBS 125376T JQ005231 JQ005318 JQ005405 JQ005492 JQ005579 JQ005665 JQ005752 – – – Damm et al. (2012a)
Col. horii ICMP 10492T GQ329690 GQ329681 JX009752 – JX009438 JX010450 JX009604 JX010137 JX010370 JQ807840 Weir et al. (2012)
Col. hsienjenchang MAFF 243051 AB738855 – AB738846 AB738847 AB738845 – – – – – Sato et al. (2012)
Col. hymenocallidicola MFLUCC 12–0531T KT290264 KT290263 KT290262 – KT290260 KT290261 – – – – Ariyawansa et al. (2015a)
Col. incanum ATCC 64682T KC110789 KC110807 – KC110798 KC110825 KC110816 – – – – Yang et al. (2014)
Col. indonesiense CBS 127551T JQ948288 JQ948618 JQ948949 JQ949279 JQ949609 JQ949939 – – – – Damm et al. (2012b)
T
Col. insertae MFLU 15–1895 KX618686 KX618684 KX618683 KX618682 KX618685 Hyde et al. (2016)
Col. jiangxiense CGMCC 3.17363T KJ955201 KJ954902 – – KJ954471 KJ955348 KJ954752 KJ955051 – KJ954607 Liu et al. (2015b)
Col. johnstonii CBS 128532 T
JQ948444 JQ948775 JQ949105 JQ949435 JQ949765 JQ950095 – – – – Damm et al. (2012b)
Col. kahawae subsp. kahawae ICMP 17816T JX010231 JX010012 JX009813 – JX009452 JX010444 JX009642 JX010130 JX010350 JQ894579 Weir et al. (2012)
T
Col. kahawae subsp. ciggaro ICMP 18539 JX010230 JX009966 JX009800 JX009523 JX010434 JX009635 JX010132 JX010346 Weir et al. (2012)
Col. karstii CBS 132134T HM585409 HM585391 HM582023 HM581995 HM585428 HM582013 – – – Yang et al. (2009)
Col. kinghornii CBS 198.35T JQ948454 JQ948785 JQ949115 JQ949445 JQ949775 JQ950105 – – – – Damm et al. (2012b)
Col. lacticiphilum CBS 112989T JQ948289 JQ948619 JQ948950 JQ949280 JQ949610 JQ949940 – – – – Damm et al. (2012b)
Col. ledebouriae CBS 141284T KX228254 – – KX228365 KX228357 – – – – – Crous et al. (2016c)
Col. lentis CBS 127604T JQ005766 KM105597 JQ005787 JQ005808 JQ005829 JQ005850 – – – – Damm et al. (2014)
Col. liaoningense CGMCC3.17616T KP890104 KP890135 KP890127 KP890097 KP890111 KP890119 Diao et al. (2017)
Col. lilii CBS 109214 GU227810 GU228202 GU228300 GU228006 GU227908 GU228104 – – – – Damm et al. (2009)
Col. limetticola CBS 114.14T JQ948193 JQ948523 JQ948854 JQ949184 JQ949514 JQ949844 – – – – Damm et al. (2012b)
Col. lindemuthianum CBS 144.31 T
JQ005779 JX546712 JQ005800 JQ005821 JQ005842 JQ005863 – KF178643 – – Damm et al. (2013),
Liu et al. (2013a)
Col. lineola CBS 125337T GU227829 GU228221 GU228319 GU228025 GU227927 GU228123 – – – – Damm et al. (2009)
Col. lini CBS 172.51T JQ005765 KM105581 JQ005786 JQ005807 JQ005828 JQ005849 – – – – Damm et al. (2014)
Col. liriopes CBS 119444 T
GU227804 GU228196 GU228294 GU228000 GU227902 GU228098 – – – – Damm et al. (2009)
Col. lupini CBS 109225T JQ948155 JQ948485 JQ948816 JQ949146 JQ949476 JQ949806 – – – – Damm et al. (2012b)
Col. magnisporum CBS 398.84 T
KF687718 KF687842 KF687782 KF687865 KF687803 KF687882 – KF687742 – – Liu et al. (2014)
www.studiesinmycology.org
Col. malvarum CBS 521.97T KF178480 KF178504 KF178529 KF178553 KF178577 KF178601 – KF178626 – – Damm et al. (2013)
Col. melonis CBS 159.84 T
JQ948194 JQ948524 JQ948855 JQ949185 JQ949515 JQ949845 – – – – Damm et al. (2012b)
Col. menispermi MFLU 14–0625HT KU242357 KU242356 KU242355 – KU242353 KU242354 – – – – Li et al. (2016)
Col. metake MAFF 244029 AB738859 (Sequences available at http://www.gene.affrc.go.jp/databases-micro_search_en.php) Sato et al. (2012)
Col. musae ICMP 19119T JX010146 JX010050 JX009896 – JX009433 HQ596280 JX009742 JX010103 JX010335 KC888926 Weir et al. (2012)
Col. neosansevieriae CBS 139918 T
KR476747 KR476791 – KR476792 KR476790 KR476797 – – – – Crous et al. (2015d)
Col. nigrum CBS 169.49T JX546838 JX546742 JX546693 JX546791 JX546646 JX546885 – – – – Liu et al. (2013a)
Col. novae-zelandiae CBS 128505 T
JQ005228 JQ005315 JQ005402 JQ005489 JQ005576 JQ005662 JQ005749 – – – Damm et al. (2012a)
Col. nupharicola ICMP 18187T JX010187 JX009972 JX009835 – JX009437 JX010398 JX009663 JX010088 JX010320 JX145319 Weir et al. (2012),
Doyle et al. (2013)
Col. nymphaeae CBS 515.78T JQ948197 JQ948527 JQ948858 JQ949188 JQ949518 JQ949848 – – – – Damm et al. (2012b)
Col. ocimi CBS 298.94 T
KM105222 KM105577 KM105292 KM105362 KM105432 KM105502 – – – – Damm et al. (2014)
Col. oncidii CBS 129828T JQ005169 JQ005256 JQ005343 JQ005430 JQ005517 JQ005603 JQ005690 – – – Damm et al. (2012a)
Col. orbiculare CBS 570.97T KF178466 KF178490 KF178515 KF178539 KF178563 KF178587 – KF178611 – – Damm et al. (2013)
Col. orchidophilum CBS 632.80T JQ948151 JQ948481 JQ948812 JQ949142 JQ949472 JQ949802 – – – – Damm et al. (2012b)
Col. panacicola C08048 GU935867 GU935847 – – GU944757 – – GU935807 – – Choi et al. (2011)
Col. paranaense CBS 134729T KC204992 KC205026 KC205043 KC205004 KC205077 KC205060 – – – – Bragança et al. (2016)
Col. parsonsiae CBS 128525 T
JQ005233 JQ005320 JQ005407 JQ005494 JQ005581 JQ005667 JQ005754 – – – Damm et al. (2012a)
Col. paxtonii IMI 165753T JQ948285 JQ948615 JQ948946 JQ949276 JQ949606 JQ949936 – – – – Damm et al. (2012b)
Col. petchii CBS 378.94 T
JQ005223 JQ005310 JQ005397 JQ005484 JQ005571 JQ005657 JQ005744 – – – Damm et al. (2012a)
Col. phormii CBS 118194T JQ948446 JQ948777 JQ949107 JQ949437 JQ949767 JQ950097 – – – – Damm et al. (2012b)
Col. phyllanthi CBS 175.67 T
JQ005221 JQ005308 JQ005395 JQ005482 JQ005569 JQ005655 JQ005742 – – – Damm et al. (2012a)
Col. pisicola CBS 724.97T KM105172 KM105522 KM105242 KM105312 KM105382 KM105452 – – – – Damm et al. (2014)
Col. proteae CBS 132882 T
KC297079 KC297009 KC296986 KC297045 KC296940 KC297101 KC296960 – KC297032 – Liu et al. (2013b)
GENERA
Col. pseudoacutatum CBS 436.77T JQ948480 JQ948811 JQ949141 JQ949471 JQ949801 JQ950131 – – – – Damm et al. (2012b)
Col. pseudomajus CBS 571.88 T
KF687722 KF687826 KF687779 KF687864 KF687801 KF687883 KF687807 KF687744 – – Liu et al. (2014)
OF PHYTOPATHOGENIC FUNGI
Col. psidii ICMP 19120 JX010219 JX009967 JX009901 – JX009515 JX010443 JX009743 JX010133 JX010366 KC888931 Weir et al. (2012)
Col. pyricola CBS 128531T JQ948445 JQ948776 JQ949106 JQ949436 JQ949766 JQ950096 – – – – Damm et al. (2012b)
Col. queenslandicum ICMP 1778T JX010276 JX009934 JX009899 – JX009447 JX010414 JX009691 JX010104 JX010336 KC888928 Weir et al. (2012)
Col. quinquefoliae MFLU 14–0626HT KU236391 KU236390 – – KU236389 KU236392 – – – – Li et al. (2016)
Col. radicis CBS 529.93T KF687719 KF687825 KF687762 KF687847 KF687785 KF687869 KF687806 KF687743 – – Liu et al. (2014)
(continued on next page)
145
146
MARIN-FELIX
Table 6. (Continued).
Species Isolates1 GenBank accession numbers2 References
ITS gapdh chs-1 his3 act tub2 cal gs sod2 ApMat
ET AL.
Col. rhexiae CBS 133134T JX145128 – – – JX145179 – – – JX145290 Doyle et al. (2013)
Col. rhombiforme CBS 129953T JQ948457 JQ948788 JQ949118 JQ949448 JQ949778 JQ950108 – – – – Damm et al. (2012b)
Col. riograndense ICMP 20083T KM655299 KM655298 KM655297 – KM655295 KM655300 KM655296 – – – Macedo et al. (2016)
Col. rusci CBS 119206T GU227818 GU228210 GU228308 GU228014 GU227916 GU228112 – – – – Damm et al. (2009)
Col. salicis CBS 607.94 T
JQ948460 JQ948791 JQ949121 JQ949451 JQ949781 JQ950111 – – – – Damm et al. (2012b)
Col. salsolae ICMP 19051T JX010242 JX009916 JX009863 – JX009562 JX010403 JX009696 JX010093 JX010325 KC888925 Weir et al. (2012)
T
Col. sansevieriae MAFF 239721 AB212991 (Sequences available at http://www.gene.affrc.go.jp/databases-micro_search_en.php) Nakamura
et al. (2006)
Col. scovillei CBS 126529T JQ948267 JQ948597 JQ948928 JQ949258 JQ949588 JQ949918 – – – – Damm et al. (2012b)
Col. sedi MFLUCC 14–1002T KM974758; KM974755 KM974754 – KM974756 KM974757 – – – – Liu et al. (2015c)
Col. siamense ICMP 18578T JX010171 JX009924 JX009865 – FJ907423 JX010404 FJ917505 JX010094 JX010326 JQ899289 Phoulivong et al. (2009),
Weir et al. (2012)
Col. sidae CBS 504.97T KF178472 KF178497 KF178521 KF178545 KF178569 KF178593 – KF178618 – – Damm et al. (2013)
Col. simmondsii CBS 122122T JQ948276 JQ948606 JQ948937 JQ949267 JQ949597 JQ949927 FJ917510 FJ972591 – – Damm et al. (2012b),
Prihastuti et al. (2009)
Col. sloanei IMI 364297T JQ948287 JQ948617 JQ948948 JQ949278 JQ949608 JQ949938 – – – – Damm et al. (2012b)
Col. spaethianum CBS 167.49 T
GU227807 GU228199 GU228297 GU228003 GU227905 GU228101 – – – – Damm et al. (2009)
Col. spinaceae CBS 128.57 GU227847 GU228239 GU228337 GU228043 GU227945 GU228141 – – – – Damm et al. (2009)
Col. spinosum CBS 515.97T KF178474 KF178498 KF178523 KF178547 KF178571 KF178595 – KF178620 – – Damm et al. (2013)
T
Col. sydowii CBS 135819 KY263783 KY263785 KY263787 KY263789 KY263791 KY263793 Present study
Col. syzygicola MFLUCC 10–0624T KF242094 KF242156 – – KF157801 KF254880 KF254859 KF242125 – – Udayanga et al. (2013)
Col. tabacum CPC 18945T KM105204 KM105557 KM105274 KM105344 KM105414 KM105484 – – – – Damm et al. (2014)
Col. tamarilloi CBS 129814T JQ948184 JQ948514 JQ948845 JQ949175 JQ949505 JQ949835 – – – – Damm et al. (2012b)
Col. tanaceti CBS 132693T JX218228 JX218243 JX259268 – JX218238 JX218233 – – – – Barimani et al. (2013),
Damm et al. (2014)
Col. tebeestii CBS 522.97T KF178473 KF178505 KF178522 KF178546 KF178570 KF178594 – KF178619 – – Damm et al. (2013)
Col. temperatum CBS 133122T JX145159 – – – – JX145211 – – – JX145298 Doyle et al. (2013)
Col. theobromicola ICMP 18649 T
JX010294 JX010006 JX009869 – JX009444 JX010447 JX009591 JX010139 JX010372 KC790726 Weir et al. (2012)
Col. ti ICMP 4832T JX010269 JX009952 JX009898 – JX009520 JX010442 JX009649 JX010123 JX010362 KM360146 Weir et al. (2012),
Liu et al. (2015b)
Col. tofieldiae CBS 495.85 GU227801 GU228193 GU228291 GU227997 GU227899 GU228095 – – – – Damm et al. (2009)
Col. torulosum CBS 128544 T
JQ005164 JQ005251 JQ005338 JQ005425 JQ005512 JQ005512 JQ005512 – – – Damm et al. (2012a)
Col. trichellum CBS 217.64 GU227812 GU228204 GU228302 GU228009 GU227910 GU228106 – – – – Damm et al. (2009)
Col. trifolii CBS 158.83T KF178478 KF178502 KF178527 KF178551 KF178575 KF178599 – KF178624 – – Damm et al. (2014)
Col. tropicale ICMP 18653 T
JX010264 JX010007 JX009870 – JX009489 JX010407 JX009719 JX010097 JX010329 KC790728 Rojas et al. (2010),
Weir et al. (2012)
Col. tropicicola BCC 38877T JN050240 JN050229 – – JN050218 JN050246 – – – – Noireung et al. (2012)
www.studiesinmycology.org
Col. truncatum CBS 151.35T GU227862 GU228254 GU228352 GU228058 GU227960 GU228156 – – – – Damm et al. (2009)
Col. utrechtense CBS 130243 T
KM105201 KM105554 KM105271 KM105341 KM105411 KM105481 – – – – Damm et al. (2014)
Col. verruculosum IMI 45525T GU227806 GU228198 GU228296 GU228002 GU227904 GU228100 – – – – Damm et al. (2009)
Col. vietnamense CBS 125478 T
KF687721 KF687832 KF687769 KF687855 KF687792 KF687877 KF687816 KF687753 – – Liu et al. (2014)
Col. vignae CBS 501.97T KM105183 KM105534 KM105253 KM105323 KM105393 KM105463 – – – – Damm et al. (2014)
Col. viniferum GZAAS 5.08601T JN412804 JN412798 – – JN412795 JN412813 JQ309639 JN412787 – – Peng et al. (2013),
Hyde et al. (2014)
Col. walleri CBS 125472T JQ948275 JQ948605 JQ948936 JQ949266 JQ949596 JQ949926 – – – – Damm et al. (2012b)
Col. wuxiense CGMCC 3.17894T KU251591 KU252045 KU251939 – KU251672 KU252200 KU251833 KU252101 – KU251722 Wang et al. (2016)
Col. xanthorrhoeae ICMP 17903 T
JX010261 JX009927 JX009823 – JX009478 JX010448 JX009653 JX010138 JX010369 KC790689 Shivas et al. (1998),
Weir et al. (2012)
Col. yunnanense CBS 132135T EF369490, JX546706 JX519231 JX546755 JX519239 JX519248 – – – – Liu et al. (2007),
JX546804 Cannon et al. (2012)
1
ATCC: American Type Culture Collection, Virginia, USA; BCC: BIOTEC Culture Collection, National Center for Genetic Engineering and Biotechnology (BIOTEC), Khlong Luang, Pathumthani, Thailand; BRIP: Queensland Plant Pathology Herbarium,
Brisbane, Australia; CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands; CGMCC: Chinese General Microbiological Culture Collection Center, Beijing, China; COAD: Coleç~ao Octavio Almeida Drummond, Universidade Ferderal de
Viçosa, Viçosa, Brazil; CPC: Culture collection of Pedro Crous, housed at Westerdijk Fungal Biodiversity Institute; GZAAS: Guizhou Academy of Agricultural Sciences, Guizhou Province, China. ICMP: International Collection of Micro-organisms from
Plants, Landcare Research, Private Bag 92170, Auckland, New Zealand; IMI: International Mycological Institute, Kew, UK; MAFF: Ministry of Agriculture, Forestry and Fisheries, Tsukuba, Ibaraki, Japan; MFLU: Herbarium of Mae Fah Luang University,
Chiang Rai, Thailand; MFLUCC: Mae Fah Luang University Culture Collection, Chiang Ria, Thailand. HT and T indicate holotype specimens and ex-type strains, respectively.
2
ITS: internal transcribed spacers and intervening 5.8S nrDNA; gapdh: partial glyceraldehyde-3-phosphate dehydrogenase gene; chs-1: partial chitin synthase-1 gene; his: partial histone H3 gene; act: partial actin gene; tub2: partial beta-tubulin gene;
cal: partial calmodulin gene; gs: partial glutamine synthetase gene; sod2: partial manganese superoxide dismutase gene; ApMat: partial Apn2-Mat1-2 intergenic spacer and partial mating type (Mat1-2) gene.
GENERA
OF PHYTOPATHOGENIC FUNGI
147
148
MARIN-FELIX
Table 7. DNA barcodes of accepted Colletotrichum spp. in the Col. graminicola and caudatum complexes.
Species Isolates1 GenBank accession numbers2 References
ITS gapdh chs-1 his3 act tub2 apn2 ApMat sod2
ET AL.
Colletotrichum alcorni IMI 176619T
EU554079, JX076858 – – – – – EU364987 FJ377901 EU554187 Crouch et al. (2009c), Crouch (2014)
Col. baltimorense BPI 892771 T
JX076866 – – – – – JX076927 JX076905 JX076886 Crouch (2014)
Col. caudasporum CGMCC 3.15106T JX625162 KC843512 – – KC843526 JX625190 – – – Tao et al. (2013)
Col. caudatum BPI 423339 LT
JX076915 – – – – – – – JX076878 Crouch (2014)
CBS 131602ET JX076860 – – – – – JX076932 JX076893 JX076878 Crouch (2014)
Col. cereale CBS 129663 DQ126177, JQ005774 – JQ005795 JQ005816 JQ005837 JQ005858 – – DQ133277 Crouch et al. (2006), O'Connell et al. (2012)
Col. duyunensis CGMCC 3.15105T JX625160 KC843515 – – KC843530 JX625187 – – – Tao et al. (2013)
Col. echinochloae MAFF 511473 T
AB439811 – – – – – – – AB440153 Moriwaki & Tsukiboshi (2009),
Col. eleusines MAFF 511155T EU554131, JX519218 – JX519226 – JX519234 JX519243 EU365038 – EU554234 Cannon et al. (2012), Crouch et al. (2009b, c),
Col. endophytum CGMCC 3.15108T JX625177 KC843521 – – KC843533 JX625206 – – – Tao et al. (2013)
Col. eremochloae CBS 129661T JQ478447, JX519220 – JX519228 – JX519236 JX519245 JQ478476 JQ478462 JQ478449 Cannon et al. (2012),
Crouch & Tomaso-Peterson (2012)
Col. falcatum CBS 147945T HM171877, JQ005772 HM171677, JQ005814 JQ005835 JQ005856 HM569770 HM569769 – Prihastuti et al. (2010), O'Connell et al. (2012)
JQ005793
Col. graminicola CBS 130836T DQ003110, JQ005767 – JQ005788 HQ005809 JQ005830 JQ005851 – FJ377994 – Crouch et al. (2009a, c), Du et al. (2005),
O'Connell et al. (2012)
Col. hanaui MAFF 3054042T EU554101, JX519217 – JX519225 – – JX519242 EU365008 FJ377922 EU554205 Crouch et al. (2009b, c), Cannon et al. (2012)
Col. jacksonii MAFF 305460 T
EU554108, JX519216 – JX519224 – JX519233 JX519241 – – EU554212 Crouch et al. (2009b, c), Cannon et al. (2012)
Col. miscanthi MAFF 510857T EU554121, JX519221 – JX519229 – JX519237 JX519246 EU365028 – EU554224 Crouch et al. (2009b, c), Cannon et al. (2012)
Col. navitas CBS 125086 T
GQ919067, JQ005769 – JQ005790 JQ005811 JQ005832 JQ005853 GQ919069 GQ919071 GQ919073 Crouch et al. (2009a), O'Connell et al. (2012)
Col. nicholsonii MAFF 511115T EU554126, JQ005770 – JQ005791 JQ005812 JQ005833 JQ005854 EU365033 FJ377946 EU554229 Crouch et al. (2009b, c), O'Connell et al. (2012)
Col. ochracea CGMCC 3.15104 T
JX625168 KC843513 – – KC843527 JX625183 – – – Tao et al. (2013)
Col. paspali MAFF 305403T EU554100, JX519219 – JX519227 – JX519235 JX519244 EU365007 FJ377921 EU554204 Crouch et al. (2009b, c), Cannon et al. (2012)
Col. somersetense CBS 131599T JX076862 – – – – – JX076918 JX076895 JX076880 Crouch (2014)
Col. sublineola CBS 131301 T
DQ003114, JQ005771 – JQ005792 JQ005813 JQ005834 JQ005855 EU365121 FJ378029 DO132051 Crouch et al. (2006),
Crouch & Tomaso-Peterson (2012),
O'Connell et al. (2012)
Col. zoysia MAFF 238573T JX076871 – – – – – JX076922 JX076899 – Crouch (2014)
1
BPI: US National Fungus Collections, Beltsville, Maryland, USA; CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands; CGMCC: Chinese General Microbiological Culture Collection Center, Beijing, China; IMI: International
Mycological Institute, Kew, UK; MAFF: Ministry of Agriculture, Forestry and Fisheries, Tsukuba, Ibaraki, Japan. LT, ET and T indicate lectotype specimen and ex-epitype and ex- type strains, respectively.
2
ITS: internal transcribed spacers and intervening 5.8S nrDNA; gapdh: partial glyceraldehyde-3-phosphate dehydrogenase gene; chs-1: partial chitin synthase-1 gene; his: partial histone H3 gene; act: partial actin gene; tub2: partial beta-tubulin gene;
apn2: partial DNA lyase gene; ApMat: partial Apn2-Mat1-2 intergenic spacer and partial mating type (Mat1-2) gene; sod2: partial manganese superoxide dismutase gene.
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 26. One of the 100 equally most parsimonious trees obtained from a heuristic search of the combined ITS, gapdh, chs-1, act and tub2 sequence data of the currently accepted
species of Colletotrichum. Parsimony and likelihood bootstrap support values 50 % are indicated at the nodes and branches with Bayesian posterior probabilities above 0.80 given
in bold. The tree is rooted with Monilochaetes infuscans CBS 869.96. GenBank accession numbers are listed in Tables 6 and 7. The ex-type strains are in bold. TreeBASE: S21045.
Plates sometimes need to be incubated for 1–2 mo to allow flowers or fruits. Additionally, crown and stem rots, ripe rot,
development of the sexual morph. seedling blights and brown blotch are caused by species of
this genus.
Distribution: Worldwide.
Notes: Due to the overlapping morphological characters, species
Hosts: Occurs on a wide range of plant families. delimitation based on morphology alone is hardly possible in
Colletotrichum. Multilocus sequence analyses combined with a
Disease symptoms: Anthracnose disease symptoms include polyphasic approach, including the analysis of geographical,
defined, often sunken necrotic spots on leaves, stems, ecological and morphological data, is generally suggested for
www.studiesinmycology.org 149
MARIN-FELIX ET AL.
species differentiation within the genus Colletotrichum (Cai et al. differentiation within the Col. gloeosporioides species complex
2009). This approach resulted in the differentiation of almost 200 (Weir et al. 2012) (Table 6). In contrast, Crouch et al. (2009b) and
species, most of them belonging to species complexes. Due to Crouch (2014) applied ITS, sod2, apn2 and Mat1/apn2 (=
simultaneous studies in the genus by different researchers, the ApMat), to study the Col. graminicola and Col. caudatum species
sets of loci used for differentiating species vary among the complexes (Table 7). Silva et al. (2012) and Sharma et al. (2015)
different species complexes. ITS, gapdh, chs-1, act, his3 and emphasised the use of ApMat in Colletotrichum species delimi-
tub2 (with some also gs or cal) gene regions have been used for tation because of its high resolution within the Col. gloeospor-
studying species within the Col. acutatum, boninense, dematium, ioides species complex compared to previously used loci. Liu
destructivum, gigasporum, orbiculare, spaethianum and trunca- et al. (2015b, 2016) applied different sets of loci and different
tum species complexes (Cannon et al. 2012, Damm et al. 2012a, phylogenetic methods on a large set of closely related Colleto-
b, 2013, 2014, Liu et al. 2014, Jayawardena et al. 2016b), while trichum strains/species belonging to this complex and revealed
gs, cal and sod2 were additionally applied for the species that ApMat should be combined with other loci to achieve
150
GENERA OF PHYTOPATHOGENIC FUNGI
0.1
Fig. 26. (continued).
satisfactory species delimitation in the Col. gloeosporioides mycologists on the locus or loci to use for species identification/
complex. barcoding. For example, most species in the Col. acutatum
Because different sets of loci are used in different species complex can be separated by tub2 sequences (Damm et al.
complexes and the resolution of species differs depending on 2012b), while species in the Col. gloeosporioides complex can
both locus and species, there is no agreement among the be identified with a combination of ApMat and gs sequences (Liu
www.studiesinmycology.org 151
MARIN-FELIX ET AL.
et al. 2015b). Research to select better genetic markers and the masses in the centre, reverse primrose, rosy-buff to grey
best secondary barcoding gene(s) is still ongoing. olivaceous, growth 26–28 mm diam in 1 wk ( 40 mm in
10 d). Conidia in mass saffron to salmon.
References: Cannon et al. 2012 (species complexes); Crouch
et al. 2009b, Crouch 2014 (phylogeny); Damm et al. 2009, Material examined: Taiwan, from leaves of Sambucus sp., 18
2012a, b, 2013, 2014, Weir et al. 2012, Liu et al. 2014 Dec. 2011, P.W. Crous (holotype CBS H-21509, culture ex-
(morphology, phylogeny). type CBS 135819 = CPC 20071); ibid., CBS 132889 = CPC
20070.
Colletotrichum sydowii Damm, sp. nov. MycoBank
MB820688. Fig. 27. Notes: Colletotrichum sydowii is to date only known from Sam-
bucus leaves in Taiwan. The conidia of this species resemble
Etymology: The species epithet is derived from Hans Sydow those of several species, e.g. Col. clidemiae, Col. australe and
(1879–1946), a German mycologist who described several Col. parsonsiae belonging to the Col. gloeosporioides, acutatum
Colletotrichum species including one on Sambucus, host from and boninense species complexes (Damm et al. 2012a, b, Weir
which this fungus was isolated. et al. 2012). Based on DNA sequences, Col. sydowii does not
belong to any known Colletotrichum species complex; the closest
Sexual morph not observed. Asexual morph on SNA: Vegetative matches in blastn searches of the ex-holotype strain in GenBank
hyphae 1.5–9.5 μm diam, hyaline to pale brown, smooth-walled, with sequences of the different loci resulted in sequences of
septate, branched. Chlamydospores not observed. Conidiomata strains from different species complexes. The ITS sequence is
absent, conidiophores and setae formed directly on hyphae. 99 % (1–2 nucleotide difference) identical to those of “Col.
Setae medium brown, smooth-walled, upper part verrucose, gloeosporioides” strain EECC-453 from Ensete ventricosum
60–115 μm long, 2–4-septate, base cylindrical, 4–6 μm diam, (GenBank KP942898, from an unpublished study in Ethiopia by
tip ± acute to ± rounded. Conidiophores hyaline to pale brown, Y. Mulugeta et al.) and “Fungal sp.” strain TCPR 106 from a
smooth-walled to verrucose, septate, branched, to 50 μm long. photosynthetic root of Tinospora cordifolia in India (GenBank
Conidiogenous cells hyaline to pale brown, smooth-walled to JX951175, R.N. Kharwar et al., unpubl. data), as well as
verrucose, cylindrical to clavate, 13–28 × 4–5 μm, with a 93–94 % identical to the ITS sequences of several species of the
gelatinous coating, opening 1–2 μm diam, collarette 0.5 μm Col. gigasporum and gloeosporioides complexes and Col.
long, periclinal thickening visible. Conidia hyaline, smooth- coccodes. The tub2 sequence is 83 % (> 130 nucleotides dif-
walled, aseptate, straight, slightly clavate to cylindrical, with ference) identical to those of Col. vietnamense strain CBS
one end round and the other truncate, (17–) 125477 (GenBank KF687876), Col. gigasporum strain CBS
17.5–19.5(–21) × 5–5.5 μm, mean ± SD = 18.3 ± 0.9 × 5.2 ± 109355 (GenBank KF687870), both belonging to the Col. giga-
0.2 μm, L/W ratio = 3.5. Appressoria single, medium brown, sporum complex (Liu et al. 2014), and Col. dracaenophilum
smooth-walled, subglobose, elliptical or irregular in outline, with a isolate DMM 170 (GenBank KJ653227, Macedo & Barreto 2016).
strongly lobate margin, (7.5–)9–14(–17.5) × (5.5–) The his3 sequence is 90–91 % identical with species from
7–10.5(–12) μm, mean ± SD = 11.4 ± 2.4 × 8.6 ± 1.8 μm, L/W different complexes, including Col. constrictum strain CBS
ratio = 1.3, appressoria of strain CBS 132889 shorter, measuring 128503 (GenBank JQ005498, Col. boninense complex, Damm
(7.5–)8.5–12.5(–14) × (6.5–)7.5–11(–13) μm, mean ± SD = et al. 2012a) and Col. vietnamense strain CBS 125477 (Gen-
10.6 ± 1.9 × 9.1 ± 1.8 μm, L/W ratio = 1.2. Asexual morph on Bank KF687854, Col. gigasporum complex, Liu et al. 2014) as
Anthriscus stem: Conidiomata, conidiophores and setae formed well as Col. yunnanense strain CBS 132135 (GenBank
on pale brown, angular cells, 3.5–8 μm diam. Setae medium JX546755, Liu et al. 2014). The chs-1 sequence is 89–91 %
brown, verruculose to verrucose, 30–80 μm long, (1–)2–3- identical with e.g. Col. dacrycarpi strain CBS 130241 (GenBank
septate, base conical to ± inflated, 4.5–7.5 μm diam, JQ005410, Col. boninense complex, Damm et al. 2012a) and
tip ± acute to ± rounded. Conidiophores pale brown, smooth- Col. grevilleae strain CBS 132879 (GenBank KC296987, Col.
walled, septate, branched, to 20 μm long. Conidiogenous cells gloeosporioides complex, Liu et al. 2013b). Closest match with
pale brown, smooth-walled, cylindrical to doliiform, the act sequence is Col. magnisporum strain CBS 398.84 with
6.5–18 × 5–6.5 μm, opening 1.5–2 μm diam, collarette 82 % identity (GenBank KF687803, Col. gigasporum complex,
0.5–1 μm long, periclinal thickening distinct. Conidia hyaline, Liu et al. 2014). There is no species with more than 52 % query
smooth-walled, aseptate, straight, cylindrical, with one end round cover to the gapdh of Col. sydowii.
and the other truncate, (14–)15.5–18.5(–20.5) × 5–6 μm, There is one Colletotrichum species that was previously
mean ± SD = 17.0 ± 1.6 × 5.5 ± 0.3 μm, L/W ratio = 3.1, conidia described from Sambucus, Col. sambuci Syd. 1942, that
of strain CBS 132889 larger, measuring (15.5–) caused fruit anthracnose of Sa. nigra in Germany. Sydow
17–20(–20.5) × (4.5–)5–5.5(–6) μm, mean ± SD = 18.6 (1942) regarded Gloeosporium fructigenum f. sambuci Müll.-
± 1.4 × 5.4 ± 0.3 μm, L/W ratio = 3.5. Thurg. 1922, described from Sa. nigra in Switzerland, as a
synonym of Col. sambuci. Conidia of Col. sambuci are cy-
Culture characteristics: Colonies on SNA flat with entire lindrical, elongate ellipsoidal to clavate with one end rounded
margin, hyaline to honey, filter paper and Anthriscus stem tapering to the other slightly acute end, measuring
partly pale to dark grey, agar medium partly covered with short 13–20 × 4.5–6 μm. They have similar dimensions as those of
felty whitish aerial mycelium, reverse similar; growth Col. sydowii, however it is unlikely that the fungus collected
27.5–29.5 mm diam in 1 wk ( 40 mm diam in 10 d). Col- from Sambucus leaves in Taiwan is identical with the fruit
onies on OA flat with entire margin; olivaceous buff to greenish anthracnose pathogen of black elderberry in Europe, as the
olivaceous, partly covered with short felty whitish aerial morphological characters apply to many Colletotrichum spe-
mycelium and grey conidiomata, saffron to salmon conidial cies and all molecular data suggest a species in the
152
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 27. Colletotrichum sydowii (holotype CBS 135819). A–B. Conidiomata. C. Tip of seta. D. Base of seta. E–F. Conidiophores. G. Tip of seta. H. Base of seta. I–K.
Conidiophores. L–P. Appressoria. Q–R. Conidia. A, C–F, Q. from Anthriscus stem. B, G–P, R. from SNA. A–B. DM; C–R. DIC. Scale bars: A applies to A, B = 100 μm; E
applies to C–R = 10 μm.
Col. acutatum species complex. Based on ITS sequences, Another species was described from Sambucus in Canada,
Benduhn et al. (2011) and Michel et al. (2013) identified Col. Vermicularia sambucina (Ellis & Dearness 1897), which how-
acutatum (s. lat.) as causal agent of the fruit anthracnose of ever has curved conidia with different dimensions
Sa. nigra in Germany and Switzerland, respectively. As part of (24 × 3–3.5 μm, Saccardo & Sydow 1899). In contrast, Col.
the multilocus alignment of the Col. acutatum complex, Col. fructicola, a species with considerably shorter conidia belonging
godetiae was identified from fruits of Sa. nigra in the to the Col. gloeosporioides complex, was isolated from leaves
Netherlands (Damm et al. 2012b). The ITS sequences of “Col. with anthracnose leaf spot symptoms on Sa. ebulus in Iran
cf. gloeosporioides” strain BBA 67435 (GenBank AJ301931) (Arzanlou et al. 2015).
from Sa. nigra in Germany and of strain BBA 71332 (Gen-
Bank AJ301972) also from Sambucus (Nirenberg et al. 2002) Authors: U. Damm, R.S. Jayawardena, L. Cai
are identical with that of strain CBS 862.70; these isolates are
probably also Col. godetiae. Conidia of the Col. godetiae Coniella Höhn. Ber. Deutsch. Bot. Ges. 36: 316. 1918. Fig. 28.
strain from the Netherlands (CBS 862.70) measure (8–) Synonyms: Schizoparme Shear, Mycologia 15: 120. 1923.
14–19(–24) × (4–)4.5–5(–5.5) μm on SNA. The shape of Baeumleria Petr. & Syd., Repert. Spec. Nov. Regni Veg. Beih.
this species can be either fusiform or clavate with only one 42: 268. 1927.
acute end, depending on the strain (Damm et al. 2012b) and Pilidiella Petr. & Syd., Repert. Spec. Nov. Regni Veg. Beih. 42:
there were no setae observed. Strain BBA 67435 also had 462. 1927.
conidia pointed only at one end (Nirenberg et al. 2002), which Anthasthoopa Subram. & K. Ramakr., Proc. Indian Acad. Sci.,
agrees with the shape of Col. sambuci. It is possible that Col. Sect. B 43: 173. 1956.
sambuci is an older name of Col. godetiae, however, we Cyclodomella Mathur et al., Sydowia 13: 144. 1959.
cannot confirm this here as we could not locate the type Embolidium Bat., Broteria, N.S. 33(3–4): 194. 1964 non Sacc.
material. 1978.
www.studiesinmycology.org 153
MARIN-FELIX ET AL.
Fig. 28. Coniella spp. A–D. Disease symptoms. A, B. Coniella eucalyptorum on Eucalyptus sp. C. Coniella tibouchinae on Tibouchina granulosa. D. Coniella granati on Punica
granatum (pictures taken by M. Mirabolfathy). E–I. Sexual morph of Coniella eucalyptigena (ex-type CBS 139893). E. Ascomata forming on OA. F. Ostiolar area. G, H. Asci. I.
Ascospores. J–R. Asexual morphs. J. Conidiomata forming on OA of Coniella diplodiella (ex-epitype CBS 111858). K. Transverse section through a conidioma of Coniella
eucalyptorum (ex-type CBS 112640). L, M. Conidiogenous cells giving rise to conidia. L. Coniella diplodiopsis (ex-type CBS 590.84). M. Coniella obovata (CBS 111025). N–R.
Conidia. N. Coniella africana (ex-type CBS 114133). O. Coniella diplodiella (ex-epitype CBS 111858). P. Coniella fusiformis (ex-type CBS 141596). Q. Coniella limoniformis (ex-
type CBS 111021). R. Coniella obovata (CBS 111025). Scale bars: E = 250 μm, others = 10 μm. Pictures taken from Alvarez et al. (2016).
154
GENERA OF PHYTOPATHOGENIC FUNGI
Classification: Sordariomycetes, Sordariomycetidae, Dia- were synonymised under Coniella because the type species of
porthales, Schizoparmaceae. the three genera clustered in a single well-supported clade in
a phylogenetic analysis based on four different loci (LSU, ITS,
Type species: Coniella fragariae (Oudem.) B. Sutton (syn. rpb2 and tef1) (Alvarez et al. 2016). Coniella and Pilidiella
Coniella pulchella Höhn.). Neotype and ex-neotype culture: CBS were initially distinguished by von Arx (1981) based on their
H-10697, CBS 172.49 = CPC 3930. conidial pigmentation, being hyaline to pale brown in Pilidiella
and dark brown in Coniella. However, Alvarez et al. (2016)
DNA barcodes (genus): LSU, rpb2. demonstrated that conidial colour evolved multiple times
throughout the clade representing Coniella, and therefore
DNA barcodes (species): ITS, rpb2, tef1. Table 8. rejected it as a character for generic delimitation in Schizo-
parmaceae. Sutton (1980) and Nag Raj (1993) also consid-
Ascomata brown to black, collapsed collabent, erumpent, ered Coniella and Pilidiella synonymous since both genera
becoming superficial, globose, papillate, with central periphysate presented identical conidiomata, conidiogenesis and orienta-
ostiole. Paraphyses lacking. Asci clavate to subcylindrical, with tion of conidiophores. However, Castlebury et al. (2002)
distinct apical ring, free at maturity. Ascospores ellipsoid, asep- demonstrated a separation of both genera in a phylogenetic
tate, hyaline, at times becoming pale brown at maturity, smooth, study based on LSU sequences. This was further supported
with or without mucoid caps. Conidiomata pycnidial, immersed to by van Niekerk et al. (2004b) based on their LSU, ITS and
semi-immersed, unilocular, glabrous, ostiolate; ostiole central, tef1 sequence data. Based on these molecular studies,
circular or oval, often situated in a conical or rostrate neck; together with the difference in conidial pigmentation reported
conidiomatal wall brown to dark brown or black, composed of by von Arx (1981), Wijayawardene et al. (2016) regarded
thin, pale brown textura angularis on exterior, and hyaline, thin- Coniella and Pilidiella as two separate genera in a recent
walled, textura prismatica in the inner layers except at base, study of dematiaceous coelomycetes. By adding more loci and
which has a convex, pulvinate tissue of hyaline textura angularis expanding the number of isolates studied, Alvarez et al.
giving rise to conidiophores or conidiogenous cells. Co- (2016) resolved the conflict that lasted a few decades
nidiophores mostly reduced to conidiogenous cells, occasionally regarding the classification of these genera.
septate and branched at base, invested in mucus. Con-
idiogenous cells discrete, cylindrical, subcylindrical, obclavate or References: Van Niekerk et al. 2004b, Crous et al. 2014a,
lageniform, hyaline, smooth-walled, proliferating percurrently, Alvarez et al. 2016 (morphology and phylogeny).
with visible periclinal thickening. Conidia ellipsoid, fusiform,
globose, napiform or naviculate with a truncate base and an Coniella duckerae H.Y. Yip, Trans. Brit. Mycol. Soc. 89: 587.
obtuse to apiculate apex, unicellular, thin- or thick-walled, 1987. Fig. 29.
smooth, hyaline, pale yellowish, pale yellowish brown, or oliva-
ceous brown to brown, sometimes with a longitudinal germ-slit, Description and illustration: Yip (1987).
with or without a mucoid appendage extending from apex to
base on one side; basal hila with or without a short tubular basal Material examined: Australia, Victoria, Wilson's Promontory,
appendage. Spermatophores formed in same conidioma, hya- Five Mile Road, on rhizosphere of Lepidospermum concavum,
line, smooth, 1-septate with several apical conidiogenous cells, unknown collector and date (holotype DAR 55703, isotype
or reduced to conidiogenous cells. Spermatogenous cells hya- VPRI 13689, culture ex-type VPRI 13689 = CBS 142045).
line, smooth, lageniform to subcylindrical, with visible periclinal
thickening. Spermatia hyaline, smooth, rod-shaped with rounded Notes: Coniella duckerae was excluded from the study of Alvarez
ends (adapted from Crous et al. 2014a). et al. (2016), as no ex-type culture was available. However, the
original culture was recently revived, and DNA barcodes could
Culture characteristics: On PDA produces white aerial mycelium thus be generated for inclusion in this study.
with or without black conidiomata. On OA frequently produces
white aerial mycelium with black conidiomata, but sometimes Coniella hibisci (B. Sutton) Crous, comb. nov. MycoBank
with luteous to orange zones. MB820811. Fig. 30.
Basionym: Coniella musaiaensis var. hibisci B. Sutton, The
Optimal media and cultivation conditions: On 2 % MEA, PDA and Coelomycetes (Kew): 420. 1980.
OA, at 25 °C under continuous near-ultraviolet light to promote
sporulation. Plant pathogenic. Conidiomata separate, immersed or superfi-
cial, globose to depressed, initially appearing hyaline, becoming
Distribution: Worldwide. olivaceous to black with age, with plate-like structures, up to
350 μm diam; ostiole central, 40–80 μm diam; conidiomatal wall
Hosts: Wide variety of hosts, e.g. Eucalyptus (Myrtaceae), Fragaria consisting of 2–4 layers of medium brown textura angularis.
(Rosaceae), Hibiscus (Malvaceae), Psidium (Myrtaceae), Punica Conidiophores densely aggregated, slightly thicker, subulate,
(Lythraceae), Terminalia (Combretaceae) and Vitis (Vitaceae). simple, frequently branched above, reduced to conidiogenous
cells, or with 1–2 supporting cells, 25–35 × 3–5 μm. Con-
Disease symptoms: Foliar, fruit, stem and root lesions, white rot idiogenous cells simple, hyaline, smooth, tapering,
and crown rot. 8–15 × 2.5–3 μm, 1.5–2 μm wide at apex, surrounded by a
gelatinous coating, with visible periclinal thickening. Conidia
Notes: In the most recent revision of the members of Schiz- hyaline to pale yellowish brown with age, fusoid to ellipsoidal,
oparmaceae, Pilidiella and its sexual morph Schizoparme inequilateral, apex acutely rounded, widest at middle tapering to
www.studiesinmycology.org 155
MARIN-FELIX ET AL.
slightly truncate base, smooth-walled, mono- to multiguttulate, Notes: The morphology of the present African ex-epitype strain
germ slits absent, (10–)11–13(–15) × (3–)3.5–4(–5) μm from Hibiscus sp. (CBS 109757 = ARS 3534) compares well with
(L/W = 3.4), with a mucoid appendage alongside conidium. that of the holotype of Coniella musaiaensis var. hibisci, which
was described from Hibiscus esculentus collected in Nigeria. A
Culture characteristics: Colonies on MEA surface dirty white, with new combination is therefore proposed, elevating it to species
prolific black conidial masses spreading from centre. On OA and rank. Presently there are still no cultures available of Con.
PDA surface dirty white with profuse black conidiomata and musaiaensis, and further collections from Bauhinia reticulata
sparse aerial mycelium. (Sierra Leone) need to be made to resolve its phylogeny. Con-
iella hibisci is also morphologically similar to Con. javanica (on
Material examined: Africa, from Hibiscus sp., unknown date, A.R. Hibiscus sabdariffa, Indonesia), although they are phylogeneti-
Rossman (epitype designated here BPI 748426, MBT376042, cally divergent (Alvarez et al. 2016).
culture ex-epitype CBS 109757 = ARS 3534). Nigeria, on leaves
of Hibiscus esculentus, 25 Jul. 1967, Arny (holotype IMI 129200). Authors: Y. Marin-Felix, J. Edwards, A.Y. Rossman & P.W. Crous
156
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 29. Coniella duckerae (ex-type CBS 142045). A. Conidiomata forming on OA. B, C. Conidiogenous cells giving rise to conidia. D. Conidia. Scale bars: A = 350 μm,
others = 10 μm.
Fig. 30. Coniella hibisci (ex-epitype CBS 109757). A. Conidiomata forming on OA. B, C. Conidiogenous cells giving rise to conidia. D. Conidia. Scale bars: A = 350 μm,
others = 10 μm.
Curvularia Boedijn, Bull. Jard. Bot. Buitenzorg, 3 Ser. 13: 123. with a sub-conical, conical, paraboloid or cylindrical neck;
1933. Fig. 31. ascomatal wall comprising pseudoparenchymatous cells of equal
Synonyms: Malustela Bat. & J.A. Lima, Publ. Inst. Micol. Recife thickness or slightly thickened at apex of the ascoma. Hama-
263: 5. 1960. thecium comprising septate, filiform, branched pseudopar-
Curvusporium Corbetta as “Curvosporium”, Riso 12: 28, 30. aphyses. Asci bitunicate, clavate, cylindrical-clavate or broadly
1963. fusoid, straight or slightly curved, thin-walled, fissitunicate, often
Pseudocochliobolus Tsuda, et al., Mycologia 69: 1117. 1978. becoming more or less distended prior to dehiscence, short
pedicellate, rounded at the apex. Ascospores multiseriate, fili-
Classification: Dothideomycetes, Pleosporomycetidae, Pleo- form or flagelliform, hyaline or sometimes pale yellow or pale
sporales, Pleosporaceae. brown at maturity, septate, helically coiled within ascus, degree
of ascospore coiling moderate to very strongly coiled, often with
Type species: Curvularia lunata (Wakker) Boedijn. Ex-neotype a mucilaginous sheath. Conidiophores straight to flexuous, often
culture: CBS 730.96. geniculate, multiseptate, usually simple, sometimes branched,
smooth to verruculose, macronematous, mononematous,
DNA barcodes (genus): LSU, ITS. sometimes nodose, cylindrical. Conidiogenous nodes cylindrical,
integrated, terminal and intercalary, proliferating sympodially,
DNA barcodes (species): ITS, gapdh, tef1. Table 9. Fig. 32. cicatrised. Conidia solitary, often curved, acropleurogenous,
broadly fusoid, elliptical, obovoid or obpyriform, mostly smooth,
Ascomata pseudothecial, mostly globose to ellipsoidal, some- sometimes verruculose, echinulate or tuberculate, 3 or more
times flask-shaped or flattened on hard substrata, brown or distoseptate, with or without an unequally swollen cell which is
black, immersed, erumpent, partially embedded or superficial, more pigmented than the other cells, septa sometimes accen-
free or developing on a basal columnar or flat stroma, smooth or tuated with a dark band in some or all the cells, germinating
covered with vegetative filaments; ostiole central, papillate or mainly from one or both polar cells with the basal germ tube
www.studiesinmycology.org 157
MARIN-FELIX ET AL.
Fig. 31. Curvularia spp. A–F. Conidiophores and conidia. A. Curvularia geniculata. B. Curvularia neergaardii (CBS 277.91). C. Curvularia portulacea (ex-isotype BRIP 14541).
D. Curvularia tropicalis (ex-isotype BRIP 14834). E. Curvularia hominis (ex-type CBS 136985). F. Curvularia muehlenbeckiae (ex-type CBS 144.63). G–I. Conidia. G. Curvularia
crustacea (ex-epitype BRIP 13524). H. Curvularia nicotiae (ex-isotype BRIP 11983). I. Curvularia pseudolunata (ex-type CBS 136987). J. Germinating conidium of Curvularia
neergaardii (CBS 277.91). K, L. Microconidiation. K. Curvularia americana (ex-type CBS 136983). L. Curvularia chlamydospora (ex-type CBS 136984). M. Chlamydospores of
Curvularia pseudolunata (ex-type CBS 136987). Scale bars: A = 50 μm; the others = 10 μm. Picture A taken from Samson et al. (2010); C, D, G, H from Tan et al. (2014); E, F, I,
K–M from Madrid et al. (2014).
growing semiaxially, hilum in a slightly protruding truncate basal convex with papillate surface, margin lobate, undulate, entire or
section of the conidial wall and often visible as two dark lenticular sometimes rhizoid.
spots in optical section arranged close together with a small
obscure narrow separating canal between them or distinctly Optimal media and cultivation conditions: Sterilised Zea mays
protuberant, first conidial septum median or submedian, second leaves placed on 1.5 % WA or slide cultures of half-strength PDA
septum often delimiting the basal cell of the mature conidium, under near-ultraviolet light (12 h light, 12 h dark) to induce
third septum then distal. Microconidiation not common, produc- sporulation of the asexual morph, while for the sexual morph
ing conidia 1–2-celled, pale brown, globose to subglobose Sach's agar with sterilised rice or wheat straw at 25 °C is used.
(adapted from Sivanesan 1987).
Distribution: Worldwide.
Culture characteristics: Colonies on PDA white or pale grey
when young, orange to brown or different shades of grey (mainly Hosts: Wide host range, occurring as pathogens or saprobes.
dark olivaceous grey) when mature, fluffy, cottony, raised or Mainly found on members of the Poaceae, being pathogens of
158
GENERA OF PHYTOPATHOGENIC FUNGI
www.studiesinmycology.org 159
MARIN-FELIX ET AL.
Table 9. (Continued).
Species Isolates1 GenBank accession numbers2 References
ITS gapdh tef1
Cu. pallescens CBS 156.35T KJ922380 KM083606 KM196570 Manamgoda et al. (2015)
Cu. perotidis CBS 350.90T JN192385 KJ415394 JN601021 Manamgoda et al. (2015)
T
Cu. pisi CBS 190.48 KY905678 KY905690 KY905697 Present study
Cu. portulacae CBS 239.48IsoT = BRIP 14541 KJ415553 KJ415393 KJ415440 Tan et al. (2014)
T
Cu. prasadii CBS 143.64 KJ922373 KM061785 KM230408 Manamgoda et al. (2014)
Cu. protuberata CBS 376.65IsoT KJ922376 KM083605 KM196576 Manamgoda et al. (2014)
Cu. pseudolunata UTHSC 09-2092 T
HE861842 HF565459 – da Cunha et al. (2013)
Cu. pseudorobusta UTHSC 08-3458 HE861838 HF565476 – da Cunha et al. (2013)
T
Cu. ravenelii BRIP 13165 JN192386 JN600978 JN601024 Manamgoda et al. (2012b)
Cu. richardiae BRIP 4371IsoLT KJ415555 KJ415391 KJ415438 Tan et al. (2014)
Cu. robusta CBS 624.68IsoT KJ909783 KM083613 KM196577 Manamgoda et al. (2014)
T
Cu. ryleyi BRIP 12554 KJ415556 KJ415390 KJ415437 Tan et al. (2014)
Cu. senegalensis CBS 149.71 HG779001 HG779128 – Madrid et al. (2014)
Cu. sesuvi Bp-Zj 01 EF175940 – – Zhang & Li (2009)
Cu. soli CBS 222.96T KY905679 KY905691 KY905698 Present study
Cu. sorghina BRIP 15900IsoT KJ415558 KJ415388 KJ415435 Tan et al. (2014)
Cu. spicifera CBS 274.52 JN192387 JN600979 JN601023 Manamgoda et al. (2012b)
T
Cu. subpapendorfii CBS 656.74 KJ909777 KM061791 KM196585 Manamgoda et al. (2015)
Cu. trifolii CBS 173.55 HG779023 HG779124 – Madrid et al. (2014)
T
Cu. tripogonis BRIP 12375 JN192388 JN600980 JN601025 Manamgoda et al. (2011)
Cu. tropicalis BRIP 14834IsoT KJ415559 KJ415387 KJ415434 Tan et al. (2014)
PT
Cu. tsudae ATCC 44764 KC424596 KC747745 KC503940 Deng et al. (2014)
Cu. tuberculata CBS 146.63IsoT JX256433 JX276445 JX266599 Manamgoda et al. (2012b)
Cu. uncinata CBS 221.52 T
HG779024 HG779134 – Madrid et al. (2014)
Cu. verruciformis CBS 537.75 HG779026 HG779133 HG779211 Madrid et al. (2014)
Cu. verruculosa CBS 150.63 KP400652 KP645346 KP735695 Manamgoda et al. (2015)
1
ATCC: American Type Culture Collection, Virginia, USA; BRIP: Queensland Plant Pathology Herbarium, Brisbane, Australia; Bp-Zj: Isolate housed in Biotechnology
Institute, Zhejiang University, Hangzhou, China; CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands; DAOM: Plant Research Institute, Department of
Agriculture (Mycology), Ottawa, Canada; MFLUCC: Mae Fah Luang University Culture Collection, Chiang Ria, Thailand, UTHSC: Fungus Testing Laboratory, Department
of Pathology at the University of Texas Health Science Center, San Antonio, Texas, USA. ET, IsoT, IsoLT, PT, SynT and T indicate ex-epitype, ex-isotype, ex-isolectotype, ex-
paratype, ex-syntype and ex-type strains, respectively.
2
ITS: internal transcribed spacers and intervening 5.8S nrDNA; gapdh: partial glyceraldehyde-3-phosphate dehydrogenase gene; tef1: partial translation elongation factor
1-alpha gene.
grass and staple crops, including rice, maize, wheat and sor- Curvularia is a rich genus in host range and geographic dis-
ghum. This genus also occurs on genera belonging to Actini- tribution compared to Bipolaris. Apart from phytopathogenic
diaceae, Aizoaceae, Caricaceae, Convolvulaceae, Fabaceae, species, this genus comprises species that are pathogens of
Iridaceae, Lamiaceae, Lythraceae, Oleaceae, Polygonaceae and humans and other animals, causing respiratory tract, cutaneous,
Rubiaceae. cerebral and corneal infections, mainly in immunocompromised
patients (Carter & Boudreaux 2004). Some species can be found
Disease symptoms: Leaf spots, leaf blight, melting out, root rot, in association with both humans and plants, such as Cu. hawai-
foot rot, among others. iensis, Cu. lunata and Cu. spicifera (Manamgoda et al. 2015).
Notes: Species delimitation in Curvularia based on morphology References: Sivanesan 1987 (morphology and pathogenicity);
only is difficult due to the morphological complexity within this Manamgoda et al. 2011 (pathogenicity), Manamgoda et al. 2015
genus, as also observed in Bipolaris. Furthermore, the differ- (morphology, pathogenicity and phylogeny).
entiation of both genera based on morphology alone is some-
times complicated (see Bipolaris notes for morphological Curvularia pisi Y. Marín & Crous, sp. nov. MycoBank
differences between Bipolaris and Curvularia). Therefore, mo- MB820814. Fig. 33.
lecular data are essential for an accurate identification of species
within these genera, ITS, gapdh and tef1 being the loci selected Etymology: Name refers to the host genus from which it was
for this purpose (Manamgoda et al. 2014, 2015). isolated, Pisum.
160
GENERA OF PHYTOPATHOGENIC FUNGI
Hyphae hyaline to pale brown, branched, septate, thin-walled, 3–4(–5)-distoseptate, (13.5–)18–28 × 7.5–11 μm; hila pro-
1.5–5 μm. Conidiophores arising in groups, septate, straight or tuberant, flat, darkened, thickened, 1.3–3.5 μm. Chlamydo-
flexuous, geniculate at upper part, verruculose, tapering towards spores, microconidiation and sexual morph not observed.
apex, sometimes branched, cells walls thicker than those of
vegetative hyphae, mononematous, semi- to macronematous, Culture characteristics: Colonies on PDA reaching 75–79 mm
pale brown to brown, paler towards apex, not swollen at the diam after 1 wk, velvety to slightly powdery; surface and reverse
base, (35–)50–210 × 2.5–5 μm. Conidiogenous cells verrucu- grey olivaceous to olivaceous black.
lose, terminal or intercalary, proliferating sympodially, pale brown
to brown, subcylindrical to swollen, (2.5–)5–15.5 × 3–7.5 μm. Material examined: Papua New Guinea, Madang, Jais Aben,
Conidia verruculose, curved, rarely straight, middle cells un- isolated from soil along coral reef coast, Nov. 1995, collected by
equally enlarged, reniform, rarely ellipsoidal, brown, with apical A. Aptroot, isol. by A. van Iperen (holotype CBS H-23116,
and basal cells paler than middle cells being subhyaline to culture ex-type CBS 222.96).
pale brown, (2–)3-distoseptate, 16–35 × 9–15.5 μm; hila
slightly protuberant, flat, darkened, slightly thickened, 1.5–4 μm. Notes: Curvularia soli is closely related to Cu. asianensis, Cu.
Chlamydospores, microconidiation and sexual morph not geniculata and Cu. senegalensis. All three species are charac-
observed. terised by conidia that are predominantly 4-distoseptate. Cur-
vularia geniculata is the only species that produces a sexual
Culture characteristics: Colonies on PDA reaching 90 mm diam morph and has the longest conidia among these taxa
within 1 wk, with sparse to moderate aerial mycelium giving a (26–48 μm). Curvularia asiatica can be distinguished from Cu.
slightly cottony appearance, margin lobate; surface apricot to soli by its much longer conidiophores [(75–)100–700(–708) μm]
chestnut; reverse umber to chestnut. and shorter conidia [(11–)15–23(–23.5) μm]. Curvularia sene-
galensis is characterised by having shorter conidiophores (up to
Material examined: Canada, Ontario, Renfrew, on Pisum sat- 150 μm) and wider conidia (10–14 μm) than Cu. soli.
ivum seeds, 15 Feb. 1943, J.W. Groves (holotype CBS H-
11405, culture ex-type CBS 190.48). Authors: Y. Marin-Felix, P.W. Crous & Y.P. Tan
Notes: Curvularia pisi is closely related to Cu. muehlenbeckiae Monilinia Honey, Mycologia 20: 153. 1928. Fig. 35.
and Cu. hominis. Morphologically, these species are similar but Synonym: Monilia Bonord., Handb. Mykol.: 7. 1851.
Cu. pisi produces shorter conidiophores. Moreover, Cu. mueh-
lenbeckiae produces smaller conidia than Cu. pisi, and Cu. Classification: Leotiomycetes, Leotiomycetidae, Helotiales,
hominis is characterised by 3–4-distoseptate conidia while the Sclerotiniaceae.
conidia in the other two species are 3-distoseptate.
Curvularia pisi is known to occur on Pisum sativum, which is Type species: Monilinia fructicola (G. Winter) Honey. Holotype:
also host to two other species of Curvularia, Cu. inaequalis and BPI 1109031.
Cu. spicifera. Curvularia spicifera produces a sexual morph, while
no sexual morph has been observed in the other two species. DNA barcode (genus): ITS.
Moreover, Cu. spicifera differs from Cu. pisi in having smooth-
walled conidia. Curvularia inaequalis can be distinguished from DNA barcode (species): tef1. Table 10. Fig. 36.
Cu. pisi by its longer conidia, which are predominantly 4-
distoseptate. Ascomata apothecial, cup- or funnel-shaped, long stipitate, pale
brown, formed solitary or in groups from pseudosclerotia in
Curvularia soli Y. Marín & Crous, sp. nov. MycoBank aborted or mummified fruits and debris partially or completely
MB820816. Fig. 34. buried in soil; stipe cylindrical, flexuous, pale brown, often darker
near the base; hymenium comprising filiform, septate, un-
Etymology: Named after its ecology, occurring in soil, “soli ”. branched and hyaline paraphyses. Asci unitunicate, inoperculate,
with amyloid apical apparatus, cylindrical to clavate, flattened or
Hyphae subhyaline to pale brown, branched, septate, thin- rounded at the apex, thin-walled, 8-spored. Ascospores ellipsoid,
walled, 2.5–5.5 μm. Conidiophores arising in groups, septate, often with tapered ends, 1-celled, hyaline, sometimes covered
straight or flexuous, geniculate at upper part, smooth to ver- with a gelatinous sheet. Conidiophores single or aggregated
ruculose, unbranched, cells walls thicker than those of vege- forming sporodochia, straight or flexuous, hyaline to subhyaline,
tative hyphae, mononematous, semi- to macronematous, pale branched, thin-walled, septate. Macroconidia blastic-acropetal,
brown to brown, slightly paler towards apex, not swollen at the oval, lemon-shaped or broadly ellipsoidal, rarely doliiform, hya-
base, (65–)90–270(–390) × 2.5–5( –6) μm. Conidiogenous line to subhyaline, thin-and smooth-walled, 1-celled, sometimes
cells smooth-walled to finely verruculose, terminal or interca- presenting distinct axial connections (disjunctors), formed in
lary, proliferating sympodially, pale brown to brown, sub- chains, simple or dichotomously branched; microconidia (sper-
cylindrical to swollen, 4–13 × 2.5–5 μm. Conidia verruculose, matia) sometimes present in old cultures, globose to pyriform,
curved, rarely straight, middle cells unequally enlarged, reni- hyaline, smooth- and thin-walled, borne on lageniform, often
form, rarely ellipsoidal, pale brown to brown, apical and basal asymmetric phialides. Arthric conidia occasionally formed, ovoid
cells paler than middle cells being subhyaline to pale brown, to ellipsoid, smooth- and thin-walled.
www.studiesinmycology.org 161
MARIN-FELIX ET AL.
0.02
162
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 33. Curvularia pisi (ex-type CBS 190.48). A, B. Conidiophores and conidia. C–G. Conidia. Scale bars: A–C = 10 μm; D–G = 5 μm.
Culture characteristics: Colonies on PDA white, yellow-grey, Other known hosts include members of Actinidiaceae, Ber-
brown-grey or olive-grey, often zonate or forming concentric beridaceae, Betulaceae, Ebernaceae, Ericaceae, Euphorbia-
rings, felty to velvety, flat or concave, margin entire or lobed ceae, Moraceae, Myricaceae, Myrtaceae, Solanaceae and
giving a rosette-like appearance, brown to black stromata can be Vitaceae.
present in old cultures.
Disease symptoms: Leaf spots, blossom and twig blight, twig and
Optimal media and cultivation conditions: PDA and WA, incu- stem canker, fruit rot.
bated under near-ultraviolet light (12 h light, 12 h dark) at
22–25 °C to determine growth rates, colour and shape of the Notes: Generic identification in vivo or in vitro is easy
colony, and induce sporulation of the asexual morph. The sexual considering the characteristic monilioid hyphae and sexual-
morph is not formed under in vitro culture conditions but can be morphs. Monilinia is morphologically similar and closely
induced by inoculation on natural substrata and incubated related to the genus Sclerotinia, from which it can be differ-
several months partially buried in sterilised soil. entiated by the absence of asexual reproduction and formation
of true sclerotia in Sclerotinia. However, species identification
Distribution: Worldwide. in Monilinia is rather difficult by means of morphology alone. A
combination of cultural features, physiology and host range is
Hosts: Mostly found as crop pathogens or causing post-harvest often necessary, including macro and micromorphology, growth
losses on stone fruits, most commonly on members of Rosa- rates, conidial dimension and characteristics of the germ tube
ceae, predominantly on Cydonia spp., Malus spp., Prunus spp. during sporulation. Other employed techniques include AFLP
and Pyrus spp., but have been reported in at least 11 other and RFLP (Gril et al. 2010, Vasic et al. 2016), specific PCR
genera on this family, linked to some kind of host specialisation. amplification for the three major brown rot pathogens
Fig. 32. RAxML phylogram obtained from the combined ITS (504 bp), gapdh (461 bp) and tef1 (893 bp), sequences of all the accepted species of Curvularia. The tree was
rooted to Bipolaris panici-miliacei CBS 199.29 and Bipolaris peregianensis DAOM 221998. The novel species described in this study are shown in bold. RAxML bootstrap
support (BS) values above 70 % and Bayesian posterior probability scores 0.95 are shown at the nodes. GenBank accession numbers are indicated in Table 9. ET, IsoT, IsoLT,
PT, SynT
and T indicate ex-epitype, ex-isotype, ex-isolectotype, ex-paratype, ex-syntype and ex-type strains, respectively. TreeBASE: S20877.
www.studiesinmycology.org 163
MARIN-FELIX ET AL.
Fig. 34. Curvularia soli (ex-type CBS 222.96). A–C. Conidiophores and conidia. D–G. Conidia. Scale bars: A = 10 μm; others = 5 μm.
M. fructigena, M. fructicola and M. laxa (Cote et al. 2004, Gell Japan (Harada et al. 2004), and later reported causing brown rot
et al. 2007) and amplification of specific introns for rapid of Prunus armeniaca (Yin et al. 2014) and Prunus salicina (Yin
identification of M. fructicola (Fulton & Brown 1997). A species et al. 2015) in China. Our phylogeny (Fig. 36) included se-
delimitation based on molecular phylogeny is currently lacking quences of two authentic isolates of Monilia numeicola and
and no ex-type material is known to exist for most taxa. supported its location in the genus Monilinia, being closely
However, several reference ITS and tef1 sequences are related to the common agents of brown rot M. fructicola,
available from a set of curated isolates in Q-bank (http://www. M. fructigena and M. laxa.
q-bank.eu/Fungi/).
A proposal to protect the generic name Monilinia over Monilia Monilinia yunnanensis (M.J. Hu & C.X. Luo) Sandoval-Denis &
has been recently published based on the complex and often Crous, comb. nov. MycoBank MB819177.
conflicting taxonomic history of the latter name (Johnston et al. Basionym: Monilia yunnanensis M.J. Hu & C.X. Luo, PloS ONE
2014). Following this proposal, two new combinations are pro- 6: 11. 2011.
posed below.
Notes: This taxon was described as a pathogen of peach
References: Batra 1988, 1991, Honey 1928, 1936, van Leeuwen (Prunus persica) in China and has subsequently been isolated
et al. 2002 (morphology and pathogenicity); van Leeuwen 2000 as the most prevalent pathogen of apple and pear in the
(morphology, pathogenicity and epidemiology); OEPP/EPPO southern, northern and western regions of that country (Zhu
2009, Martini & Mari 2014 (morphology, pathogenicity and et al. 2016). Its phylogenetic placement in Monilinia was sup-
biology). ported in our phylogeny (Fig. 36) based on sequences from two
authentic isolates, showing that it forms a clade basal to the
Monilinia mumeicola (Y. Harada et al.) Sandoval-Denis & main cluster grouping the most economically relevant species
Crous, comb. nov. MycoBank MB819176. of the genus.
Basionym: Monilia mumeicola [as ‘mumecola’] Y. Harada et al., J.
Gen. Plant Pathol. 70: 305. 2004. Authors: M. Sandoval-Denis & P.W. Crous
Notes: This species is only known from its asexual morph. It was Neofabraea H.S. Jacks., Rep. Oregon Exp. Sta. 1911–1912:
described as a pathogen on Japanese apricot (Prunus mume) in 187. 1913. Fig. 37.
164
GENERA OF PHYTOPATHOGENIC FUNGI
Classification: Leotiomycetes, Leotiomycetidae, Helotiales, that species of Neofabraea are more explicitly pathogenic than
Dermateaceae. those of Pezicula. Neofabraea further differs from Pezicula in that
Neofabraea produces ascomata with excipular tissues less
Type species: Neofabraea malicorticis H.S. Jacks. Neotype and differentiated and macroconidia more strongly curved with the
ex-neotype culture: CBS H-22219, CBS 122030 = OSC 100036. basal scar less distinct than in Pezicula. Moreover, Pezicula
comprises species that have two types of conidiogenesis: con-
DNA barcodes (genus): LSU. idiogenous cells are determinate and phialidic, or indeterminate
and proliferating percurrently, while Neofabraea spp. only pro-
DNA barcodes (species): ITS, tub2, rpb2. Table 11. Fig. 38. duces phialidic conidiogenous cells (Chen et al. 2016). Recently,
Chen et al. (2016) carried out a revision of the genus by per-
Ascomata apothecial, erumpent from bark, sessile to short- forming a phylogenetic study based on LSU, ITS, tub2 and rpb2
stalked, solitary or in clusters on a basal stroma; disc often sequences of Neofabraea, Pezicula and related genera.
not well-delimited, circular, elliptical, or irregular and merged, Consequently, the genus Phlyctema was re-established to
greyish, flesh-coloured to pale reddish or brownish, drying accommodate Neofabraea alba, which is the main pathogen
darker, 0.5–2.0 mm diam. Paraphyses numerous, filiform, causing bull's eye rot in continental Europe. Moreover, the new
septate, obtuse, simple or branched, hyaline, smooth-walled, genera Parafabraea and Pseudofabraea were introduced in or-
apical cells mostly slightly swollen. Asci inoperculate, der to accommodate Neofabraea eucalypti and Neofabraea cit-
cylindrical-clavate, apex rounded or truncate-rounded, attenu- ricarpa, respectively (Chen et al. 2016).
ated into a stalk of variable length, crozier present, 8-spored;
apical apparatus with a well-developed apical thickening, References: Verkley 1999 (morphology and pathogenicity),
Lugol's + or −, blue in herbarium material, Melzer's + or −. Wang et al. 2015 (morphology and key of Neofabraea spp.),
Ascospores inequilateral, elongated ellipsoid, ends rounded, Chen et al. 2016 (phylogeny).
straight or curved, aseptate, thin-walled, smooth, hyaline, with
granular contents or small oil droplets; later septate, sometimes Verkleyomyces Y. Marín & Crous, gen. nov. MycoBank
germinating or forming conidia from minute openings or phia- MB820818.
lides. Conidiomata erumpent from bark, stromatic, acervular,
plane to pulvinate. Conidiophores simple or branched, smooth, Etymology: Named after Gerard J.M. Verkley, in recognition for
hyaline, acrogenous or acropleurogenous. Conidiogenous cells his contributions to the understanding of Neofabraea and related
discrete or integrated, determinate, phialidic, cylindrical to genera.
narrowly ampulliform, giving rise to macro- and/or microconidia.
Macroconidia cylindrical-fusiform, allantoid to ellipsoid, straight Mycelium hyaline to pale brown, branched, septate. Ascomata
or curved, rounded or somewhat pointed at apex, rounded or apothecial, partly immersed, erumpent, sessile, solitary, some-
attenuated and with an indistinct, barely or non-protruding scar times gregarious; medullary excipulum weakly developed,
at base, smooth, aseptate, hyaline, and thin-walled when composed of hyaline textura prismatica; ectal excipulum
liberated, mostly filled with numerous oil droplets; later composed of brown to olivaceous brown textura prismatica at
becoming septate and brown. Microconidia present or absent, the base, and pale brown textura intricata towards the margin;
cylindrical, rounded at apex, narrowly truncate at base, asep- subhymenium hyaline, composed of interwoven hyphae. Pa-
tate, hyaline, thin- and smooth-walled, with minute granular raphyses cylindrical, slender, septate, apex rounded, hyaline,
contents (adapted from Chen et al. 2016). flexuous, numerous. Asci unitunicate, clavate to cylindrical-
clavate, base truncate, short pedicellate, with an apical appa-
Culture characteristics: Colonies on OA white, cottony. Colonies ratus stained blue or purplish blue in Melzer's reagent, 8-
on PDA orange or red, slimy. spored, ascospores discharging through apical pore. Asco-
spores fusoid to ellipsoid, hyaline, ends rounded or somewhat
Optimal media and cultivation conditions: OA at 25 °C under pointed, straight or slightly curved, thin-walled, guttulate or
near-ultraviolet light (12 h light, 12 h dark); OA supplemented eguttulate, initially aseptate, or later becoming 1-septate. Con-
with sterile nettle stems (Anthriscus sylvestris) or direct inocu- idiomata acervular or cupulate, semi-immersed, dark, separate,
lation into apple fruit (Malus domestica) can be used to induce formed of olivaceous brown textura intricata, dehiscence by
sporulation. irregular fissures, sometimes by a central ostiole. Co-
nidiophores simple, hyaline, smooth, thin-walled, septate at the
Distribution: Worldwide. base, unbranched, discrete, or rarely integrated beneath the
aged conidiogenous cell. Conidiogenous cells enteroblastic,
Hosts: Pathogens or harmless saprobes of apples and pears, but phialidic, cylindrical, hyaline, smooth, thin-walled, sometimes
also of several other hosts such as species of Prunus and with proliferation, periclinal thickening present. Conidia cylin-
Populus. drical, straight, apex obtuse, base abruptly tapered to a distinct
scar, hyaline, smooth, thin-walled, aseptate, eguttulate to
Disease symptoms: Anthracnose canker, perennial canker and biguttulate.
bull's-eye rot.
Culture characteristics: Colonies on PDA glaucous to sky-grey,
Notes: Neofabraea was introduced by Jackson (1913) to with irregular white margin; reverse olivaceous black.
accommodate the sexual morph Gloeosporium malicorticis.
Subsequently, Nannfeldt (1932) synonymised this genus with Type species: Verkleyomyces illicii (X. Sun et al.) Y. Marín & Crous.
Pezicula. However, Verkley (1999) revalidated it and observed Holotype and ex-type culture: HMAS244704, ASH-3-6-2-5b.
www.studiesinmycology.org 165
MARIN-FELIX ET AL.
166
GENERA OF PHYTOPATHOGENIC FUNGI
Notes: Verkleyomyces is introduced to accommodate Neo- Verkleyomyces illicii (X. Sun et al.) Y. Marín & Crous, comb.
fabraea illicii, the most recently published species of Neofabraea nov. MycoBank MB820819.
(Wang et al. 2015). In the phylogenetic analysis based on ITS Basionym: Neofabraea illicii X. Sun et al., Mycoscience 56: 334.
sequences (Fig. 38), this species was located in a clade separate 2015.
from the rest of the species belonging to Neofabraea. Ver-
kleyomyces is mainly differentiated by its endophytic habit. Description and illustration: Wang et al. (2015).
Morphologically both genera are comparable, but Verkleyomyces
produces 1-septate ascospores and aseptate conidia, while Note: Verkleyomyces illicii is an endophytic fungus isolated from
Neofabraea is characterised by aseptate ascospores and pre- Illicium verum, cultivated in a plantation in southern China.
dominately septate conidia. Parafabraea, which is more closely
related, also produces aseptate conidia, but this can be differ- Authors: Y. Marin-Felix & P.W. Crous
entiated from Verkleyomyces by the production of aseptate as-
cospores. Other similar genera are Pezicula and Dermea, but Neofusicoccum Crous et al., Stud. Mycol. 55: 247. 2006.
these can easily be distinguished by the production of asco- Fig. 39.
spores that are initially hyaline, and then become coloured or
contain coloured oil droplets.
Fig. 35. Monilinia spp. A–C. Disease symptoms. A, B. Monilinia fructigena on Malus sp. (A, CBS 348.72) and on Sorbus aucuperiae mummified fruit (B, CBS H-14553). C.
Monilinia laxa (CBS H-14556) leaf spot on Prunus padus. D. Sporodochia in vivo of Monilinia fructigena (CBS 348.72). E, F. Conidiophores. E. Monilinia fructigena (CBS
348.72). F. Monilinia fructicola (CBS 101512). G, H. Apothecia. G. Monilinia johnsonii (CBS H-005908) on Crategus sp. mummified fruit. H. Monilinia johnsonii (CBS H-005908)
stipitate apothecia. I–K. Asci of Monilinia johnsonii (CBS H-14554). K. Tip of an ascus showing a blue reaction with Meltzer's solution. L. Ascospores of Monilinia johnsonii
(CBS H-14554). M, N. Macroconidia. M. Monilinia fructicola (CBS 101512). N. Monilinia fructigena (CBS 348.72). O. Microconidia of Monilinia fructicola (CBS 101512). Scale
bars: A–C, G, H = 1 mm; D = 100 μm; E, F, I = 20 μm; J–O = 10 μm.
www.studiesinmycology.org 167
MARIN-FELIX ET AL.
CBS 102688T
98/99/1.0
M. polystroma
0.2 95/95/1.0 CBS 102687 (KX982703,LT632541)
CBS 492.50 (KX982698,LT632536)
100/100/1.0 CBS 348.72 M. fructigena
98/100/1.0 3231 01-03* (AB125614,-)
79/-/0.99 3231 01-01* M. mumeicola
CBS 133.21 (KX982699,LT632538) M. laxa
CBS 132.21
98/94/1.0
CBS 329.35
CBS 350.49 (KX982696,LT632534) M. fructicola
AL2-1 (KR778936,-)
-/-/0.99 KY-1 M. yunnanensis
86/100/0.97 CBS 170.24 M. seaveri
-/81/- CBS 139.23 M.mespili
ATCC 58542 M. johnsonii
100/100/1.0 CBS 120174 (KX982707,LT632544)
86/-/0.99 CBS 172.24 M. vaccinii-corymbosii
75/75/-
ATCC 64508 M. gaylussaciae
86/81/- ATCC 58546 M. polycodii
82/100/0.98 99/97/- CBS 388.93
ARO 951.2 (Z73773,-) M. baccarum
100/-/-
ARO 1087.P M. oxycocci
75/100/-
97/100/1.0
ARO 476.1 M. urnula
ARO 619.2 M. megalospora
100/100/1.0
4222T* M. jezoensis
74/-/- ATCC 58539 M. azaleae
100/100/1.0 ARO 1459.S M. cassiopes
CBS 150.22
M. linhartiana
MON09 (HM581953,-)
89/90/-
2769* M. mali
80/-/1.0
ATCC 58538 M. amelanchieris
8x
100/100/1.0
ARO 885.2 M. aucupariae
ARO 923.K M. padi
HHUF 19771T M. ssiori
93/97/100
NBRC 9725 M. kusanoi
Encoelia glauca (LT158438,KX090673)
Chlorociboria aeruginosa AFTOL-ID 151 (DQ491501,DQ471053)
Fig. 36. RaxML phylogram obtained from the combined ITS (428 bp) and tef1 (420 bp) sequences of Monilinia spp. currently known by DNA data. Maximum parsimony and
RaxML bootstrap support (BS) values above 70 % are shown at the nodes. Numbers between parentheses correspond to GenBank accession numbers for ITS and tef1
sequences, respectively. T indicates ex-type strain. TreeBASE: S20877.
Classification: Dothideomycetes, Incertae sedis, Botryosphaer- form periclinal thickenings. Conidia ellipsoidal with apex round
iales, Botryosphaeriaceae. and base flat, unicellular, hyaline, old conidia becoming 1–2-
septate hyaline, or light brown with the middle cell darker than
Type species: Neofusicoccum parvum (Pennycook & Samuels) the terminal cells. Dichomera synasexual morph: Conidia sub-
Crous et al. Holotype and ex-type culture: PDD 45438 (Her- globose to obpyriform, brown, apex obtuse, base truncate, 1–3
barium of Plant Diseases Division), ATCC 58191 = CBS transverse septa, 1–2 longitudinal septa, and 1–2 oblique septa.
138823 = PDDCC 8003 = ICMP 8003 = CMW 9081.
Culture characteristics: Colonies initially white to buff turning
DNA barcodes (genus): LSU, rpb2. olivaceous grey becoming black with age, moderately dense,
appressed mycelial mat with irregular very dense aerial aggre-
DNA barcodes (species): ITS, tef1, tub2, rpb2. Table 12. Fig. 40. gations, some conidioma covered by mycelium, immersed-
erumpent, conidia and spermatia present. Reverse white to
Ascomata forming botryose clusters, each comprising many olivaceous black. Reaching 90 mm diam on half strength MEA in
ascomata, erumpent through the bark, globose, with a short, 3–4 d.
conical papilla, dark brown to black, smooth, thick-walled;
ascomatal wall composed of dark brown thick-walled cells of Optimal media and cultivation conditions: Half strength MEA at
textura angularis, lined with thin-walled hyaline cells of textura 25–30 °C.
angularis. Asci clavate, 8-spored, bitunicate. Ascospores broadly
ellipsoidal to fusoid, hyaline, smooth, aseptate, occasionally Distribution: Worldwide.
becoming 1-septate. Conidiomata globose and non-papillate,
entire locule lined with conidiogenous cells. Conidiogenous Hosts: Plurivorous, mainly pathogenic on Anacardiaceae,
cells holoblastic, hyaline, subcylindrical, proliferating percurrently Cupressaceae, Ebenaceae, Fagaceae, Juglandaceae, Laur-
to form 1–2 annellations, or proliferating at the same level to aceae, Moraceae, Myrtaceae, Oleaceae, Pinaceae, Proteaceae,
168
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 37. Neofabraea malicorticis (ex-neotype CBS 122030). A. Colony on MEA. B. Colony on OA. C. Conidiomata on inoculated apple. D. Conidial mass on apple peel. E.
Conidiogenous cells from sporodochium on OA. F. Conidiogenous cells giving rise to macroconidia. G. Microconidia on OA. H. Macroconidia from OA. I. Macroconidia from
inoculated apple. J, K. Intermediate conidia between macro- and microconidia. Scale bars: 10 μm, I applies to H, I. Pictures taken from Chen et al. (2016).
Rosaceae, Rutaceae, Vitaceae, families belonging to Lamiales To separate Neofusicoccum from Botryosphaeria based solely
and various other host plants. on morphology can be difficult due to similar morphological
characteristics. Therefore, molecular data are required to ach-
Disease symptoms: Fruit rot, wood canker, leaf spots. ieve accurate identification. One morphological difference be-
tween both genera is the presence of a Dichomera synasexual
Notes: Neofusicoccum was introduced by Crous et al. (2006b) morph in Neofusicoccum. However, this synasexual morph is
to accommodate species morphologically similar to, but not produced by all Neofusicoccum species, nor even all iso-
phylogenetically divergent from Botryosphaeria (= Fusicoccum). lates of any given species. Moreover, dichomera-like conidia
www.studiesinmycology.org 169
MARIN-FELIX ET AL.
Fig. 38. RAxML phylogram obtained from the ITS (564 bp) sequences of Neofabraea spp. and related genera. Maximum parsimony and RAxML bootstrap support (BS) values
above 70 % are shown in the nodes. The new genus introduced in this study is shown in bold. The tree was rooted to Sclerotinia sclerotiorum CBS 499.50. Numbers between
parentheses correspond to GenBank accession numbers. T indicates ex-type strain. TreeBASE: S20877.
were reported in some isolates of Bot. dothidea (Barber et al. (phylogeny); Pavlic et al. 2009b (morphology, pathogenicity
2005, Phillips et al. 2005). Other morphological differences are and phylogeny), Phillips et al. 2013 (morphology, phylogeny and
the absence of paraphyses in the conidiomata of Neo- dichotomous key).
fusicoccum spp., while these have been seen in most of the
currently accepted Botryosphaeria species, and the conidial L/ Neofusicoccum italicum Dissanayake & K.D. Hyde, sp. nov.
W ratios being less than 4 in Neofusicoccum. Furthermore, the MycoBank MB820799, Facesoffungi number FOF02963. Fig. 41.
conidia of Neofusicoccum are more ellipsoidal than the fusiform
ones of Fusicoccum s. str. Etymology: Based on the country where the type specimen was
Species in Neofusicoccum are morphologically similar and collected, Italy.
hard to differentiate from one another. Neofusicoccum spe-
cies are currently defined on the basis of conidial di- Sexual morph not observed. Conidiomata 0.5–1.5 × 1.5–2 mm,
mensions and pigmentation, pigment production in culture black, scattered, uniloculate, globose; conidiomatal wall
media and ITS sequence data. Taxa in some of the species composed of dark brown textura angularis, becoming hyaline
complexes are defined exclusively on DNA sequence data towards conidiogenous region. Conidiophores reduced to con-
(ITS, often together with tef1, tub2 and rpb2. In some cases, idiogenous cells. Conidiogenous cells 9–16.5 × 2.5–3.5 μm,
multigene sequence data are essential for species lining inner wall of pycnidium, holoblastic, cylindrical to sub-
identification. obpyriform, hyaline, discrete, determinate, occasionally indeter-
minate and proliferating percurrently with indistinct annellations.
References: Crous et al. 2006b, Berraf-Tebbal et al. 2014, Yang Conidia 13–18.5 × 3.5–6 μm, obovoid, fusiform, base truncate,
et al. 2017 (morphology and phylogeny); Pavlic et al. 2009a apex obtuse to subobtuse, hyaline, guttulate, non-septate, older
170
GENERA OF PHYTOPATHOGENIC FUNGI
conidia may become brownish and septate before germination. from Nm. pistaciarum, which is the closest phylogenetic species,
Dichomera synasexual morph not reported. and also a pathogen of Pistacia vera. Other species of Neo-
fusicoccum associated to this host are Nm. australe, Nm.
Culture characteristics: Colonies white with abundant aerial mediterraneum, Nm. nonquaesitum, Nm. parvum and Nm. pis-
mycelium reaching 90 mm diam within 1 wk on PDA at 28 °C. taciae (Inderbitzin et al. 2010, Phillips et al. 2013, Yang et al.
Aerial mycelium becoming smoke-grey to olivaceous grey at the 2017).
surface and dull green to brown-vinaceous at the reverse after
2 wk in the dark at 28 °C. Neofusicoccum pruni Crous, sp. nov. MycoBank MB820821.
Fig. 43.
Materials examined: Italy, on a dead branch of Vitis vinifera, 22
Nov. 2014, E. Camporesi (holotype MFLU 16-2872, culture ex- Etymology: Named after the host genus from which it was
type MFLUCC 15-0900). New Zealand, on Malus × domestica, collected, Prunus.
unknown date, H.J. Boesewinkel, CBS 719.85.
Sexual morph not observed. Conidiomata stromatic, solitary,
Notes: According to the phylogenetic analysis Neofusicoccum globose to obpyriform, up to 300 μm diam; conidiomata wall
italicum clustered close to Nm. algeriense, which has larger 6–10 cell layers thick, of brown textura angularis, becoming
conidia (17.6 × 5.6 μm) than those of Nm. italicum hyaline toward inner region. Conidiophores 0–1-septate, hya-
(15.8 × 5.2 μm). Both species are pathogens of Vitis vinifera, but line, subcylindrical, 10–20 × 2.5–4 μm. Conidiogenous cells
Nm. algeriense is restricted to this host while Nm. italicum was holoblastic, hyaline, subcylindrical, 10–15 × 2.5–3.5 μm,
also isolated from Malus × domestica. Other species of Neo- proliferating percurrently with numerous proliferations, or
fusicoccum associated with Vitis vinifera are Nm. australe, Nm. proliferating at the same level (phialidic) with minute periclinal
luteum, Nm. mediterraneum, Nm. parvum, Nm. stellenboschiana, thickening. Conidia hyaline, granular, aseptate, fusoid to ellip-
Nm. viticlavatum and Nm. vitifusiforme (Van Niekerk et al. 2004a, soid, widest in the middle or upper third with an obtuse apex
Phillips et al. 2013, Yang et al. 2017). Neofusicoccum and other and flattened, subtruncate base, (18–)20–23(–25) × (6.5–)
related genera belonging to Botryosphaeriaceae are widely 7–7.5(–8.5) μm. Spermatia or Dichomera synasexual morph
distributed pathogens of grapevines that cause bud mortality, not observed.
dieback, brown streaking inside the wood, internal necrotic le-
sions and in some cases bunch rot (Phillips et al. 2013). Culture characteristics: Colonies on MEA reaching 90 mm diam
within 1 wk, with fluffy moderate aerial mycelium; surface and
Neofusicoccum pistaciicola Crous, sp. nov. MycoBank reverse greenish black.
MB820820. Fig. 42.
Material examined: South Africa, Limpopo, Mookgopong,
Etymology: Named after the host genus from which it was from branches of Prunus salicina, Aug. 2004, U. Damm
collected, Pistacia. (holotype CBS H-23109, culture ex-type CBS 121112 = CPC
5912).
Sexual morph not observed. Conidiomata stromatic, solitary,
globose, up to 300 μm diam; conidiomatal wall 6–8 cell layers Notes: Neofusicoccum vitifusiforme was initially described
thick, of brown textura angularis, becoming hyaline toward inner from Vitis vinifera in South Africa by van Niekerk et al.
region. Conidiophores 0–2-septate, branched, hyaline, smooth, (2004a). Damm et al. (2007) was the first to report this fun-
subcylindrical, 15–25 × 4–5 μm. Conidiogenous cells holo- gus as a pathogen from Prunus salicina in South Africa,
blastic, hyaline, smooth, subcylindrical, proliferating percurrently, although their phylogenetic tree showed this isolate (CBS
12–17 × 2.5–3.5 μm. Conidia hyaline, smooth, thin-walled, 121112) to cluster basal to the grapevine strains based on ITS
granular, aseptate, subcylindrical to fusoid-ellipsoid, apex sub- and tef1 sequence data. A recent study by Yang et al. (2017),
obtuse, base truncate, 1.5–2.5 μm, straight to irregularly curved, which incorporated all Neofusicoccum isolates available in the
(15–)18–24(–27) × (4–)4.5(–5) μm. Spermatia or Dichomera CBS culture collection, as well as additional genes (rpb2 and
synasexual morph not observed. tub2) showed the Prunus isolate to represent a distinct spe-
cies. This isolate (formerly sterile) has subsequently been
Culture characteristics: Colonies on MEA reaching 90 mm diam induced to sporulate, and is therefore named in the present
within 1 wk, with fluffy moderate aerial mycelium; surface pale study.
mouse-grey, reverse mouse-grey to dark mouse-grey.
Authors: Y. Marin-Felix, E. Camporesi, A. Dissanayake, K.D.
Material examined: USA, California, Glenn County, on Pistacia Hyde & P.W. Crous
vera, 12 Apr. 2002, T.J. Michailides (holotype CBS H-23108,
culture ex-type CBS 113089). Pilidium Kunze, Mykol. Hefte 2: 92. 1823. Fig. 44.
Synonyms: Sclerotiopsis Speg., Anal. Soc. Cient. Argent. 13: 14.
Notes: Neofusicoccum pistaciicola is morphologically similar to 1882.
Nm. hellenicum, which Chen et al. (2015b) recently described Hainesia Ellis & Sacc., in Saccardo, Syll. fung. (Abellini) 3: 698.
from Pistacia vera in the USA. However, compared with Nm. 1884.
hellenicum, Nm. pistaciicola possesses smaller conidiomata and Discohainesia Nannf., Nova Acta Regiae Soc. Sci. Upsal., Ser. 4
narrower conidia. The same features are used to distinguish it 8: 88. 1932.
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MARIN-FELIX ET AL.
Fig. 39. Neofusicoccum spp. A–D. Disease symptoms. A. Leaf blight on Protea sp. B. Canker on Vitis vinifera. C, D. Cankers on Eucalyptus sp. E–J. Sexual morphs. E, F.
Ascomata. E. Neofusicoccum parvum (ex-type ATCC 58191). F. Neofusicoccum luteum (ex-type ATCC 58193). G, H. Asci. G. Neofusicoccum luteum (ex-type ATCC 58193). H.
Neofusicoccum australe (ex-type CMW 6837). I. Detail of ascus apex of Neofusicoccum parvum (ex-type ATCC 58191). J. Ascospores of Neofusicoccum parvum (ex-type
172
GENERA OF PHYTOPATHOGENIC FUNGI
ATCC 58191). K–S. Asexual morph. K. Conidiomata on pine needles in culture of Neofusicoccum australe (CMW 6837). L, M. Conidiogenous cells. L. Neofusicoccum
mediterraneum (ex-type CBS 121718). M. Neofusicoccum parvum (ex-type ATCC 58191). N–P. Conidia. N. Neofusicoccum arbuti (ex-type CBS 116131). O. Neofusicoccum
australe (ex-type CMW 6837). P. Neofusicoccum vitifusiforme (ex-type CBS 110887). Q. Coloured, 1- and 2-septate conidia of Neofusicoccum parvum (ex-type ATCC 58191).
R. Spermatogenous cells of Neofusicoccum mediterraneum (ex-type CBS 121718). S. Spermatia of Neofusicoccum mediterraneum (ex-type CBS 121718). Scale bar:
E–G = 50 μm; H, J, L–P, R = 10 μm; I, Q, S = 5 μm; K = 1 mm. Pictures taken from Phillips et al. (2013).
www.studiesinmycology.org 173
MARIN-FELIX ET AL.
0.03
174
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 41. Neofusicoccum italicum (ex-type MFLUCC 15-0900). A. Conidiomata on host substrate. B, C. Cross section of conidiomata. D, E. Immature and mature conidia
attached to conidiogenous cells. F. Mature conidia. Scale bars: B, C = 100 μm. D–F = 20 μm.
Classification: Leotiomycetes, Leotiomycetidae, Helotiales, irregularly, or lacking. Conidiophores hyaline, smooth, branched,
Chaetomellaceae. cylindrical or filiform. Conidiogenous cells enteroblastic, phialidic,
acropleurogenous, hyaline, smooth. Conidia mostly non-septate,
Type species: Pilidium acerinum (Alb. & Schwein.) Kunze. hyaline, smooth, fusiform to falcate or cymbiform, with ends
Iconotype in Kunze & Schmidt (1817), table 2, fig. 5. Epitype and slightly pointed, straight to curved. Sporodochia globose
ex-epitype culture: BPI 843555, CBS 736.68. becoming cupulate, discoid, with irregularly wavy margin, slimy,
pale luteous, superficial, solitary, stalk pale brown near base,
DNA barcode (genus): LSU. becoming dark brown at apex. Conidiophores hyaline, smooth,
branched, cylindrical or filiform. Conidiogenous cells entero-
DNA barcode (species): ITS. Table 13. Fig. 45. blastic, phialidic, acropleurogenous, determinate, integrated,
filiform or subcylindrical, hyaline, smooth, with minute collarette.
Ascomata apothecial, flat to funnel-shaped, short stipitate, white, Conidia aseptate, hyaline, smooth, fusiform to falcate or cym-
pale brown to amber in the basal portion, wall pseudoparen- biform to allantoid, with acute ends, straight to curved.
chymatous (plectenchymatous). Paraphyses narrow, simple or
branched, aseptate. Asci unitunicate, cylindrical, clavate, Culture characteristics: Colonies on PDA surface and reverse
rounded or truncate at the apex, deliquescent. Ascospores white to cinnamon, buff, honey, sepia or isabelline, slimy with
ellipsoidal, somewhat enlarged at one side, straight to slightly aerial mycelium absent or sparse, flat, granulose due to pro-
curved, aseptate, smooth-walled. Conidiomata pycnidial or duction of fruiting bodies; margin smooth and lobate.
sporodochial; pycnidia globose, subglobose, obpyriform or
oblong, sessile, pale brown when young, dark brown to black at Optimal media and cultivation conditions: PDA, OA and MEA
maturity, superficial, solitary or gregarious, uniloculate, smooth; incubated at 25 °C for 1 wk at 25 °C under alternating fluores-
conidiomatal wall with two regions: outer region dark brown, cent (12 h) and near ultraviolet (12 h) light are suitable to
inner region hyaline; opening by a stellate slit, rupturing determine cultural characteristics and induce sporulation of the
Fig. 40. RAxML phylogram obtained from the combined ITS (541 bp), tef1 (302 bp), rpb2 (594 bp) and tub2 (463 bp) sequences of Neofusicoccum spp. The tree was rooted to
Botryosphaeria dothidea CBS 100564. The novel species described in this study are shown in bold. RAxML bootstrap support (BS) values above 70 % and Bayesian posterior
probability scores 0.95 are shown at the nodes. GenBank accession numbers were listed in Berraf-Tebbal et al. (2014), Chen et al. (2015b), and Yang et al. (2017). T and NT
indicate ex-type and ex-neotype strains, respectively. TreeBASE: S20877.
www.studiesinmycology.org 175
MARIN-FELIX ET AL.
Fig. 42. Neofusicoccum pistaciicola (ex-type CBS 113089). A. Conidiomata forming on PNA. B, C. Conidiomata cells giving rise to conidia. D. Conidia. Scale bars: 10 μm.
Fig. 43. Neofusicoccum prunii (ex-type CBS 121112). A. Conidiomata forming on PNA. B, C. Conidiomata cells giving rise to conidia. D. Conidia. Scale bars: 10 μm.
asexual morph. The sexual morph is not formed in vitro, and is Discohainesia oenotherae and Hainesia lythri were
relatively uncommon and inconspicuous. considered the sexual and synasexual morphs of Pi. lythri
(Rossman et al. 2004). However, after the one fungus = one
Distribution: Worldwide. name initiative the generic name Pilidium was proposed for
conservation over Hainesia and Discohainesia (Johnston et al.
Hosts: Species of this genus are mainly found on different hosts 2014).
of Anacardiaceae, Hippocastanaceae, Myrtaceae and Rosa-
ceae, and also in several other families such as Betulaceae, References: Sutton 1980, Shear & Dodge 1921, Palm 1991
Ebenaceae, Fabaceae, Geraniaceae, Oleaceae, Paeoniaceae, (morphology); Sutton & Gibson 1977 (morphology and patho-
Pinaceae, Polygonaceae, Salicaceae, Sapindaceae, Saxi- genicity); Rossman et al. 2004 (morphology, pathogenicity and
fragaceae and Vitaceae. ecology).
Disease symptoms: Leaf spots, root lesions and tan-brown rot of Pilidium septatum Giraldo & Crous, sp. nov. MycoBank
fruits. MB820871. Fig. 46
Notes: Species of Pilidium are commonly found as plant- Etymology: Refers to the presence of septate conidia.
associated fungi or isolated from soil (Sutton 1980), and they
are known to produce two kinds of conidiomata. Pilidium lythri Conidiomata pycnidial, superficial, solitary or gregarious, brown
(formerly known as Pi. concavum) and Pi. pseudoconcavum to black, smooth, uniloculate, subglobose to obpyriform,
form sporodochia in culture. Although, the former species also 97–260 × 127–230 μm; outer conidiomatal wall 11–27 μm thick,
produces the pycnidial morph, both species can be distinguished with textura angularis, formed by thick-walled, brown cells; inner
based on conidial shape (fusiform vs. cymbiform), sporodochial conidiomatal wall 13–20 μm thick, with textura angularis or
size (300–1000 μm diam vs. up to 300 μm diam) and DNA globulosa, formed by 4–5 layers of thick-walled, hyaline cells.
sequences (Crous et al. 2013b). Both Pi. acerinum and Pi. Conidiophores branched, cylindrical, septate, hyaline, smooth,
eucalyptorum produce brown pycnidia in vitro and they are up to 24 μm long, 1.5–2 μm diam. Conidiogenous cells acrop-
closely related (Fig. 45). However, they differ in pycnidial size leurogenous, monophialidic, cylindrical, slightly curved, smooth,
(200–1000 μm diam vs. up to 300 μm diam), conidiophore shape hyaline, delineating the inner part from the pycnidium,
(cylindrical vs. filiform) and in the production of guttulate conidia, 7–11 × 1.5–2 μm. Conidia 1-septate, hyaline, falcate with ends
which are absent in Pi. acerinum and present in Pi. eucalyptorum slightly pointed, thin- and smooth-walled, (8.1–)
(Rossman et al. 2004, Crous et al. 2015e). 9–11(–12.5) × (1–)1.5(–2) μm.
176
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 44. Pilidium species. A, E, G. Pilidium eucalyptorum (CBS 140662). B, F, H. Pilidium pseudoconcavum (CBS 136433). C, D, I. Pilidium leucospermi (holotype PREM
59602). A, B. Conidiomata on OA and SNA, respectively. C. Vertical section of conidioma. D. Peridium. E, F. Conidiogenous cells. G–I. Conidia. Scale bars: C = 50 μm;
D–I = 10 μm. Pictures C, D, I modified from Marincowitz et al. (2008a).
Culture characteristics: Colonies on OA and PDA reaching culture ex-type BCC 79016); Nan province, Bo Kluea district,
30–40 mm in 2 wk. Colonies flat, granulose due to production of N19.14833333° E101.1566667, from soil, 8 Aug. 2015, A.
pycnidia, with scarce aerial mycelium, surface honey to Giraldo (BCC 79037).
isabelline.
Notes: Presently the genus includes only species with aseptate
Materials examined: Thailand, Nakhon Nayok province, conidia, and thus Pi. septatum, with septate conidia, expands the
Mueang Nakhon Nayok district, Wang Takhrai waterfall, generic concept of Pilidium. In addition to the phylogenetic
N14.330023° E101.307168°, 64 m above sea level, from soil, relationship revealed through the analysis of LSU and ITS re-
22 Jul. 2015, A. Giraldo (holotype metabolically inactive, gions (Fig. 45), morphological characteristics such as the
www.studiesinmycology.org 177
MARIN-FELIX ET AL.
100/1.0
CBS 114293
Pi. lythri
0.01 99/1.0 BPI 1107274 (AY487098,AY487097)
100/1.0
CBS 136433T Pi. pseudoconcavum
100/1.0
CBS 736.68ET
100/1.0 Pi. acerinum
CBS 403.71 (AY487089, AY487088)
100/1.0
BCC 79016T
Pi. septatum
BCC 79037 (PENDING, PENDING)
Chaetomella raphigera CBS 130.64IT (AY487086, AY487085)
Fig. 45. Maximum likelihood (ML) tree based on partial sequences of LSU (792 bp) and ITS (477 bp) regions from reference and ex-type strains of Pilidium species. Bootstrap
support values and posterior probabilities above 70 % and 0.95, respectively are shown at the nodes. Chaetomella raphigera and Chaetomella oblonga (Chaetomellaceae,
Helotiales) were used as outgroup taxa. Numbers within parentheses correspond to GenBank accession numbers of LSU and ITS sequences, respectively.T and ET indicate ex-
type and ex-epitype strains, respectively. TreeBASE: S20877.
morphology of the pycnidia, the production of acropleurogenous Conidiogenous cells mono- and polyblastic, integrated, terminal
conidiogenous cells and conidial shape, support the inclusion of and intercalary, cylindrical. Conidia solitary, dry, subcylindrical to
this species within the genus. fusoid, mostly curved, narrowed to obtuse at the apex, truncate
at the base, pale to dark brown, smooth, multiseptate; apical cell
Authors: A. Giraldo, J. Luangsa-ard & P.W. Crous bears several long, hyaline, subulate appendages which are
sometimes branched. Chlamydospores present or absent, brown
Pleiochaeta (Sacc.) S. Hughes, Mycol. Pap. 36: 39. 1951. Figs to dark brown in chains or in groups.
47, 48.
Synonym: Ceratophorum subgen. Pleiochaeta Sacc., Syll. fung. Culture characteristics: Colonies on PDA grey to olivaceous
(Abellini) 11: 622. 1895. black with aerial mycelium white, cottony, margin fimbriate,
effuse; reverse black.
Classification: Dothideomycetes, Pleosporomycetidae, Pleo-
sporales, Dothidotthiaceae. Optimal media and cultivation conditions: MEA, OA, PDA or SNA
with sterilised twigs, incubated at 25 °C. Not all strains sporulate
Type species: Pleiochaeta setosa (Kirchner) S. Hughes. Epitype well in culture.
and ex-epitype culture designated here: CBS H-23058, CBS
496.63 = MUCL 8091). Distribution: Worldwide.
DNA barcode (genus): LSU. Hosts: Mainly pathogens of legumes, with one species reported
from carrots.
DNA barcode (species): ITS. Table 14. Figs 49, 50.
Disease symptoms: Brown leaf spots, lesions are circular and
Sexual morph unknown. Conidiophores macronematous, mon- zonate. It also can attack stems, pods and roots, and destroy
onematous or grouped in fascicles, simple, erect, straight to whole plants.
flexuous, or geniculate, hyaline to pale olivaceous, smooth.
178
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 46. Pilidium septatum (ex-type BCC 79016). A. Conidiomata on OA. B, C. Longitudinal sections of pycnidia. D. Details of ostiolar region. E. Details of the outer and inner
pycnidial walls. F, G. Conidiophores and conidiogenous cells. H. Conidia. Scale bars: B–H = 10 μm.
Notes: Pleiochaeta was established by Hughes (1951) to Mycelium partly immersed, partly superficial, composed of
accommodate two species previously included in Ceratophorum, branched, septate, hyaline to dark brown, smooth, 3–9 μm wide,
namely Plei. setosa and Plei. albizziae. Currently this genus hyphae. Conidiophores macronematous, mononematous, usu-
comprises six species, including pathogens and saprobes. ally unbranched, flexuous, frequently geniculate, hyaline or pale
Pleiochaeta setosa, the generic type, is the most important olivaceous, smooth. Conidiogenous cells mono- and polyblastic,
species from a phytopathogenic point of view, causing serious integrated, terminal and intercalary, sympodial, cylindrical to
damage in Lupinus spp. and other legumes members of Faba- geniculate. Conidia solitary, dry, subcylindrical ellipsoid to fusoid,
ceae. Sequences available to date for the genus are scant. After mostly curved, narrowed at apex, truncate at the base, at first
the analysis of LSU and ITS sequences of the isolates studied colourless becoming orange-brown to olivaceous brown,
with members of Pleosporales (Dothideomycetes), we support smooth, 92–137 × 16–22 μm, 6–10-septate, usually constricted
the phylogenetic position of Plei. setosa and Plei. ghindensis in at the septa; basal cell conical, truncate, subhyaline to pale
the Dothidotthiaceae. Furthermore, our results allow us to brown, 8–11 μm wide; apical cell obtuse, arising 2–3 hyaline
describe a new species from South Africa, Plei. carotae, causing appendages, with one appendage arising apically which are
a disease on carrot leaves. Cultures of Plei. albiziae, Plei. usually branched 2–4 times, and another two laterally on the
amazonensis, Plei. cassiae and Plei. stellaris were not available sides which are usually branched 1–2(–3) times, appendages
for this study, and their phylogenetic position remains unknown. 70–114 μm long, 4.5–7 μm wide at the point of origin and
Further studies with additional molecular data of isolates from pointed at their apices. Chlamydospores not observed.
different origins and substrates, as well as pathogenicity tests,
need to be conducted. Culture characteristics: Colonies reaching 40–55 mm diam after
1 wk at 25 °C on OA, PDA and MEA olivaceous black, cottony,
References: Hughes 1951 (taxonomy and morphology); with white aerial mycelium in the centre, exudate hyaline, margin
Pirozynski 1974 (morphology and distribution); Bateman 1997 fimbriate, effuse, colourless; reverse black.
(pathogenicity); Yang & Sweetingham 2002 (morphology and
pathogenicity). Material examined: South Africa, Gauteng, Pretoria, on carrot
leaf, Mar. 2015, M. Truter (holotype CBS H-23057, culture ex-
Pleiochaeta carotae Hern.-Restr., van der Linde & Crous, sp. type CPC 27452 = CBS 142644).
nov. MycoBank MB820795. Fig. 47.
Notes: This is the first species of Pleiochaeta described from
Etymology: Named after the host genus from which it was iso- carrots, a non-legume host plant. Conidia of this species
lated, Daucus carota. resemble those of Plei. ghindensis, having branched apical
www.studiesinmycology.org 179
MARIN-FELIX ET AL.
Fig. 47. Pleiochaeta carotae (ex-type CBS 142644) A. Conidiophores with conidia. B. Conidiophores and conidiogenous cells. C–P. Conidia. Scale bars: 10 μm
appendages, usually more than twice branched. In Plei. ghin- mono-, usually polyblastic, integrated, terminal and intercalary,
densis conidiogenous cells are monoblastic, terminal and cylin- sympodial, cylindrical, geniculate, hyaline to pale olivaceous,
drical with percurrent proliferations. However, in Plei. carotae, 25–68 × 8–11.5 μm. Conidia solitary, dry, subcylindrical to
conidiogenous cells are mono- and polyblastic, terminal and fusoid, mostly curved, narrowed at the apex, truncate at the
intercalary and geniculate with sympodial proliferations. base, colourless or with the cell at each end hyaline or sub-
Furthermore, conidia in Plei. carotae are larger (92–137 μm vs. hyaline and intermediate cells straw-coloured to golden brown,
85–115 μm in Plei. ghindensis) and with a larger number of smooth, 68–88.5 × 11–25 μm, 8.5–11 μm wide at the base,
septa (6–10 vs. 6–7 in Plei. ghindensis). Finally, the basal 4–7-septate; apical cell bears 3–4 hyaline, subulate append-
conidial cells are usually paler than the other cells (in Plei. ages, 89–150 × 2.5–5.5 μm, apical appendage at first simple
ghindensis conidia are concolourous). later becoming branched, lateral appendages simple. Chla-
mydospores pale brown to dark brown, terminal and intercalary,
Pleiochaeta setosa (Kirchn.) S. Hughes. Mycol. Pap. 36: 34. in chains or in groups (observed in CBS 142.51 and 502.80, but
1951. Figs 48, 51. not in the epitype).
Basionym: Ceratophorum setosum Kirchn. Z. Pflanzenkrankh.
Pflanzenschutz 2: 324. 1892. Culture characteristics: Colonies reaching 25–50 mm diam
Synonyms: Pestalotia lupini Sorauer, Z. Pflanzenkrankh. Pflan- after 1 wk at 25 °C on OA, PDA and MEA, cottony to
zenschutz 8: 269. 1898. glabrous, smoke-grey to olivaceous black, with aerial myce-
Mastigosporium lupini (Sorauer) Cavara, Riv. Patol. Veg. 14: 13. lium in the centre white, margin effuse, fimbriate; reverse
1924. black. On OA sometimes with hyaline exudate and apricot
diffusible pigment.
Mycelium partly immersed, partly superficial, composed of
branched, septate, hyaline to brown, smooth, 4–7.5 μm wide, Material examined: Lectotype designated here: figs 1–6 in
hyphae. Conidiophores macronematous, mononematous, usu- Kirchner O. 1892. Über das Absterben junger Cytisus-Pflanzen.
ally unbranched, flexuous, frequently geniculate, hyaline or pale Z. Pflanzenkrankh. Pflanzenschutz 2: 324–327, MBT376013.
olivaceous, smooth, 34–138 × 5–11 μm. Conidiogenous cells
180
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 48. Pleiochaeta setosa (ex-epitype CBS 496.63, CBS 502.80). A–D. Conidiophores with conidia (ex-epitype CBS 496.63). E, F. Conidiogenous cells (ex-epitype CBS
496.63). G–L. Conidia (ex-epitype CBS 496.63). M–O. Chlamydospores (CBS 502.80). Scale bars: 10 μm.
www.studiesinmycology.org 181
MARIN-FELIX ET AL.
Austria, Wallersberg, near Völkermarkt, on living stem and leaf DNA barcodes (genus): LSU, ITS.
of Genista sagittale, Aug. 1980, W. Gams, CBS 502.80. Ger-
many, Berlin, on leaf of Cytisus racemosus, unknown date, R. DNA barcodes (species): tub2, rpb2. Table 15. Fig. 53.
Schneider (epitype designated here CBS H-23058,
MBT376012, culture ex-epitype = CBS 496.63 = MUCL 8091). Ascomata solitary, scattered or in small groups, erumpent to
The Netherlands, Boskoop, on spot on stem of Cytisus sp., superficial, subglobose, broadly or narrowly conical, small- to
unknown date, I. de Boer, CBS 142.51. Unknown country, on medium sized, dark brown to black, smooth, ostiolate; ostiole
leaf of Laburnum sp., unknown date, dep. C.M. Doyer, CBS apex with a conical, well developed papilla; ascomatal wall
118.25. composed of two to several layers of scleroplectenchymatous
cells. Hamathecium comprising long, septate, pseudopar-
Notes: Pleiochaeta setosa was introduced by Kirchner (1892) as aphyses. Asci 8-spored, bitunicate, fissitunicate, cylindrical,
Ceratophorum setosum for a fungus that infects Cytisus in rounded at the apex, with an ocular chamber, short pedicel.
Germany and later was transferred to Pleiochaeta by Hughes Ascospores cylindrical to ellipsoidal, yellowish brown, septate,
(1951). Since type material for Plei. setosa is inexistent, the il- not or slightly constricted at septa, guttulate and lacking a
lustrations included in the protologue reproduced here (Fig. 51) mucilaginous sheath, cell above central septum slightly wider.
serve as lectotype. In addition, to fix the use of the name the Conidiomata. Type 1: solitary, scattered or in small groups,
strain CBS 496.63 is designated here as ex-epitype. This isolate erumpent to superficial, subglobose or flask shaped with a broad
was collected, from the same locality and host genus where it base, mostly black, ostiolate; ostiole with a long neck and well
was found the first time (Kirchner 1892) and fits well with the developed poroid papilla in the apex. Type 2: solitary, scattered
description of the protologue. This species has a worldwide or in small groups, erumpent to superficial, mostly subglobose,
distribution and it is frequently reported as pathogen of Lupinus ostiolate; ostiole slightly papillate with a narrow pore or opening
(Hughes 1951, Pirozynski 1974). Nevertheless, Crotalaria, via a rupture. Conidiomatal wall composed of several layers with
Genista, Laburnum and Ornithopus can also be hosts of this thick-walled cells of textura angularis, surface heavily pigmented.
species (Pirozynski 1974, Yang & Sweetingham 2002). Unfor- Conidiophores reduced to conidiogenous cells. Conidiogenous
tunately, host specificity studies are not available for this species, cells phialidic, hyaline, smooth, ampulliform. Conidia hyaline,
even though Yang & Sweetingham (2002) reported morpholog- aseptate, ellipsoidal to subcylindrical (adapted from Ariyawansa
ical and pathogenicity differences among isolates from Lupinus et al. 2015b).
spp. and Ornithopus spp.
Culture characteristics: Colonies on OA yellow/green to oliva-
Authors: M. Hernandez-Restrepo, E.J. van der Linde & P.W. ceous grey, dull green, or translucent, aerial mycelium tenuous,
Crous margin irregular and whitish, compact, floccose.
Plenodomus Preuss, Linnaea 24: 145. 1851. Fig. 52. Optimal media and cultivation conditions: OA or PNA near-
Synonyms: Phoma sect. Plenodomus (Preuss) Boerema, Kes- ultraviolet light (12 h light, 12 h dark) to promote sporulation at
teren & Loer., Trans. Brit. Mycol. Soc. 77: 61. 1981. 25 °C.
Diploplenodomus Diedicke, Ann. Mycol. 10: 140. 1912.
Plectophomella Moesz, Magyar Bot. Lapok 21: 13. 1922. Distribution: Worldwide.
Apocytospora Höhn., Mitt. Bot. Lab. TH Wien 1: 43. 1924.
Deuterophoma Petri, Boll. R. Staz. Patalog. Veget. Roma 9: 396. Hosts: As pathogens of herbaceous plants in different families,
1929. most records refer to Asteraceae, and on leaves, branches,
For Additional synonyms of the asexual morph and sexual morph bark, wood and dead stems of various trees and shrubs of
genera listed below see Boerema et al. (1994) and Khashnobish Brassicaceae, Lamiaceae, Rutaceae, Salicaceae and Vita-
et al. (1995), respectively. ceae. In addition, some Plenodomus species are found as
opportunistic or pathogenic fungi on Apiaceae, Bignoniaceae,
Classification: Dothideomycetes, Pleosporomycetidae, Pleo- Caprifoliaceae, Fabaceae, Rosaceae, Ulmaceae and
sporales, Leptosphaeriaceae. Umbelliferae.
Type species: Plenodomus lingam (Tode: Fr.) Höhn. Represen- Disease symptoms: Leaf spots, stem lesions, slow wilt, bark
tative strains: CBS 532.66 and CBS 475.81. canker, root rot, shoot dieback.
182
GENERA OF PHYTOPATHOGENIC FUNGI
0.03
Fig. 49. RAxML phylogram obtained from LSU (883 bp) sequences of Dothideomycetes. RAxML bootstrap support (BS) values above 70 % and Bayesian posterior probability scores
0.95 are shown at the nodes. The tree was rooted to Botryosphaeria dothidea CBS 115476, Neofusicoccum parvum CBS 124491 and Saccharata proteae CBS 115206. Numbers
between parentheses correspond to GenBank accession numbers. T, ET, NT and PT indicate ex-type, ex-epitype, ex-neotype and ex-paratype, respectively. TreeBASE: S20877.
www.studiesinmycology.org 183
MARIN-FELIX ET AL.
Fig. 50. Phylogenetic tree resulting from a Bayesian analysis of the combined LSU and ITS sequences alignment of Pleiochaeta species. Bayesian posterior probabilities >0.95
are indicated at the nodes. The tree was rooted to Thyrostroma compactum and Thyrostroma cornicola. Numbers between parentheses correspond to GenBank accession
numbers of ITS and LSU, respectively. T and ET indicate ex-type and ex-epitype strains, respectively. *, ITS and LSU sequences. TreeBASE: S20877.
Fig. 51. Reproduction of the original drawings by Kirchner (1892) illustrating Ceratophorum setosum (original numbers are maintained to indicate the different structures). A. fig.
1. Symptoms in Cytisus capitatus. B. fig. 2. Young conidia. C. fig. 3. Conidiophores and conidia. D, E. figs 4, 5. Conidia. F. fig. 6. Germinating conidia.
184
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 52. Plenodomus spp. A. Symptoms of stem canker of Plenodomus biglobosa. B, C. Section through ascomata. B. Plenodomus guttulatus (holotype MFLU 15-1876). C.
Plenodomus salviae (holotype MFLU 15-0515). D–G. Asci. D, E. Plenodomus guttulatus (holotype MFLU 15-1876); F, G. Plenodomus salviae (holotype MFLU 15-0515). H–K.
Ascospores. H, I. Plenodomus guttulatus (holotype MFLU 15-1876). J, K. Plenodomus salviae (holotype MFLU 15-0515). Scale bars: B = 75 μm; C = 25 μm; D–G, J,
K = 10 μm; H, I = 5 μm. Picture A taken from Fitt et al. (2008); B–K from Ariyawansa et al. (2015b).
Notes: The genus Plenodomus was first established by Preuss after 1 wk, margin regular, floccose, white, greyish brown near the
(1851), and recently re-introduced and placed in the family centre; reverse buff to amber. NaOH test negative.
Leptosphaeriaceae by de Gruyter et al. (2013). The genus
mainly consists of species that formerly belonged to Phoma Material examined: China, Yunnan, Dequin, isolated from soil,
section Plenodomus and the sexual morph Leptosphaeria. Ple- Apr. 2011, M.M. Wang (holotype HMAS 247058, culture ex-type
nodomus includes several well-known important plant patho- CGMCC 3.18221 = LC 5189).
gens, such as Plen. biglobosus, Plen. lindquistii, Plen.
tracheiphilus, and Plen. wasabiae. Notes: Plenodomus deqinensis was collected from soil on a
snow mountain in China, and proved able to grow at a low
References: Boerema et al. 2004 (morphology and pathoge- temperature (15 °C). This species clustered with Plen. agnitus,
nicity); de Gruyter et al. 2013, Ariyawansa et al. 2015b Plen. fallaciosus and Plen. lupini in the phylogenetic tree
(morphology and phylogeny). (Fig. 53). The NaOH test of Plen. deqinensis proved negative,
while in Plen. agnitus it was positive (Boerema et al. 1994).
Plenodomus deqinensis Q. Chen & L. Cai, sp. nov. MycoBank Morphologically, Plen. deqinensis differs from Plen. lupini in the
MB818821. Fig. 54. slightly wider conidiogenous cells (5–7 × 4–6.5 μm vs.
3–8 × 3–6 μm), and being conspicuously biguttulate (de Gruyter
Etymology: Named after the location where the holotype was et al. 1993). Plenodomus fallaciosus has hitherto only been
collected, Deqin, Yunnan Province in China. observed as a sexual morph.
Conidiomata pycnidial, solitary, globose to subglobose, glabrous, Authors: Q. Chen & L. Cai
superficial, (150–)165–355 × (105–)125–305 μm; ostiole sin-
gle, slightly papillate with a narrow pore or opening via a rupture; Protostegia Cooke, Grevillea 9: 19. 1880. Fig. 55.
conidiomatal wall pseudoparenchymatous, 3–6-layered,
16–28 μm thick, composed of isodiametric to oblong cells, outer Classification: Dothideomycetes, Dothideomycetidae, Capno-
layer brown. Conidiophores reduced to conidiogenous cells. diales, Mycosphaerellaceae.
Conidiogenous cells phialidic, hyaline, smooth, ampulliform,
5–7 × 4–6.5 μm. Conidia ellipsoidal-cylindrical, smooth- and Type species: Protostegia eucleae Kalchbr. & Cooke. Slide ho-
thin-walled, aseptate, 3.5–5.5 × 1.5–2.5 μm, with 2 minute polar lotype: IMI 230771. Epitype and ex-epitype cultures: PREM
guttules. Conidial exudates not recorded. Sexual morph not 60879, CPC 23549 = CBS 137232.
observed.
DNA barcode (genus): LSU.
Culture characteristics: Colonies on OA 35 mm diam after 1 wk,
margin regular, floccose, white, pale grey near the centre; reverse DNA barcode (species): ITS. Table 16.
white to slightly pale olivaceous. Colonies on MEA 17–23 mm
diam after 1 wk, margin irregular, aerial mycelia sparse, pale Sexual morph unknown. Conidiomata pycnidial, immersed,
green; reverse concolourous. Colonies on PDA 25–27 mm diam becoming somewhat erumpent, solitary, exuding a mucoid
www.studiesinmycology.org 185
MARIN-FELIX ET AL.
conidial cirrhus, pale brown, splitting the leaf surface, with various Euclea spp. However, Euclea is widespread
central ostiole; conidiomatal wall brown, textura intricata. Co- throughout Africa, and therefore Protostegia may be more
nidiophores reduced to conidiogenous cells. Conidiogenous widespread than currently known. Protostegia was introduced
cells hyaline, smooth, lining the inner cavity, lageniform to by Kalchbrenner & Cooke (1880) in order to accommodate
subcylindrical, proliferating percurrently at apex. Conidia hya- Stegia magnoliae and the new species Pr. eucleae, and then
line, smooth, scolecosporous, euseptate (adapted from Crous four more species were allocated in this genus. However,
et al. 2015a). Dyko et al. (1979) transferred three of these species to other
genera and another two species were rejected as doubtful.
Culture characteristics: Colonies erumpent, slow growing, with Therefore, only the type species Pr. eucleae was retained and
uneven or lobate, feathery margins and sparse to moderate until now this genus has remained monotypic. Protostegia is
aerial mycelium. On MEA surface and reverse greyish sepia or characterised by immersed conidiomata with walls of textura
surface pale olivaceous grey and reverse olivaceous grey; on intricata, splitting the epidermis and appearing acervular, but
OA surface mouse-grey or pale olivaceous grey, reverse oliva- having a well-developed ostiole (Dyko et al. 1979). Recently
ceous grey; on PDA surface greyish sepia or pale olivaceous Pr. eucleae was placed in the Mycosphaerellaceae together
grey, reverse mouse-grey or olivaceous grey. with Cytostagonospora martiniana and Phaeophleospora spp.
on the basis of phylogenetic analysis of ITS and LSU se-
Optimal media and cultivation conditions: PNA incubated at quences (Crous et al. 2015a). Cytostagonospora martiniana
25 °C under continuous near-ultraviolet light to promote can be distinguished from Protostegia by having percurrent
sporulation. and polyphialidic conidiogenous cells, and solitary to aggre-
gated conidiomata embedded in stromatic tissue (Quaedvlieg
Distribution: South Africa. et al. 2013). Phaeophleospora differs by the production of
pigmented conidiogenous cells and conidia (Crous et al.
Hosts: Euclea divinorum, E. lanceolata, E. natalensis, 2009b).
E. racemosa and E. undulata.
References: Dyko et al. 1979 (morphology); Crous et al. 2015a
Disease symptoms: Leaf spots. (morphology and phylogeny).
Notes: The genus Protostegia is thus far only known from Protostegia eucleicola Crous, sp. nov. MycoBank MB820822.
South Africa, where it has been reported from leaves of Fig. 55.
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GENERA OF PHYTOPATHOGENIC FUNGI
CBS 381.67
. Plenodomus lindquistii
74
100.0
Fig. 53. Phylogenetic tree generated from a maximum parsimony analysis based on the combined LSU, ITS, tub2 and rpb2 sequences. Values above the branches represent
parsimony bootstrap support values (> 50 %). Novel species are shown in bold. The tree is rooted with Leptosphaeria doliolum CBS 505.75. GenBank accession numbers are
listed in Table 15. T and ET indicate ex-type and ex-epitype strains, respectively. TreeBASE: S21048.
Etymology: Name refers to the host genus it was isolated from, inner cavity, lageniform to subcylindrical, 8–10 × 4–5 μm,
Euclea. proliferating percurrently at apex. Conidia hyaline, smooth,
curved, guttulate, apices subacutely rounded, basal cell tapering
Conidiomata epiphyllous on living leaves, erumpent, solitary, not to a truncate hilum, 1.5–2 μm diam, 3–7-septate, (40–)
associated with leaf spots, exuding a mucoid conidial cirrhus that 50–70(–75) × (2.5–)3–4 μm.
dries to a hard, dark brown crystalline droplet on the leaf surface,
up to 250 μm diam, immersed, pale brown, splitting the leaf Culture characteristics: Colonies erumpent, slow growing, with
surface, with central ostiole, 10–30 μm diam; conidiomatal wall lobate, feathery margins and sparse aerial mycelium; on MEA
brown, textura intricata. Conidiophores reduced to con- surface and reverse greyish sepia; on OA surface mouse-grey;
idiogenous cells. Conidiogenous cells hyaline, smooth, lining the on PDA surface greyish sepia, reverse mouse-grey.
www.studiesinmycology.org 187
MARIN-FELIX ET AL.
Fig. 54. Plenodomus deqinensis (ex-type CGMCC 3.18221). A, B. Colony on OA (front and reverse). C, D. Colony on MEA (front and reverse). E, F. Colony on PDA (front and
reverse). G, H. Pycnidia. I. Section of pycnidium. J. Section of pycnidial wall. K–M. Conidiogenous cells. N. Conidia. Scale bars: G, H = 50 μm; I = 10 μm; J–M = 5 μm;
N = 10 μm.
Material examined: South Africa, Western Cape Province, Classification: Sordariomycetes, Sordariomycetidae, Magnapor-
Porcupine Hills wine farm, between Botrivier and Villiersdorp, on thales, Pyriculariaceae.
Euclea racemosa, 29 Dec. 2014, A.R. Wood (holotype CBS H-
23110, culture ex-type CPC 27224 = CBS 142615). Type species: Pseudopyricularia kyllingae Klaubauf et al. Holo-
type and ex-type culture: CBS H-21841, CBS 133597.
Notes: With the description of Pr. eucleicola, the genus is
presently known from only two species. Protostegia eucleae DNA barcodes (genus): LSU, rpb1.
[conidia (40–)50–75(–80) × (2–)2.5–3 μm] is morphologically
similar to Pr. eucleicola [conidia (40–)50–70(–75) × (2.5–) DNA barcodes (species): ITS, rpb1, act, cal. Table 17. Fig. 57.
3–4 μm], although the conidia are slightly wider in the latter. The
two species are best distinguished based on their DNA data. It is Sexual morph unknown. Conidiophores solitary, erect, straight or
possible that many collections originally reported as Pr. eucleae, curved, branched or not, medium brown, smooth or finely rough-
actually represent Pr. eucleicola. ened, septate. Conidiogenous cells integrated, terminal, rarely
intercalary, medium brown, smooth or finely roughened, forming a
Authors: Y. Marin-Felix, A.R. Wood & P.W. Crous rachis with several protruding denticles usually flat-tipped. Conidia
solitary, obclavate, pale to medium brown, smooth or/to finely
Pseudopyricularia Klaubauf et al., Stud. Mycol. 79: 109. 2014. roughened, guttulate, 1–2-septate; hila truncate, slightly protrud-
Fig. 56. ing, unthickened, not darkened (adapted from Klaubauf et al. 2014).
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GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 55. A–E. Protostegia eucleadicola (ex-type CBS 142615). A, B. Conidiomata on leaf and OA, respectively. C. Conidiogenous cells. D, E. Conidia. F–N. Protostegia
eucleae (ex-epitype CBS 137232). F. Leaf symptoms. G. Close-up of conidiomata in vivo. H. Vertical section through conidioma. I–K. Conidia. L. Colony on MEA. M.
Conidiogenous cells. N. Conidia in vitro. Scale bars: A, B, G = 250 μm, H = 60 μm, L = 5 mm, all others = 10 μm. Pictures G–N taken from Crous et al. (2015a).
Culture characteristics: Colonies smooth with sparse to mod- Distribution: Mainly found in Asia, but also in North America,
erate aerial mycelium. On MEA transparent, buff, honey to Africa and New Zealand.
isabelline or white with patches of greyish sepia. On OA
transparent sometimes with patches of olivaceous grey or Hosts: Pathogens of Cyperaceae, but also found on Bothriochloa
greyish sepia. On PDA transparent, white, greyish sepia or bladhii (Poaceae) and Typha orientalis (Typhaceae).
olivaceous black.
Disease symptoms: Leaf spots.
Optimal media and cultivation conditions: Sterile barley seed on
SNA at 25 °C under continuous near-ultraviolet light to promote Notes: Pseudopyricularia was one of the genera introduced
sporulation. recently in order to resolve the polyphyletic nature of
www.studiesinmycology.org 189
MARIN-FELIX ET AL.
Table 16. DNA barcodes of accepted Protostegia spp. DNA barcode (species): ITS (evidence for intraspecific and intra-
isolate diversity), LSU. Table 18. Fig. 59.
Species Isolates1 GenBank accession References
numbers2 Spermogonia dark brown to black, often on adaxial leaf surface,
ITS LSU subepidermal, concave hymenia with well-developed periphyses
at ostiole [Group V, type 4 sensu Hiratsuka & Hiratsuka (1980)].
Protostegia CBS 137232ET KR873252 KR873280 Crous et al.
eucleae (2015a)
Spermatia exuded in droplets, small, aseptate, hyaline. Aecia
Pr. eucleicola CBS 142615T KY905668 KY905662 Present study erumpent, usually abaxial, cup-shaped, with well-developed
1 peridium; peridial cells irregular and verrucose. Aeciospores cat-
CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands. T and ET
indicate ex-type and ex-epitype strains, respectively. enulate, globose to subglobose, verruculose. Uredinia subepi-
2
ITS: internal transcribed spacers and intervening 5.8S nrDNA; LSU: partial 28S dermal or erumpent, on both leaf surfaces and stems, without
large subunit RNA gene. peridium, pale yellow to brown. Paraphyses either absent, pe-
ripheral or within the sorus. Urediniospores borne singly on pedi-
cels, mostly echinulate, usually globose, subglobose, ellipsoid to
Pyricularia (Klaubauf et al. 2014). Pseudopyricularia is mainly obovoid, germ pores absent or conspicuous. Telia subepidermal or
distinguished from Pyricularia by having short, determinate, erumpent, mostly dark brown to black, on both leaf surfaces and
brown conidiophores with an apical rachis with flat-tipped stems. Teliospores typically 2-celled by transverse or oblique septa
denticles. (but may have variations of 1–4 cells in some species), borne
singly on pedicels, mostly pale to dark brown, cell walls smooth or
Reference: Klaubauf et al. 2014 (morphology and phylogeny). ornamented. Basidia transversely septate (phragmobasidia), 2–4
celled, external. Basidiospores formed singly from each basidial
Pseudopyricularia bothriochloae (Crous & Cheew.) Y. Marín & cell on a sterigma, sometimes ballistosporic.
Crous, comb. nov. MycoBank MB819002.
Basionym: Pyricularia bothriochloae Crous & Cheew., Persoonia Distribution: Worldwide.
31: 229. 2013.
Hosts: Species of Puccinia are obligate plant pathogens that
Notes: This fungus was initially described as a new species of occur on host species in many families, especially Asteraceae,
Pyricularia (Crous et al. 2013b) before Klaubauf et al. (2014) Cyperaceae, Fabaceae, Lamiaceae, Liliaceae s. lat., Malvaceae
introduced the new genus Pseudopyricularia. In the latter and Poaceae. Heteroecious species of Puccinia, e.g. Pu. gra-
study, this species was incorporated in the phylogenetic analysis minis, require two host plant species to complete their life cycle.
based on LSU sequence data, but not in the combined analysis, The spermogonia and aecia of heteroecious species occur on
since only ITS and LSU sequences were available. Although the one host species, while the uredinia and telia occur on another,
ex-type strain of Py. bothriochloae grouped in the Pseudopyr- often unrelated, host species. Autoecious species complete their
icularia clade, a new combination was not proposed, as it could life cycle on one host species. There are many variations in the
not be incorporated in the combined analysis. However, in the life cycles of species of Puccinia. For example, some species,
phylogenetic tree based on ITS and LSU sequences (Fig. 57), e.g. Pu. lagenophorae, do not form spermogonia or uredinia.
Py. bothriochloae was located in the Pseudopyricularia clade Other species are known only from their telia, or telia and
(100 % bootstrap support / 1 Posterior Probability) and accord- spermogonia, e.g. Pu. malvacearum and Pu. grevilleae.
ingly the new combination, Py. bothriochloae, is made here. This Frequent host jumps in the evolution of Puccinia and related
species produces conidiophores with apical rachis with flat- genera have resulted in closely related species of Puccinia
tipped denticles with periclinal thickening, which characterises across wide host ranges, as well as distantly related species that
Pseudopyricularia spp. occur on the same host plant species (Maier et al. 2007, van der
Pseudopyricularia spp. are mainly pathogens of Cyperaceae. Merwe et al. 2008, Dixon et al. 2010, McTaggart et al. 2016a).
However, this species was found on Bothriochloa bladhii (Poa-
ceae), producing angular leaf spots. Morphologically, Py. Disease symptoms: Spermogonia, aecia (Fig. 58A, B), uredinia
bothriochloae can be easily distinguished by the 1-septate (Fig. 58C, G) and telia (Fig. 58H, I) occur on leaves and stems,
conidia (2-septate in all the other species). often associated with chlorotic lesions, sometimes on bullate
swellings, solitary or scattered or aggregated in groups, arranged
Authors: Y. Marin-Felix & P.W. Crous linearly or concentrically or irregularly, often erumpent, in cases
of severe infection leaves prematurely wilt and senesce.
Puccinia Pers., Neues Mag. Bot. 1: 118. 1794. Fig. 58.
For synonyms see Cunningham (1931). Notes: The starting publication for names of all rust fungi for
purposes of priority as provided by Art. 13 of the International
Classification: Basidiomycota, Pucciniomycotina, Pucciniomy- Code of Nomenclature for algae, fungi, and plants (ICN)
cetes, Pucciniales, Pucciniaceae. (McNeill et al. 2012) is the Synopsis Methodica Fungorum by
Persoon (1801), who listed 11 species of Puccinia, 19 species of
Type species: Puccinia graminis Pers. Designated as type Aecidium and 30 species of Uredo. The genera Aecidium,
species of Puccinia by Cunningham (1931) on cultivated Triti- Uredo and Puccinia were established for rust fungi with aecia,
cum; lectotypified by Jørstad (1958). uredinia and telia, respectively. Many species described in these
three genera are conspecific, e.g. the lectotype of Aecidium
DNA barcodes (genus): ITS, LSU. berberidis designated by Clements & Shear (1931) is the aecial
190
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 56. Pseudopyricularia spp. A. Sporulation of Pseudopyricularia kyllingae (ex-type CBS 133597) on sterile barley seed on SNA. B. Sporulation of Pseudopyricularia
bothriochloae (ex-type CBS 136427) on PNA. C–G. Conidiophores. C. Pseudopyricularia hagahagae (ex-type CPC 25635). D. Pseudopyricularia cyperi (ex-type CBS 133595).
E. Pseudopyricularia bothriochloae (ex-type CBS 136427). F. Pseudopyricularia hagahagae (ex-type CPC 25635). G. Pseudopyricularia kyllingae (ex-type CBS 133597). H–K.
Conidia. H. Pseudopyricularia cyperi (ex-type CBS 133595). I. Pseudopyricularia bothriochloae (ex-type CBS 136427). J. Pseudopyricularia hagahagae (ex-type CPC 25635).
K. Pseudopyricularia kyllingae (ex-type CBS 133597). Scale bars = 10 μm. Pictures A, D, G, H, K taken from Klaubauf et al. (2014); B, E, I taken from Crous et al. (2013b), C, F,
J taken from Crous et al. (2015e).
stage of Pu. graminis. There is little possibility that Aecidium and placement of Uromyces beticola, the lectotype of Uredo
Uredo (asexual genera) will displace Puccinia (sexual genus) (Laundon 1970). A taxonomic working group on the Basidio-
under Art. 57.2 of the ICN (McNeill et al. 2012). Whether Uredo mycota in 2011 recommended the use of Uredo for uredinial
is a synonym of Puccinia depends on the phylogenetic species that could not be assigned to a monophyletic sexual
www.studiesinmycology.org 191
MARIN-FELIX ET AL.
Fig. 57. RAxML phylogram obtained from the combined ITS (546 bp) and LSU (750 bp) sequences of members of Pyriculariaceae. The tree was rooted to Bussabanomyces
longisporus CBS 125232. The new combination proposed is indicated in bold. RAxML bootstrap support (BS) values above 70 % and Bayesian posterior probability scores
0.95 are shown at the nodes. Numbers between parentheses correspond to GenBank accession numbers of ITS and LSU sequences, respectively. T and NT indicate ex-type
and ex-neotype strains, respectively. TreeBASE: S20877.
genus (available at: http://www.imafungus.org/Issue/31/05.pdf). ITS region was found in Pu. horiana and Pu. kuehnii
Many species of Aecidium and Uredo will need to be transferred (Virtudazo et al. 2001, Alaei et al. 2009). Multiple haplotypes
to Puccinia, or other monophyletic genera, in order to preserve and paralogous copies of the ITS region within species of rust
the one name equals one fungus principle (Hawksworth et al. must be considered for phylogenetic and molecular barcode
2011). studies.
There are about 4 000 described species of Puccinia (Kirk Phylogenetic studies have identified several sexual genera as
et al. 2008), which have mostly been delimited by host taxon. potentially congeneric with Puccinia. Puccinia is either para-
Many of these species have diversified in the last 50 million phyletic or polyphyletic with respect to Ceratocoma (McTaggart
years as a result of host jumps (McTaggart et al. 2016b), with et al. 2016b), Cumminsiella (Maier et al. 2003), Dietelia
the aecial host serving as a pathway for further speciation (van (Wingfield et al. 2004), Diorchidium (Beenken & Wood 2015),
der Merwe et al. 2008). The morphology of teliospores and Endophyllum (Maier et al. 2003), Macruropyxis (Beenken &
urediniospores is often sufficient to distinguish species of Wood 2015), Miyagia (Wingfield et al. 2004), Sphenospora
Puccinia that occur on the same host. Molecular approaches (Aime 2006) and Uromyces (Maier et al. 2003). Three major
have uncovered cryptic diversity in some species of Puccinia clades that contained Puccinia and related genera were identi-
(Liu & Hambleton 2013) as well as linking aecial to telial fied in molecular phylogenetic studies (van der Merwe et al.
morphs in the life cycles of heteroecious rusts (Jin et al. 2010). 2008, Dixon et al. 2010). One clade diversified on Cyper-
Other studies have shown there is less species biodiversity in aceae, Juncaceae and orders of plants in the asterids and rosids
some rusts than previously thought, e.g. Pu. lagenophorae (The Angiosperm Phylogeny 2016), and the another on Poaceae
and closely related species (Scholler et al. 2011, McTaggart and Ranunculaceae (van der Merwe et al. 2008). A third clade
et al. 2014). Intraspecific and intra-isolate diversity of the included species of Puccinia on Poaceae (Dixon et al. 2010). The
192
GENERA OF PHYTOPATHOGENIC FUNGI
Fig 58. Puccinia spp. A, D. Aecia and aeciospores of Puccinia paederiae (BRIP 58338). B, E. Aecia and aeciospores of Puccinia loranthicola (BRIP 59685). C, F. Uredinia and
urediniospores of Puccinia oxalidis (BRIP 58379). G, J. Uredinia and urediniospores of Puccinia philippinensis (BRIP 57418). H, K. Telia and teliospores of Puccinia mal-
vacearum (BRIP 60128). I, L. Telia and teliospores of Puccinia thwaitesii (BRIP 58354). Scale bars = 10 μm.
www.studiesinmycology.org 193
MARIN-FELIX ET AL.
194
GENERA OF PHYTOPATHOGENIC FUNGI
relationships between the major clades in Puccinia can be phylogenetic taxonomic concept, we have transferred four spe-
observed in our phylogenetic analysis (Fig. 59). cies of Uredo from the Australasian region to Puccinia. Further
Uromyces requires particular consideration as it has long examples of taxa recovered in Puccinia, include Aecidium
been thought an aseptate variant of Puccinia (Sydow & Sydow kalanchoe (Hernadez et al. 2004) and Uredo guerichiani (Maier
1904, Savile 1978). Morphology alone does not reliably sepa- et al. 2007). We have chosen not to make new combinations of
rate Puccinia and Uromyces, because puccinioid (2-celled) and these species without examination of a specimen. Molecular
1-celled spores and characteristics of the pedicel are homo- phylogenetic support must be an essential requirement for the
plasious in the Pucciniales (Maier et al. 2007, Minnis et al. description of new species or new combinations in Puccinia
2012, Beenken & Wood 2015). Several studies have shown because several species known from an anamorphic stage have
that Puccinia and Uromyces are polyphyletic, and furthermore an affinity with other genera of rust fungi, e.g. Uredo rolliniae
that Puccinia is paraphyletic with respect to the type of Uro- (now Phakopsora rolliniae) (Beenken 2014).
myces (U. appendiculatus) and other species of Uromyces on ITS and LSU sequences are available for approximately 200
Fabaceae (Maier et al. 2007, van der Merwe et al. 2008). species of Puccinia on GenBank (accessed 5 Sep. 2016).
Consequently, either a taxonomy that accepts Puccinia as a These two gene regions are generally reliable as a molecular
paraphyletic group must be adopted or Uromyces must be barcode for identification of species of Puccinia. GenBank
synonymised under Puccinia. In the latter case, many important numbers for some of the most important species of Puccinia
species of Uromyces will require name changes. The traditional that are associated with a herbarium specimen, reference
use of Uromyces for species with aseptate teliospores has genome sequence, or peer reviewed study, are provided in
been replaced by a phylogenetic approach; for example, Table 18.
Demers et al. (2017) used a phylogenetic approach to describe
two species of Puccinia with aseptate teliospores, which would References: Sydow & Sydow 1904 (morphology); Cummins &
have been described as Uromyces based on morphology. Hiratsuka 2003 (biology, morphology and taxonomy).
The future of Puccinia depends on whether it can be divided
into monophyletic genera or sub-genera that reflect synapo- Puccinia dianellae (Dietel) McTaggart & R.G. Shivas, comb.
morphies or ecological relationships on which a natural classi- nov. MycoBank MB819750.
fication can be based. A broad concept of Puccinia that accepts Basionym: Uredo dianellae Dietel, Hedwigia 37: 213. 1898.
species with puccinioid spores that are recovered in closely
related clades as defined by van der Merwe et al. (2008) and Material examined: Philippines, Benguet, Tuba, Mount Santo
Dixon et al. (2010) is adopted here. Based on this molecular Tomas, on Dianella javanica, 26 Jun. 2012, K.L. Lancetta, V.A.
www.studiesinmycology.org 195
MARIN-FELIX ET AL.
Felices, T.U. Dalisay, A.I. Llano, A.R. McTaggart, R.G. Shivas & Notes: Puccinia rhagodiae was recovered in Puccinia group I
M.D.E. Shivas (BRIP 57433). sensu van der Merwe et al. (2008). Telia have not been reported.
Several other species of Puccinia on Amaranthaceae were
Notes: Puccinia dianellae was recovered in a monophyletic shown to be closely related, including Pu. arthrocnemi, Pu.
group with species of Puccinia on Hemerocallidaceae bassiae and Pu. tetragoniae, although they did not form a
(McTaggart et al. 2016a). Telia have not been reported. monophyletic group. Morphological identification of Pu. rhago-
diae can be assisted by the Rust Fungi of Australia Lucid Key
Puccinia geitonoplesii (McAlpine) McTaggart & R.G. Shivas, (Shivas et al. 2014) (http://collections.daff.qld.gov.au/web/key/
comb. nov. MycoBank MB819751. rustfungi/).
Basionym: Uredo geitonoplesii McAlpine, The Rusts of
Australia, their Structure, Nature and Classification: 203. 1906. Authors: A.R. McTaggart & R.G. Shivas
Material examined: Australia, Queensland, Coochiemudlo Is- Saccharata Denman & Crous, CBS Biodiversity Ser. (Utrecht) 2:
land, Victoria Parade, on leaf of Geitonoplesium cymosum, 25 104. 2004. Fig. 60.
Aug. 2012, C. Doungsa-ard & A.R. McTaggart (BRIP 57603).
Classification: Dothideomycetes, Incertae sedis, Botryosphaer-
Notes: Puccinia geitonoplesii was recovered in a monophyletic iales, Saccharataceae.
group with species of Puccinia on Hemerocallidaceae
(McTaggart et al. 2016a). Telia have not been reported. Type species: Saccharata proteae (Wakef.) Denman & Crous.
Morphological identification of P. geitonoplesii can be assisted by Holotype and ex-type culture: PREM 32915, STE-U 1694.
the Rust Fungi of Australia Lucid Key (Shivas et al. 2014) (http://
collections.daff.qld.gov.au/web/key/rustfungi/). DNA barcode (genus): LSU.
Puccinia merrilliana (Syd. & P. Syd.) McTaggart & R.G. Shivas, DNA barcodes (species): ITS, rpb2, tef1, tub2. Table 19.
nom. nov. MycoBank MB819752.
Basionym: Uredo operculinae Syd. & P. Syd., Philipp. J. Sci., C, Ascomata epiphyllous, separate, becoming aggregated, uniloc-
Bot. 8: 476. 1913. ular, immersed, substomatal, with a central, flattened ostiole,
surrounded by a continuous, clypeus-like apical thickening of the
Material examined: Australia, Western Australia, Kununurra, wall, obovoid, slightly depressed; ascomata wall consisting of
Ivanhoe Crossing turnoff, on leaf of Operculina aequisepala, 16 8–11 layers of brown pseudoparenchymatous textura angularis.
Apr. 2012, M. Butt, C. Doungsa-ard, A.R. McTaggart, R. Berndt, Pseudoparaphyses hyaline, septate, branched, frequently
V. Faust-Berndt, M.D.E. Shivas & R.G. Shivas (BRIP 56913). attached to the top and base of the pseudothecial cavity. Asci
clavate to cylindrical, stipitate, bitunicate, fissitunicate; apical
Notes: Uredo operculinae was first described on Operculina chamber visible as a notch-like indentation at the apex. Asco-
turpethum from the Philippines (Sydow & Sydow 1913). The spores uni- to biseriate, hyaline, guttulate, smooth, ellipsoidal,
transfer of U. operculinae to Puccinia requires a new name, clavate to fusiform, frequently widest in the upper third of the
Pu. merrilliana, as Pu. operculiniae is already occupied for a ascospore, tapering to obtuse ends. Conidiomata pycnidial,
rust on O. turpethum in the Malabar region in southern India black, opening by a single, central ostiole, infrequently
(Ramakrishnan & Sundaram 1953). The new name honours embedded in stromatic tissue with thickened, darkened upper
Elmer Drew Merrill (1876‒1956), an American botanist, who layer; conidiomatal wall consisting of 2–3 layers of brown textura
collected this fungus while living in the Philippines, where he angularis. Conidiophores hyaline, smooth, subcylindrical,
became an expert on the flora of the Asia-Pacific region. branched, or reduced to conidiogenous cells, lining the inner
Puccinia merrilliana has fewer (1‒2) germ pores than Pu. layer of the cavity, 1–3-septate. Paraphyses intermingled among
operculinae, which has 3‒4 germ pores. Telia have not been conidiophores, hyaline, smooth, subcylindrical, unbranched or
reported for Pu. merrilliana. The specimens examined from branched above, with obtuse ends, 0–3-septate, extending
Australia are morphologically identical to the type description above conidiophores or slightly above the conidia. Con-
by Sydow & Sydow (p. 425, 1924). Morphological identification idiogenous cells hyaline, smooth, phialidic, proliferating via per-
of Pu. merrilliana can be assisted by the Rust Fungi of iclinal thickening or percurrent proliferation, with or without
Australia Lucid Key (Shivas et al. 2014) (http://collections.daff. collarettes. Conidia hyaline, smooth, thin-walled, aseptate,
qld.gov.au/web/key/rustfungi/). Puccinia merrilliana was granular, fusiform to narrowly ellipsoid or fusoid-ellipsoid, apex
recovered in Puccinia in Group I sensu van der Merwe et al. subobtuse, base subtruncate or truncate with minute marginal
(2008). frill, widest in the middle of the conidium. Synasexual morph
formed in separate conidiomata, or in same conidiomata with
Puccinia rhagodiae (Cooke & Massee) McTaggart & R.G. asexual morph. Synasexual conidia pigmented, thick-walled,
Shivas, comb. nov. MycoBank MB819756. finely verruculose, ellipsoid or oval, aseptate. Spermatogonia
Basionym: Uredo rhagodiae Cooke & Massee, Grevillea 15 (no.
similar to conidiomata in anatomy. Spermatogenous cells
76): 99. 1887.
ampulliform to lageniform or subcylindrical, hyaline smooth,
phialidic. Spermatia developing in conidiomata or spermato-
Material examined: Australia, Tasmania, Lilico Beach, on leaf of
gonia, hyaline, smooth, granular, subcylindrical or dumbbell-
Chenopodium candolleanum, 15 Dec. 2013, A.R. McTaggart,
shaped, with rounded ends (adapted from Crous et al. 2004a
L.S. Shuey, M.D.E. Shivas & R.G. Shivas (BRIP 60078).
and Slippers et al. 2013).
196
GENERA OF PHYTOPATHOGENIC FUNGI
Culture characteristics: Colonies on PDA, OA and MEA percurrent proliferations. Conidia hyaline, smooth, fusiform to
spreading, with moderate aerial mycelium, usually erumpent, narrowly ellipsoid, apex subobtuse, base truncate with minute
less frequent flat, margins irregular; surface and reverse show marginal frill, minutely guttulate, thin-walled, (13–)
different shades of grey. 14–16(–19) × (4–)4.5(–5) μm.
Optimal media and cultivation conditions: On OA or PNA at Culture characteristics: Colonies on MEA at 25 °C in the dark
25 °C under continuous near-ultraviolet light to promote after 1 wk: spreading, erumpent, surface crumpled, irregular, with
sporulation. uneven, feathery margin and moderate aerial mycelium; surface
pale mouse-grey, reverse mouse-grey.
Distribution: Commonly found in South Africa, but also Australia,
North America (incl. Hawaii) and Europe. Material examined: South Africa, Western Cape Province,
Kogelberg Nature Reserve, on leaf litter of Leucospermum
Hosts: Members of Proteaceae, especially in species of Banksia, conocarpodendron subsp. viridum, 11 Jul. 2000, S. Marincowitz
Hakea, Isopogon, Lambertia, Leucospermum, Petrophile and (holotype CBS H-20078, culture ex-type CBS 122694 = CPC
Protea. Also found on Daviesia (Fabaceae), Encephalartos 13698 = CMW 22197).
(Zamiaceae), and Eucalyptus (Myrtaceae) (see Crous et al.
2016b). Notes: In the treatment of microfungi occurring on leaf litter of
Proteceae, Marincowitz et al. (2008a) listed CBS 122694 as a
Disease symptoms: Leaf tip die-back and leaf spots. Saccharata sp., acknowledging the fact that it appeared to be
different. Three other species are known from Protea leaves in
Notes: Saccharata is the only genus located in the family South Africa, namely S. proteae (conidia 20–30 × 4.5–6 μm;
Saccharataceae, which was recently introduced by Slippers Denman et al. 1999), S. intermedia [conidia (17–)
et al. (2013). This genus was described by Crous et al. 18–20(–22) × (3.5–)5–6 μm; Crous et al. 2009a], and
(2004a) in order to accommodate “Botryosphaeria” proteae, S. hawaiiensis [conidia (17–)24–30(–38) × (4–)5–7(–8) μm;
and subsequently several additional species were added to the Yang et al. 2017]. Saccharata leucospermi can readily be
genus from South Africa. All the species were found on Pro- distinguished from these three species by having smaller conidia.
teaceae expect Saccharata kirstenboschensis, which was iso-
lated from Encephalartos princeps (Crous et al. 2008). South Saccharata protearum Crous, sp. nov. MycoBank MB820824.
African Saccharata spp. that occur on Proteaceae can be Fig. 62.
distinguished from other members of Botryosphaeriales by their
asexual morphology, which includes a hyaline, fusicoccum-like Etymology: Named after the host genus from which it was
and a pigmented diplodia-like asexual morph (Crous et al. collected, Protea.
2013a). However, Crous et al. (2016b) introduced eight spe-
cies from a range of hosts (Myrtaceae and Proteaceae) in Conidiomata pycnidial, eustromatic, to 400 μm diam, immersed,
Australia, and also widened the generic concept to include the subepidermal, erumpent in culture, separate, or aggregated,
genus Neoseptorioides (3-septate, cylindrical conidia; Crous linked by a stroma, dark brown, uni- to multi-locular, walls con-
et al. 2015e). In spite of the range of variation observed in sisting of dark brown textura angularis, ostiolate. Fusicoccum-
the asexual morphs, morphology of the sexual morphs of like asexual morph: Conidiophores hyaline, smooth, branched,
Australian and South African species appear remarkably subcylindrical, 1–3-septate, formed from the inner layer of the
conserved. locule, 10–30 × 2.5–3.5 μm, intermingled with hyaline, septate
paraphyses. Conidiogenous cells phialidic, discrete or integrated,
References: Crous et al. 2008, 2013a, 2016b (morphology and hyaline, smooth, cylindrical, enteroblastic, proliferating percur-
phylogeny). rently with 1–2 annellations, 9–15 × 2.5–3.5 μm. Conidia hya-
line, thin-walled, aseptate, smooth, fusoid, widest in the middle or
Saccharata leucospermi Crous, sp. nov. MycoBank upper third of the conidium, with a subobtuse apex, and a
MB820823. Fig. 61. truncate base, (17–)20–25(–27) × (4–)4.5–5(–6) μm. Micro-
conidial morph occurring in separate or the same conidiomata as
Etymology: Named for the host genus from which it was the fusicoccum-like asexual morph. Microconidiophores hyaline,
collected, Leucospermum. smooth, branched, cylindrical, 1–3-septate, formed from the
inner layers of the locule, 20–30 × 2.5–3 μm. Micro-
Conidiomata on PDA pycnidial, black, up to 300 μm diam, with conidiogenous cells phialidic, discrete or integrated, hyaline,
a single, central ostiole; conidiomatal wall consisting of 2–3 smooth, cylindrical, determinate, with prominent periclinal thick-
layers of brown textura angularis. Conidiophores sub- ening, 5–11 × 2–2.5 μm. Microconidia medium brown, thin-
cylindrical, hyaline, smooth, frequently reduced to con- walled, finely verruculose, guttulate, aseptate, subcylindrical to
idiogenous cells or branched in apical part, 1–2-septate, narrowly ellipsoid with rounded ends, (7–)10–15(–17) × (2.5–)
7–20 × 2–3.5 μm. Paraphyses rarely observed, intermingled 3(–4) μm.
among conidiophores, unbranched hyaline, smooth, 0–1-
septate, 2–3 μm wide, extending above conidiophores. Con- Culture characteristics: Colonies on MEA at 25 °C in the dark after
idiogenous cells terminal, subcylindrical, hyaline, 1 wk: flat, spreading, with moderate aerial mycelium; surface pale
7–10 × 2–3 μm, with periclinal thickening, rarely with mouse-grey with patches of dirty white, reverse mouse-grey.
www.studiesinmycology.org 197
MARIN-FELIX ET AL.
Fig 59. Phylogram obtained from a maximum likelihood search of LSU and cytochrome c oxidase subunit 3 of mitochondrial DNA (co3), partitioned as two separate genes in
RAxML. Bootstrap values ( 70 %) from 1 000 replicates in a maximum likelihood search shown above nodes. Posterior probabilities (0.95) summarised from 30 000 trees
obtained by Bayesian inference in MrBayes are shown below nodes. General time-reversible (GTR) with GAMMA distribution was used as a model of evolution for both
198
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 60. Saccharata spp. A. On Banksia sp. B. Symptomatic leaves of Saccharata proteae (CBS 121406). C. Close-up of subepidermal conidiomata of Saccharata proteae.
D–E. Sexual morph of Saccharata proteae (CBS 121406). D, E. Asci, paraphyses and ascospores. F–N. Asexual morphs. F. Colony sporulating on OA of Saccharata capensis
(ex-type CBS 122693). G. Pycnidial conidioma of Saccharata capensis (ex-type CBS 122693). H–J. Conidiogenous cells and conidia. H. Saccharata proteae (CBS 121406). I,
J. Saccharata capensis (ex-type CBS 122693). K–M. Conidia. K. Saccharata intermedia (ex-type CBS 125546). L. Saccharata kirstenboschensis (ex-type CBS 123537). M.
Saccharata proteae (CBS 121406). N. Spermatia of Saccharata capensis (ex-type CBS 122693). Scale bars: G = 100 μm, others = 10 μm; I applies to I, J. Pictures B–K, J–N
taken from Crous et al. (2013a); L from Crous et al. (2008).
phylogenetic criteria. Major clades of Puccinia obtained in previous studies are shaded. New combinations made in the present study are in bold. Two species of Sphaer-
ophragmiaceae were selected as outgroup to the Pucciniaceae. Numbers between parentheses correspond to GenBank accession numbers for LSU and co3 sequences,
respectively. The locus co3 was used as a second, independent gene in the phylogenetic analyses; however it is not regarded as a molecular barcode for species of Puccinia as
there are limited nucleotide differences between closely related species. TreeBASE: S21061.
www.studiesinmycology.org 199
MARIN-FELIX ET AL.
Material examined: USA, Hawaii, Maui, on leaf of Protea sp., 16 subcylindrical, 1–3-septate. Conidiogenous cells brown, sub-
Dec. 1998, P.W. Crous & M.E. Palm, (holotype CBS H-23111, cylindrical, finely roughened, proliferating percurrently at apex.
culture ex-type CPC 2169 = CBS 114569). Conidia cylindrical, clavate, or ellipsoid to fusoid, pale to me-
dium brown, smooth-walled, with (1–)4 transverse septa, and
Notes: In the reassessment of Botryosphaeriaceae and allied 0–3 oblique or longitudinal septa, rounded at the apex, base
taxa published by Marincowitz et al. (2008b), the ITS DNA data truncate.
could not distinguish CBS 114569 from isolates of S. proteae.
However, in the recent study of Yang et al. (2017), the combined Culture characteristics: Colonies reaching 90 mm diam after
sequence dataset (ITS, rpb2 and tef1), showed CBS 114569 to 2 wk, with sparse or fluffy aerial mycelium. Colonies on MEA,
cluster basal to S. hawaiiensis. Morphologically, conidia of iso- PDA and OA showing different shades of grey or chestnut to
lates of CBS 114569 [(17–)20–25(–27) × (4–)4.5–5(–6) μm] umber.
are also smaller than those of S. hawaiiensis [(17–)
24–30(–38) × (4–)5–7(–8) μm; Yang et al. 2017], and thus this Optimal media and cultivation conditions: MEA, PDA and OA at
isolate is herewith introduced as a new species, S. protearum. 25 °C.
Authors: Y. Marin-Felix, S. Marincowitz & P.W. Crous Distribution: Asia, Europe and North America.
Thyrostroma Höhn., Sitzungsber. Kaiserl. Akad. Wiss., Math.- Hosts: Pathogens of Ulmus spp., Sambucus caerulea, Styph-
Naturwiss. Cl., Abt. 1 120: 472 (94 repr.). 1911. Fig. 63. nolobium japonicum, Tilia spp., and Cornus officinalis.
Classification: Dothideomycetes, Pleosporomycetidae, Pleo- Disease symptoms: Thyrostroma canker, dieback and leaf spots.
sporales, Dothidotthiaceae.
Notes: Thyrostroma was introduced in 1911 in order to accom-
Type species: Thyrostroma compactum (Sacc.) Höhn. Holotype modate T. compactum (von Höhnel 1911). Despite being
could not be located, and a neotype from Europe is required. described more than 100 years ago, the phylogenetic position of
Thyrostroma remains unresolved. Thyrostroma was considered
DNA barcode (genus): LSU. the asexual morph of Dothidotthia by Phillips et al. (2008).
Subsequently, Slippers et al. (2013) placed Thyrostroma in the
DNA barcodes (species): ITS, tef1. Table 20. Fig. 64. Botryosphaeriaceae based on morphology, since molecular data
of Thyrostroma spp. were lacking. In the phylogenetic trees
Sexual morph unknown. Conidiomata sporodochial, punctiform, based on LSU sequences (Fig. 49), the type species of Thyro-
dark brown or black. Stroma immersed to superficial, brown. stroma, T. compactum, does not cluster with Dothidotthia
Conidiophores brown, finely roughened, cylindrical to (Dothidotthiaceae), demonstrating that these genera are not
200
GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 61. Saccharata leucospermi (ex-type CBS 122694). A. Conidiomata forming on OA. B, C. Conidiogenous cells giving rise to conidia. D. Conidia. Scale bars: A = 300 μm,
others = 10 μm.
Fig. 62. Saccharata protearum (ex-type CBS 114569). A. Conidiomata forming on OA. B, C. Conidiogenous cells giving rise to conidia. D. Conidia. Scale bars: A = 400 μm,
others = 10 μm.
congeneric, as was recently mentioned by Crous et al. (2016c). Material examined: USA, Nevada, Death Valley, on dead leaf
However, Thyrostroma did cluster in the Dothidotthiaceae clade, of Franseria sp., 7 Jul. 1970, F.W. Went (holotype CBS H-
as originally proposed by Phillips et al. (2008). 23112, culture ex-type CBS 487.71); Nevada, north end of
Death Valley, on green, living leaf of Franseria sp., Jul. 1970,
References: Ellis 1959, 1971, Crous et al. 2016c (morphology). F.W. Went, CBS H-18568, culture CBS 700.70.
Thyrostroma franseriae Crous, sp. nov. MycoBank Notes: Thyrostroma franseriae is known from two isolates, both
MB820825. Fig. 63. of which were collected from leaves of Franseria sp. in Death
Valley, Nevada (USA) in 1970. Morphologically, isolate CBS
Etymology: Named after the host genus from which it was 700.70 differs from CBS 487.71 in having larger conidia that
collected, Franseria. are more cylindrical, clavate to ellipsoid, with 2–4 transverse
septa, 2–8 oblique or longitudinal septa, 40–65 × 18–25 μm.
Sporodochia dark brown, punctiform, up to 250 μm diam. Stro- However, the two isolates are phylogenetically indistinguishable
mata brown, superficial, 100–150 μm diam. Conidiophores (Fig. 64).
brown, finely roughened, subcylindrical, 0–1-septate, Thyrostroma compactum is a European species originally
10–18 × 6–11 μm. Conidiogenous cells brown, subcylindrical, described from Ulmus in Italy. One such isolate was available for
finely roughened, proliferating percurrently at apex, study, namely CBS 335.37, collected by J.C. Carter (a US-based
5–10 × 6–11 μm. Conidia brown, ellipsoid to fusoid, with 2–4 researcher), but the origin of this strain remains unknown, and it
oblique or longitudinal septa, 1–3 transverse septa, apex broadly proved to be sterile in culture. Phylogenetically, however, CBS
obtuse, base truncate, 8–9 μm diam, (25–)28–33(–35) × (18–) 335.37 is distinct from T. franseriae (Fig. 64), although we could
20–25 μm. not confirm that CBS 335.37 is authentic for the name it was
deposited under by J.C. Carter.
Culture characteristics: Colonies flat, spreading, with sparse
aerial mycelium and feathery margins, reaching 60 mm diam Authors: Y. Marin-Felix & P.W. Crous
after 2 wk on MEA, PDA and OA; surface and reverse iron-grey.
www.studiesinmycology.org 201
MARIN-FELIX ET AL.
Fig. 63. A–H. Thyrostroma cornicola (ex-type CBS 141280). A, B. Symptomatic leaves of Cornus officinalis. C. Sporodochia on PNA. D. Sporulation on PNA. E–H. Con-
idiogenous cells giving rise to conidia. I–O. Thyrostroma franseriae (ex-type CBS 487.71). I. Sporulation on PNA. J–O. Conidiogenous cells giving rise to conidia. P. Conidia.
Scale bars: 20 μm. Pictures B–F, H taken from Crous et al. (2016c).
Venturia Sacc., Syll. fung. (Abellini) 1: 586. 1882. Fig. 65. Classification: Dothideomycetes, Pleosporomycetidae, Ventur-
Synonyms: Fusicladium Bonord., Handb. Mykol.: 80. 1851. iales, Venturiaceae.
Apiosporina Höhn., Sitzungsber. Kaiserl. Akad. Wiss., Math.-
Naturw. Cl., Abt. 1, 119: 439. 1910. Type species: Venturia inaequalis (Cooke) G. Winter. Type
Metacoleroa Petr., Ann. Mycol. 25: 332. 1927. material in Kew: IMI 47413.
Caproventuria U. Braun, A Monograph of Cercosporella,
Ramularia and Allied Genera (Phytopathogenic Hyphomycetes) DNA barcode (genus): LSU.
2: 396. 1998.
Pseudocladosporium U. Braun, A Monograph of Cercosporella, DNA barcodes (species): ITS, tef1, tub2. Table 21. Fig. 66.
Ramularia and Allied Genera (Phytopathogenic Hyphomycetes)
2: 392. 1998. Ascomata pseudothecial, globose, subglobose, black, initially
immersed, becoming erumpent, solitary, scattered or gregarious,
202
GENERA OF PHYTOPATHOGENIC FUNGI
100/-
100/1 CBS 159.51 (KY905671, KY905683)
Wilsonomyces carpophilus
CBS 231.89ET (KY905666, KY905684)
Fig. 64. RAxML phylogram obtained from the combined ITS (531 bp) and tef1 (389 bp) sequences of members of Dothidotthiaceae. The new species proposed is indicated in
bold. RAxML bootstrap support (BS) values above 70 % and Bayesian posterior probability scores 0.95 are shown in the nodes. Numbers between parentheses correspond
to GenBank accession numbers of ITS and tef1 sequences, respectively. T and ET indicate ex-type and ex-epitype strains, respectively. TreeBASE: S20877.
covered with setae; ostiole central, papillate; ascomatal wall and regular, but feathery margins. Colonies normally reaching
composed of a few layers of pigmented cells of textura angularis, not more than 15 mm diam after 1 mo on PDA at 25 °C in the
which is of equal thickness or slightly thickened at apex. dark.
Hamathecium comprising septate, filiform pseudoparaphyses,
evanescent in mature ascomata. Asci bitunicate, oblong to Optimal media and cultivation conditions: PDA, MEA and CMA.
obclavate, fissitunicate dehiscence unknown, with or without a Optimal growing temperature is 24–28 °C. Sometimes grows
short, thick pedicel, rounded at the apex with an inconspicuous faster after cold-shock under 10 °C for 1 wk.
ocular chamber. Ascospores obliquely uniseriate, partially over-
lapping to biseriate, especially at the base, ellipsoidal, with Distribution: Worldwide.
broadly rounded ends, pale brown, 1-septate, slightly constricted
at the septum, the upper cell shorter than the lower one, smooth- Hosts: Mainly on woody dicotyledonous plants. Twenty-four families
walled. Conidiophores single, sometimes arranged in small of plants have been reported hosting venturiaceous fungi, i.e.
groups, straight to flexuous, pale olivaceous to dark brown, Aceraceae, Amaryllidaceae, Asteraceae, Betulaceae, Caprifolia-
unbranched or occasionally branched, thin- to slightly thick- ceae, Cornaceae, Dipsacaceae, Ericaceae, Fagaceae, Gentiana-
walled, conidiophores often reduced to conidiogenous cells or ceae, Geraniaceae, Iridaceae, Juncaginaceae, Liliaceae,
composed of several cells. Conidiogenous nodes smooth to Onagraceae, Oleaceae, Polygonaceae, Ranunculaceae, Rham-
verruculose. Conidia in simple or branched acropetal chains, naceae, Rosaceae, Rubiaceae, Salicaceae, Sapindaceae and
ellipsoid-ovoid, obovoid, fusoid, obclavate-subcylindrical, canoe- Ulmaceae (Barr 1968, 1989, Sivanesan 1977). After studying a
shaped, straight to curved, subhyaline to medium brown, but large number of type materials of Venturia species, many have been
mostly olivaceous, thin- to thick-walled, smooth to verruculose, found to be representative of other genera (Shen et al. in prep.).
0–3(–4)-euseptate, germinating by production of germination
tubes from middle or polar cells; hila often denticle-like, some- Disease symptoms: Leaf spots, flower and fruit canker.
what protuberant, unthickened or almost so, occasionally
somewhat darkened-refractive; septum ontogeny: first septum Notes: Species of Venturia are widely distributed in the northern
median to sub-median. temperate region of the world, and are saprobic or parasitic on a
large variety of dicotyledonous plants. Venturia comprises 198
Culture characteristics: Colonies on PDA fuscous black, and species according to Index Fungorum. Based on the morphology
reverse dark fuscous-black, with moderate aerial mycelium of type specimens studied, the diagnostic characteristics of
www.studiesinmycology.org 203
MARIN-FELIX ET AL.
Fig. 65. Venturia spp. A–C. Disease symptoms. A. Symptoms caused by Venturia martianoffiana (HMAS 247008). B. Symptoms caused by Venturia catenospora (HMAS
247006). C. Symptoms caused by Venturia fuliginosa (HMAS 247007). D–O. Sexual morphs. D–F. Ascomata on the host. D. Venturia chinensis (HMAS 246485). E. Venturia
canadensis (NY 00914436). F. Venturia atriseda (K 189232). G–J. Asci. G. Venturia cephalariae (K 189236). H. Venturia chinensis (HMAS 246485). I. Venturia inaequalis (NY
00914442). J. Venturia asperata (PDD 31846). K–O. Ascospores. K. Venturia atriseda (K 189232). L. Venturia cephalariae (K 189236). M. Venturia carpophila (K 189234). N.
Venturia inaequalis (NY 00914442). O. Venturia helvetica (ZT 49111). P–T. Asexual morphs. P. Conidial chains of Venturia phaeosepta (ex-type CGMCC 3.18368). Q. Co-
nidiophores sporulation of Venturia inaequalis (CGMCC 3.18372). R. Conidia of Venturia inaequalis (CGMCC 3.18372). S. Fasciculate conidiophores of Venturia pyrina (HMAS
03923). T. Conidium of Venturia pyrina (HMAS 03923). Scale bars: D = 300 μm; E, F = 0.2 mm; G, H, J–M, Q, T = 10 μm; I, N, O, S = 5 μm; P, R = 20 μm.
Venturia are as follows: Ascomata immersed, semi-immersed or 1977). The genus is morphologically comparable to the
superficial, scattered or gregarious, often papillate and ostiolate Mycosphaerella morph of Ramularia in having bitunicate, oblong
with setae. Hamathecium narrowly cellular, hyaline, evanescent to obclavate asci with a short, thick pedicel or pedicel lacking,
in mature ascomata. Asci 8-spored, bitunicate, fissitunicate, ellipsoidal, 1-septate ascospores which are slightly constricted at
broadly cylindrical to obclavate, usually lacking a pedicel. As- the septum. However, Venturia can be distinguished from the
cospores pale olivaceous to brown, 1-septate, usually asym- sexual morph of Ramularia by its setose ascomata, pale oliva-
metrical. Morphological discrimination of the sexual morph is ceous to brown and asymmetrical ascospores. In addition,
limited, and the asexual morph is more informative (Sivanesan pseudoparaphyses are lacking in the sexual morph of Ramularia.
204
GENERA OF PHYTOPATHOGENIC FUNGI
Although several studies have been conducted on the phylogeny sometimes flexuous at the apex, unbranched or apically
of Venturia, they mostly relied on rDNA sequences of the ITS and branched, 12–29 × 5–8 μm, 0–1-septate, pale to medium
LSU, which proved insufficient in distinguishing some species brown, smooth, with somewhat thickened walls, sometimes
(Crous et al. 2007d, Zhang et al. 2011). More genes, especially conidiophores reduced to conidiogenous cells. Conidiogenous
protein coding genes are required to provide a better resolution cells integrated, terminal, 15–27 × 5–8 μm, with a 1–2(–3)
at the species level. denticle-like conidiogenous loci, proliferation sympodial, loci
unthickened, not or only somewhat darkened-refractive,
References: Menon 1956, Nüesch 1960, Barr 1968, Sivanesan 2–3 μm wide. Conidia in simple or branched chains, clavate,
1977 (morphology); Schubert et al. 2003 (morphology of subcylindrical, ellipsoid or rarely fusiform, (12–)
asexual stage); Crous et al. 2007d, Zhang et al. 2011, 2016 16–29 × 4–7 μm, pale olivaceous brown, 0–1(–3)-septate,
(morphology and phylogeny). smooth, tapering towards both ends, apex mostly truncate,
occasionally rounded or pointed, base truncate; hila often
Venturia martianoffiana (Thüm.) Y. Zhang ter & J.Q. Zhang, somewhat thickened and darkened-refractive, 1.5–3 μm wide.
comb. nov. Mycobank MB821418. Sexual morph not observed. On MEA: Mycelium consisting of
Basionym: Cladosporium martianoffianum Thüm., Byull. Mos- pale olivaceous, smooth, branched, 1.5–3 μm wide hyphae.
kovsk. Obshch. Isp. Prir., Otd. Biol. 55: 74. 1880. Conidiophores integrated, produced in the middle of the
mycelium, 3–6-septate, visible as small, protruding, denticle-
Venturia phaeosepta Y. Zhang ter & J.Q. Zhang, sp. nov. like loci, up to 92 μm long, 5–6 μm wide. Conidiogenous
MycoBank MB817355. Fig. 67. cells subcylindrical, 15–25 × 5–7 μm, pale to medium oliva-
ceous, smooth, tapering to 1–2 apical truncate loci, 2–4 μm
Etymology: Latin “phaeo-”, in reference to “dark” septum. wide. Conidia pale olivaceous, smooth, subcylindrical to
narrowly ellipsoid, occurring in simple or branched chains,
On Populus: Leaf spots amphigenous, subcircular to angular, 0–1(–2)-septate, tapering towards subtruncate ends, ends
1.5–13 mm wide, often confluent, diffuse, mostly spread along 2–4 μm wide, aseptate conidia 12–21.5 × 5–7 μm, septate
leaf veins, dark brown to black, with an irregular margin. conidia up to 28 μm long and 5–7 μm wide; basal hila usually
Colonies amphigenous, caespitose, greenish brown to thickened and darkened-refractive; microcyclic conidiation
blackish. Mycelium mainly subcuticular. Stromata variable in common in older cultures. Sexual morph not observed.
size, composed of pale olivaceous to brown, angular to
rounded, thick-walled, pseudoparenchymatous cells, 4–8 μm Culture characteristics: Colonies reaching 43 mm diam after
diam. Conidiophores solitary or loosely fasciculate, arising 1 mo on PDA at 25 °C in the dark. Colonies sporulated, erum-
mostly from stromata or from hyphae, erect, straight, pent, spreading, with abundant aerial mycelium and feathery to
www.studiesinmycology.org 205
MARIN-FELIX ET AL.
10
Fig. 66. Maximum likelihood tree generated from a sequence analysis of the ITS rDNA dataset. The outgroup is Fusicladium africanum CPC 12829. Maximum likelihood
bootstrap support values above 50 % are shown at the nodes and based on 1 000 replicates. Bayesian posterior probability values above 0.70 are shown at the nodes. The
species from poplar are in bold. Numbers between parentheses correspond to GenBank accession numbers. T indicates ex-type strain. TreeBASE: S21068.
smooth margins; grey olivaceous (surface), reverse dark Yangling, on leaves of Populus sp. (sects. Aigeiros), 4 Sep.
olivaceous. 2015, Y.F. Zhang (paratype, HMAS 247004, CGMCC3.18378);
ibid. (paratype, HMAS 247005, CGMCC3.18379).
Habitat and distribution: China (Henan, Shannxi), on leaves of
Populus spp. Notes: Among the reported venturiaceous species occurring on
Populus, the asexual morph of Venturia phaeosepta is more
Material examined: China, Henan, Puyang City Academy comparable with Venturia martianoffiana and F. romellianum in
Experimental Farm, on leaves of Populus × euramericana cv. 74/ the morphology of the conidiophore and mode of conidia pro-
76 (sect. Aigeiros), 20 May 2015, W. He (holotype, HMAS duction (Schubert et al. 2003). Venturia phaeosepta, however,
246998, culture ex-type CGMCC3.18368); on leaves of can readily be distinguished from V. martianoffiana by its
Populus × euramericana cv. 74/76 (sects. Aigeiros), Y.F. Zhang, 1–2(–3) apical denticle-like conidiogenous loci (vs. a single or
20 Jun. 2015 (paratype, HMAS 246999, CGMCC3.18371); 6 several (>3) conidiogenous loci of V. martianoffiana). Venturia
August 2015 (paratype, HMAS 247000, CGMCC3.18373); 7 phaeosepta differs from F. romellianum by its septate (vs. chiefly
Aug. 2015 (paratype, HMAS 247002, CGMCC3.18374); 8 Aug. aseptate) conidia (Schubert et al. 2003).
2015 (paratype, HMAS 247001, CGMCC3.18375); Shanxi,
206
GENERA OF PHYTOPATHOGENIC FUNGI
Authors: Y. Zhang, M. Shen & J.Q. Zhang out. This genus also produces necrotic spots on the twigs and
necrotic lesions on fruit.
Wilsonomyces Adask. et al., Mycotaxon 37: 283. 1990. Fig. 68.
Notes: Wilsonomyces is a monotypic genus. Wilsonomyces
Classification: Dothideomycetes, Pleosporomycetidae, Pleo- carpophilus was initially described as a new species of Hel-
sporales, Dothidotthiaceae. minthosporium, and was subsequently transferred to different
genera until Adaskaveg et al. (1990) introduced Wilsonomyces
Type species: Wilsonomyces carpophilus (Lev.) Adask. et al. to accommodate it. The taxonomy of the genus was contro-
Lectotype: plate 7, fig. 5 in Leveille JH. 1843. Ann. Sci. Nat., Bot., versial, and Sutton (1997) regarded it as synonym of Thyro-
ser. 2 19: 215. Epitype and ex-epitype culture designated here: stroma. However, all the strains of Wilsonomyces carpophilus
CBS H-23113, CBS 231.89. included in the phylogenetic analysis based on LSU, ITS and
tef1 (Figs 49, 64) sequences were located in a clade separate
DNA barcode (genus): LSU. from the rest of the taxa incorporated in the tree including the
type species of Thyrostroma, T. compactum. Therefore, it is
DNA barcodes (species): ITS, tef1. Table 22. Fig. 64. herewith supported that Wilsonomyces represents a distinct
genus. Finally, its location in the Dothidotthiaceae is also
Sexual morph unknown. Conidiomata sporodochial, usually supported.
punctiform, tan to olivaceous brown, finally becoming black.
Stroma present in host tissue, compact, immersed, erumpent, References: Ellis 1959, Adaskaveg et al. 1990 (morphology);
discoid on leaves, fusoid on twigs. Conidiophores macro- Ahmadpour et al. 2012a (morphology and pathogenicity).
nematous, mononematous, densely compacted, straight or
flexuous, branched or not, subcylindrical, geniculate, smooth, Wilsonomyces carpophilus (Lev.) Adask. et al., Mycotaxon 37:
subhyaline to pale brown, cicatrised, 1–4-septate. Con- 283. 1990. Fig. 68.
idiogenous cells terminal and intercalary, subcylindrical, sub- Basionym: Helminthosporium carpophilum Lev., Annls Sci. Nat.,
hyaline, smooth, proliferating sympodially at apex, scars Bot., ser. 2 19: 215. 1843.
unthickened. Conidia holoblastic, solitary, dry, acrogenous, Synonyms: Clasterosporium carpophilum (Lev.) Aderh., Landw.
simple, thick-walled, cylindrical, clavate, ellipsoidal or fusiform, Jahrb. 30: 815. 1901.
occasionally forked, rounded to acute at the apex, truncate at the Coryneum carpophilum (Lev.) Jauch, Int. Bull. Pl. Protect. 14: 99.
base, generally (2–)3–5(–10) transverse with occasionally 1–2 1940.
oblique septa, rarely with 1 longitudinal septum, subhyaline, Stigmina carpophila (Lev.) M.B. Ellis, Mycol. Pap. 72: 56. 1959.
becoming medium brown to golden-brown, dark olivaceous to Sciniatosporium carpophilum (Lev.) Morgan-Jones, Canad. J.
black in mass, conidia in vivo are larger (adapted from Bot. 49: 995. 1971.
Adaskaveg et al. 1990). Sporocadus carpophilus (Lev.) Arx, Gen. Fungi Sporul. Cult.,
Edn 3 (Vaduz): 224. 1981.
Culture characteristics: Growth moderate, PDA plates covered in Thyrostroma carpophilum (Lev.) B. Sutton, Arnoldia 14: 34. 1997.
4 wk, mostly consisting of submerged hyphae with sparse aerial For additional synonyms see Adaskaveg et al. (1990).
mycelium. In cultures grown in the dark, aerial mycelium sub-
felty to felty, initially white becoming pale olive-grey to greyish Conidiomata sporodochial, brown, with immersed to erumpent
olive, occasionally olive-ochre. In cultures grown exposed to stromata, 30–200 μm diam. Conidiophores subcylindrical, branched
light, submerged light brownish olive to olive-brown hyphae or not, geniculate, 10–70 × 5–7 μm, subhyaline to pale brown,
radiate outward from mycelial mat; aerial hyphae buffy-brown; smooth, 1–4-septate. Conidiogenous cells terminal and intercalary,
olivaceous black to black conidia produced in mass (more de- subcylindrical, subhyaline, smooth, 10–30 × 5–7 μm, proliferating
tails in Adaskaveg et al. 1990). sympodially, scars unthickened, 3.5–5 μm diam. Conidia narrowly
ellipsoid to subcylindrical or fusoid, subhyaline, becoming medium
Optimal media and cultivation conditions: PDA at 20 °C on the brown to golden-brown, smooth, with (2–)3–7(–11) dark, trans-
laboratory bench. verse septa, rarely with any oblique septum, (27–)
32–45(–55) × (12–)13–14(–16) μm, base truncate, 4–6 μm diam
Distribution: Worldwide. in vitro. Conidia in vivo are larger, namely 20–90 × 7–16 μm
(adapted from Adaskaveg et al. 1990).
Hosts: Pathogens mainly of Prunus spp., particularly peaches
and apricots, but also of other members of the family Rosaceae, Culture characteristics: Colonies flat, spreading, with moderate
i.e. Pyrus communis, Malus domestica, Sorbus aucuparia and aerial mycelium, and feathery margins, reaching 40 mm diam after
Cydonia oblonga. Also reported in Cleome sp. (Cleomaceae) 2 wk. On MEA, PDA and OA surface umber, reverse isabelline.
and Quercus ilex (Fagaceae).
Material examined: Lectotype: plate 7, fig. 5 in Leveille JH.
Disease symptoms: Wilsonomyces causes a disease known as 1843. Ann. Sci. Nat., Bot., ser. 2 19: 215. Unknown country, on
shot-hole disease because of the symptoms on the host leaves: petiole of Prunus subhirtella, 1989, J.W. Veenbaas-Rijks (epi-
small circular purple lesions with pale centres that gradually type designated here CBS H-23113, MBT376057, culture ex-
enlarge and become necrotic in the centre until the centre falls epitype CBS 231.89).
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Fig. 67. Venturia phaeosepta (ex-type CGMCC3.18368). A–F. On MEA. A. Colony on MEA. B. Conidial chains. C–D. Ramoconidia and conidia. E. Germinating conidium. F.
Conidium. G–M. On leaves. G. Leaves infected by Venturia phaeosepta. H. Conidiophores and conidia. I. Conidiogenous cells giving rise conidia. J. Conidiogenous cell. K.
Conidial chains. L. Conidia. M. Germinating conidium. Scale bars: B–D = 20 μm; E, F = 10 μm; G = 0.5 cm; H–M = 10 μm.
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GENERA OF PHYTOPATHOGENIC FUNGI
Fig. 68. Wilsonomyces carpophilus (ex-epitype CBS 231.89). A. Conidiomata. B–G. Conidiogenous cells giving rise to conidia. E. Conidia. Scale bars: 10 μm.
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