Septoria and septoria-like genera in the molecular era

Although it had previously been speculated by Sutton (1980) that Septoria was in fact polyphyletic, definitive proof of this hypothesis awaited the introduction of molecular techniques. Cunfer & Ueng (1999) were the first to use rDNA sequence data of the internal transcribed spacer region (ITS) to postulate that Zymoseptoria tritici (then known as Septoria tritici) and several Stagonospora spp. (a morphologically similar genus, previously linked to Septoria) actually belonged to two distinct genera. Verkley et al. (2004) extended this study by employing a combination of 28S nrDNA (LSU) and ITS data to prove that Septoria was in fact both poly- and paraphyletic. Their work showed that septoria-like species such as Z. tritici and Z. passerinii were more closely related to Ramularia than to the majority of the other Septoria species used in their datasets.

Feau et al. (2006) were the first to use a multi-locus polyphasic sequencing approach to reliably identify Septoria spp. Besides ITS and LSU sequence data, they also used β-tubulin (Btub) sequence data to separate closely related species into distinct monophyletic groups that frequently correlated with their respective host families. These results supported the approach of using multi-gene sequence data for studying a large collection of Septoria strains at species level.

Septoria s. str. was finally demarcated when Quaedvlieg et al. (2011) managed to obtain both ITS and LSU sequence data from S. cytisi herbarium specimens. Phylogenetic analysis of the obtained S. cytisi LSU sequence data clearly proved that Z. tritici and Z. passerinii [as previously indicated by Cunfer & Ueng (1999) and Verkley et al. (2004)] did not belong to Septoria s. str., but in fact belonged to a separate genus, closely related to Ramularia. These two species were subsequently split off from Septoria and placed in a new genus, Zymoseptoria (named for the yeast-like state produced in culture). Since the initial Zymoseptoria paper, five additional species from members of Poaceae have been described in this genus (Crous et al. 2012a, Stukenbrock et al. 2012).

DNA extraction, amplification and sequencing

Genomic DNA was extracted from fungal mycelium growing on MEA, using the UltraClean® Microbial DNA Isolation Kit (Mo Bio Laboratories, Inc., Solana Beach, CA, USA). Strains (Table 1) were screened for five loci (β-tubulin (Btub), internal transcribed spacer (ITS), Translation elongation factor 1-alpha (EF-1α) 28S nrDNA (LSU) and RNA polymerase II second largest subunit (RPB2) using the primer sets listed in Table 2. The PCR amplifications were performed in a total volume of 12.5 μL solution containing 10-20 ng of template DNA, 1 × PCR buffer, 0.7 μL DMSO (99.9 %), 2 mM MgCl₂, 0.4 μM of each primer, 25 μM of each dNTP and 1.0 U Taq DNA polymerase (GoTaq, Promega). PCR amplification conditions were set as follows: an initial denaturation temperature of 96 °C for 2 min, followed by 40 cycles of denaturation temperature of 96 °C for 45 s, primer annealing at the temperature stipulated in Table 2, primer extension at 72 °C for 90 s and a final extension step at 72 °C for 2 min. The resulting fragments were sequenced using the PCR primers together with a BigDye Terminator Cycle Sequencing Kit v. 3.1 (Applied Biosystems, Foster City, CA). Sequencing reactions were performed as described by Cheewangkoon et al. (2008). All novel sequences were deposited in NCBI’s GenBank database and alignments and phylogenetic trees in TreeBASE.

Phylogenetic analyses

A basic alignment of the obtained sequence data was first done using MAFFT v. 7 [(http://mafft.cbrc.jp/alignment/server/index.html) (Katoh et al. 2002)] and if necessary, manually improved in BioEdit v. 7.0.5.2 (Hall 1999). To check the congruency of the RPB2 and LSU dataset, a 70 % neighbour-joining (NJ) reciprocal bootstrap method with maximum likelihood distance was performed (Mason-Gamer & Kellogg 1996, Lombard et al. 2010). Bayesian analyses (critical value for the topological convergence diagnostic set to 0.01) were performed on the concatenated loci using MrBayes v. 3.2.1 (Huelsenbeck & Ronquist 2001) as described by Crous et al. (2006) using nucleotide substitution models that were selected using MrModeltest v.2.3 (Table 3) (Nylander 2004). In order to keep the trees manageable for publication, two separate Bayesian trees were run. The first tree was run with all the Septoria and septoria-like isolates that either belonged to, or where more closely related to the Mycosphaerellaceae (Fig. 1) while the second tree contained all the septoria-like isolates either belonging to, or being more closely related to the Phaeosphaeriaceae (Fig. 2). Parastagonospora nodorum (CBS 259.49) was used as outgroup for the Mycosphaerellaceae dataset, while Dothistroma pini (CBS 121005) was used as outgroup for the Phaeosphaeriaceae dataset. As the novel genera and species described in this study were already clearly distinquishable in the LSU/RPB2 trees, the ITS, EF-1α and Btub sequence data of these isolates were deposited in GenBank without their subsequent trees being published in this paper.

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Fig. 1.

A Bayesian 50 % majority rule RPB2/LSU consensus tree containing all Septoria and septoria-like taxa available at the CBS, which cluster in or near the Mycosphaerellaceae. Bayesian posterior probabilities support values for the respective nodes are displayed in the tree. A stop rule (set to 0.01) for the critical value for the topological convergence diagnostic was used for the Bayesian analysis. The tree was rooted to Phaeosphaeria nodorum (CBS 259.49). The scalebar indicates 0.1 expected changes per site.

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Fig. 2.

A Bayesian 50 % majority rule RPB2/LSU consensus tree containing all Septoria and septoria-like taxa available at the CBS, which cluster in or near the Phaeosphaeriaceae. Bayesian posterior probabilities support values for the respective nodes are displayed in the tree. A stop rule (set to 0.01) for the critical value for the topological convergence diagnostic was used for the Bayesian analysis. The tree was rooted to Dothistroma pini (CBS 121005). The scalebar indicates 0.01 expected changes per site.

Taxonomy

A total of 347 isolates representing 170 species were subjected to DNA analysis and morphological comparison. Phylogenetic analyses based on the LSU and RPB2 genes resolved a total of 47 clades of which 26 contained species belonging to the Septoria (-like) complex. These 47 resolved clades belong to a multitude of different families within the Dothidiomycetes ranging from the Mycosphaerellaceae in the Capnodiales to the Lentitheciaceae in the Pleosporales. It is still unclear within the Dothidiomycetes where the phylogenetic family borders are located, or even how many phylogenetically substainable families there actually are. The family annotation in the phylogenetic trees (Figs ​(Figs1,1, ​,2)2) is therefore based on the closest LSU neighbour that was available in GenBank, with clades treated as incertae sedis if no closer relationship than 97 % could be found.

Septoria and septoria-like genera

In addition to Septoria s. str., numerous septoria-like genera (pycnidial/acervular/stromatic conidioma with filiform conidia) have since been described. Although the majority of these have no ex-type culture available for DNA analysis, many have type material deposited in herbaria, which were available for morphological examination. A summary of these genera is provided below.

Pycnidial forms

Cytostagonospora Bubák, Ann. Mycol. 14: 150. 1916. Fig. 3.

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Fig. 3.

Conidia and conidiogenous cells of Cytostagonospora photiniicola (redrawn from Sutton 1980). Scale bar = 10 μm.

Mycelium immersed, dark brown, branched, septate. Conidiomata pycnidial, amphigenous, separate, globose, dark brown to black, immersed, unilocular, thick-walled, clypeate; walls of dark brown, thick-walled textura angularis to textura globulosa, becoming hyaline towards the conidiogenous region, extending in the upper part to become a circular clypeus of similar thickness to the wall. Ostiole central, circular, papillate to shortly rostrate, depressed, situated immersed within the clypeus. Conidiophores reduced to conidiogenous cells. Conidiogenous cells holoblastic, determinate, discrete, lageniform, hyaline, smooth, formed from the inner cells of the pycnidial wall. Conidia hyaline, 0-2-euseptate, not constricted at septa, base truncate, apex obtuse, thin-walled, eguttulate, smooth, filiform, often curved (Sutton 1980).

Type species: C. photiniicola Bubák, Ann. Mycol. 14(3-4): 150. 1916.

Notes: Von Arx (1983) and Sutton (1980) disagreed about the link of Cytostagonospora to Septoria. Von Arx treated it as a synonym of Septoria, while Sutton retained it as a separate genus.

Dearnessia Bubák, Hedwigia 58: 25. 1916.

Mycelium hyaline to brown, branched, septate. Conidiomata pycnidial, amphigenous, separate, globose, immersed, brown; wall of thin-walled textura angularis. Ostiole central, circular, papillate. Setae ostiolar, approximately straight, unbranched, tapered towards apex, dark brown, smooth, thin-walled, septate. Conidiogenous cells holoblastic, determinate, discrete, doliiform to ampulliform, hyaline, smooth and formed from the inner layer of the pycnidial wall. Conidia cylindrical to irregular, hyaline, 1-multi-transversely euseptate, rarely with 1-2 longitudinal eusepta, continuous or constricted, often tapered at the apex, base truncate, thin-walled, smooth, guttulate or not (Sutton 1980).

Type species: D. apocyni Bubák, Hedwigia 58: 25. 1916.

Dearnessia apocyni Bubák, Hedwigia 58: 25. 1916. Figs ​Figs4,4, ​,55.

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Fig. 4.

Conidia and conidiogenous cells of Dearnessia apocyni (F43227). Scale bars = 10 μm.

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Fig. 5.

Dearnessia apocyni (F43227). A. Leaf spot. B, C. Conidiogenous cells. D. Conidia. Scale bars = 10 μm.

Leaf spots amphigenous, irregular, feathery to angular, dark brown, 3-6 mm diam, surrounded by a wide chlorotic zone up to 3 mm diam. Conidiomata epiphyllous, pycnidial, erumpent, up to 150 μm diam, with central ostiole; wall of 3-6 layers of brown textura angularis. Conidiogenous cells doliiform, globose to subcylindrical, hyaline, smooth, thin-walled, mode of proliferation obscure, 5-10 × 4-6 μm. Conidia hyaline, smooth, subcylindrical to obclavate, apex obtuse, base truncate to subobtuse, straight to irregular (lateral swellings?), 1-4-septate, 16-33 × 5-8 μm.

Specimen examined: Canada, Ontario, London, on leaves of Apocynum androsaemifolium (Apocynaceae), 11 Aug. 1910, J. Dearness, holotype F43227.

Notes: Because the specimen is in poor condition, no definite conclusion could be reached about its potential relationships. However, D. apocyni does appear septoria-like in general morphology.

Jahniella Petr., Ann. Mycol. 18: 123. 1921. [1920]. Figs ​Figs6,6, ​,77.

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Fig. 6.

Conidia and conidiogenous cells of Jahniella bohemica (redrawn from Sutton 1980). Scale bar = 10 μm.

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Fig. 7.

Jahniella bohemica [K(M) 180917]. A. Vertical section through conidioma. B. Ostiolar region with loose cells. C. Conidiogenous cells. D. Conidia. Scale bars = 10 μm.

Mycelium branched, immersed, septate, brown. Conidiomata pycnidial, superficial on epidermis, immersed, separate, globose, papillate, dark brown, thick-walled, sclerenchymatic; wall consisting of an outer layer of dark brown, thick-walled textura angularis, a middle layer of 8 cells thick, of hyaline to pale brown, thick-walled cells, and an inner layer of thin-walled, hyaline, irregular cells. Ostiole single, circular, with a distinct channel and hyaline periphysoid cells. Conidiophores reduced to conidiogenous cells. Conidiogenous cells holoblastic, determinate, discrete, hyaline, ampulliform, lining the wall of the pycnidium. Conidia straight or slightly curved, hyaline, thin-walled, smooth, 3-4-euseptate, eguttulate, truncate at the base, slightly tapered to the apex (Sutton 1980).

Type species: J. bohemica Petr., Ann. Mycol. 18(4-6): 123. 1921. [1920]

Specimen examined: Czech Republic, Bohemia, on stems of Scrophularia nodosa (Scrophulariaceae), 18 Mar. 1916, J. Jahn, holotype K(M) 180917, slides ex BPI.

Note: The specimen correlates closely with the description provided by Sutton (1980), except that the conidiomata are superficial, not immersed in the epidermis.

Megaloseptoria Naumov, Morbi Plantarum 14: 144. 1925. Figs ​Figs8,8, ​,99.

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Fig. 8.

Conidia and conidiogenous cells of Megaloseptoria mirabilis (MA-Fungi 6978-1). Scale bars = 10 μm.

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Fig. 9.

Megaloseptoria mirabilis (MA-Fungi 6978-1). A. Conidiomata on host tissue. B. Conidiogenous cells. C. Conidia. Scale bars = 10 μm.

Mycelium immersed, branched, septate, brown. Conidiomata pycnidial, separate, globose, slightly papillate, dark brown to black, superficial, sessile, often aggregated in groups, unilocular, thick-walled; wall of several cell layers of brown textura angularis, more darkly pigmented on the outside. Ostiole single, circular. Conidiophores hyaline, branched, septate (mainly at the base), smooth, straight or irregular, formed from the inner cells of the pycnidial wall. Conidiogenous cells enteroblastic, determinate, discrete or integrated, doliiform, ampulliform or irregularly cylindrical, hyaline, smooth, collarette evident, channel wide, periclinal thickening present. Conidia hyaline to pale brown with several transverse eusepta, continuous, tapered near the obtuse apex and truncate base, thin-walled, smooth, cylindrical, straight or slightly curved, often with 2 guttules in each cell (Sutton 1980).

Type species: M. mirabilis Naumov, Morbi Plant. Script. Sect. Phytopath. Hort. Bot. Prince. USSR 14: 144. 1925.

Megaloseptoria mirabilis Naumov, Morbi Plantarum 14: 144. 1925.

Conidiomata aggregated in a black stroma at the ends of branchlets, globose, black, smooth, with central ostiole, up to 600 μm diam, papillate; wall of 3-8 layers of dark brown textura angularis. Conidiogenous cells lining the cavity, subcylindrical to ampulliform, hyaline, smooth, 7-15 × 4-8 μm; proliferating percurrently near apex. Conidia solitary, scolecosporous, variously curved, subcylindrical, tapering in upper third to obtuse apex, base truncate, 3-4 μm diam, transversely 30-40-septate, (170-)200-250 × (5-)6(-7) μm.

Specimen examined: Switzerland, Zürich, St. Schnach., on branchlets of Pinus pungens var. glauba (Pinaceae), 10 July 1951, E. Müller, holotype MA-Fungi 6978-1.

Note: Megaloseptoria differs from Septoria in that the conidiomata are aggregated in a black stroma, which is not the case in Septoria s. str.

Phaeoseptoria Speg., Revista Mus. La Plata 15(2): 39. 1908.

Leaf spots angular-subcircular, 0.5-3 mm diam, becoming confluent. Conidiomata pycnidial, epiphyllous, subepidermal, black, 60-90 μm diam. Conidiogenesis cells hyaline, smooth, holoblastic (?). Conidia filiform, obclavate, smooth, 1-3-euseptate, medium brown, 30 × 3 μm (Saccardo & Trotter 1913, Walker et al. 1992, Crous et al. 1997).

Type species: P. papayae Speg., Revista Mus. La Plata 15(2): 39. 1908.

Notes: Phaeoseptoria papayae was originally described from leaf spots on Carica papaya collected in the São Paulo Botanical Garden, Brazil. Presently there are numerous clades that contain isolates conforming to this morphology, and this matter can only be resolved once fresh material of P. papayae has been recollected to clarify its phylogeny (see below).

Pseudoseptoria Speg., Ann. Mus. Nac. B. Aires, Ser. 3 13: 388. 1910.

Mycelium immersed, branched, septate, pale brown. Conidiomata pycnidial, solitary or linearly aggregated, immersed, brown, globose, unilocular; walls thin, of pale brown textura angularis. Ostiole distinct, central, circular. Conidiophores reduced to conidiogenous cells. Conidiogenous cells discrete, determinate or indeterminate, hyaline, smooth, ampulliform with a prominent cylindrical papilla with several percurrent proliferations at the apex. Conidia falcate, fusoid, acutely rounded at each end, hyaline, aseptate, guttulate, smooth, thin-walled (Sutton 1980).

Type species: P. donacicola Speg., Ann. Mus. Nac. B. Aires, Ser. 3 13: 388. 1910.

Note: Species of Pseudoseptoria are plant pathogenic to members of Poaceae.

Rhabdospora (Durieu & Mont. ex Sacc.) Sacc., Syll. Fung. (Abellini) 3: 578. 1884. nom. cons.

Basionym: Septoria sect. Rhabdospora Durieu & Mont., in Durieu, Expl. Sci. Alg. 1 (livr. 15): 592. 1849. [1846-1849].

Type species: R. oleandri Durieu & Mont., in Durieu, Expl. Sci. Alg. 1 (livr. 15): 593. 1849 [1846-1849].

Notes: Rhabdospora is a poorly defined genus, originally established to accommodate septoria-like species occurring on stems (Priest 2006). Of the 11 species treated by Sutton (1980), most are currently placed in Septoria. This genus is in need of revision pending the recollection of fresh material (on Nerium oleander from Algeria).

Sclerostagonospora Höhn., Hedwigia 59: 252. 1917.

Conidiomata pycnidial, immersed, separate, dark brown to black, globose, unilocular; walls thin, composed of thick-walled, dark brown textura angularis; ostiole single, circular, central, papillate. Conidiophores reduced to conidiogenous cells. Conidiogenous cells holoblastic, determinate, discrete, hyaline, smooth, ampulliform to irregular, formed from the inner cells of the pycnidial wall. Conidia subcylindrical, pale brown, thin-walled, minutely verruculose, 3-euseptate, sometimes slightly constricted at the septa (from Sutton 1980).

Type species: S. heraclei (Sacc.) Höhn., Hedwigia 59: 252. 1917.

Note: Sclerostagonospora differs from Stagonospora in having pigmented conidia.

Septoria (Sacc.) Sacc., Syll. Fung 3: 474. 1884. nom. cons. Figs ​Figs10,10, ​,1111.

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Fig. 10.

Conidia and conidiogenous cells of Septoria cytisi (BPI USO 378994). Scale bars = 10 μm.

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Fig. 11.

Septoria cytisi (BPI USO 378994). A. Leaf with symptoms. B. Close-up of leaf spot with conidiomata. C, D. Conidiogenous cells giving rise to conidia. E. Conidia. Scale bars = 10 μm.

• = Septaria Fr., Novit. Fl. Svec. 5: 78. 1819. nom. rejic.

Mycelium slow-growing, pale brown, septate, immersed. Conidiomata pycnidial, immersed, separate or aggregated (but not confluent), globose, papillate (or not), brown, wall of thin, pale brown textura angularis, inner layer of flattened, hyaline textura angularis, frequently somewhat darker and more thick-walled around the ostiole. Ostiole single, circular, central. Conidiophores reduced to conidiogenous cells. Conidiogenous cells holoblastic, either determinate or indeterminate, proliferating sympodially and/or percurrently, hyaline, smooth, ampulliform, dolliform or lageniform to short cylindrical; scars unthickened. Conidia hyaline, multiseptate, filiform, smooth, continuous or constricted at septa. Sexual states are mycosphaerella-like.

Type species: S. cytisi Desm., Ann. Sci. Nat. Bot. 8: 24. 1847.

Specimen examined: Slovakia, Muehlthal near Bratislava (Pressburg), on leaves of Laburnum anagyroides (Leguminosae), 1884, J.A. Baeumler, BPI USO 378994.

Note: The ITS and LSU sequences of this specimen were published respectively under GenBank accession numbers JF700932 and JF700954.

Stagonospora (Sacc.) Sacc., Syll. Fung. (Abellini) 3: 445. 1884. nom. cons.

Basionym: Hendersonia subgen. Stagonospora Sacc., Michelia 2 (no. 6): 8. 1880.

Conidiomata pycnidial, immersed, unilocular, globose, separate, ostiolate; walls of dark brown, thick-walled textura angularis, and on the inside of hyaline, thin-walled, flattened cells. Conidiophores reduced to conidiogenous cells. Conidiogenous cells doliiform, hyaline, with several percurrent proliferations at the apex, formed from the inner cells of the pycnidial wall. Conidia hyaline, smooth to finely verruculose, 1-multiseptate, cylindrical or fusoid-ellipsoidal, straight or slightly curved, often guttulate, constricted or not at septa.

Type species: S. paludosa (Sacc. & Speg.) Sacc., Syll. Fung. (Abellini) 3: 453. 1884.

Stenocarpella Syd. & P. Syd., Ann. Mycol. 15(3-4): 258. 1917. Fig. 12.

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Fig. 12.

Stenocarpella maydis (top) and S. macrospora (bottom) (redrawn from Sutton 1980). Scale bars = 10 μm.

Mycelium immersed, brown, branched, septate. Conidiomata pycnidial, separate or sometimes confluent, globose or elongated, dark brown, subepidermal, unilocular, thick-walled; walls composed of dark brown, thick-walled textura angularis. Ostiole single, circular, papillate, protruding. Conidiophores usually absent. Conidiogenous cells cylindrical, hyaline, determinate, discrete, phialidic, with collarette and minute periclinal thickening, lining the inner layer of the pycnidial wall. Conidia subcylindrical, straight or curved, fusiform, apex obtuse, base tapered, truncate, thick-walled, smooth-walled, granular, pale to medium brown, 0-3-euseptate. Beta conidia hyaline, scolecosporous, curved (Crous et al. 2006, Lamprecht et al. 2011).

Type species: S. zeae Syd. & P. Syd., Ann. Mycol. 15(3-4): 258. 1917. [= S. macrospora (Earle) B. Sutton]

Specimens examined: South Africa, KwaZulu-Natal, Hlabisa, rain-damaged Bt Zea mays hybrid (Poaceae), 2003-04 season, J. Rheeder (ex-epitype, CBS 117560 =MRC 8615, designated in Crous et al. 2006); KwaZulu-Natal, Zea mays kernels, 2005, P. Caldwell, CPC 11863 = CBS 128560.

Notes: Stenocarpella presently contains two species, S. macrospora and S. maydis, both causing “Diplodia ear rot of maize”. These two taxa were previously assigned to Diplodia and Macrodiplodia, respectively (Petrak & Sydow 1927, Sutton 1964). Several years later, Sutton re-examining these taxa and placed them in their own genus, Stenocarpella (Sutton 1977, 1980). Recent phylogenetic studies confirmed that these taxa indeed cluster by themselves within the Diaporthales (Crous et al. 2006, Lamprecht et al. 2011), supporting the decision of Sutton (1980).

Trichoseptoria Cavara, Atti Ist. Bot. Univ. Lab. Crittog. Pavia 2: 40. 1892.

Type species: T. alpei Cavara, Atti Ist. Bot. Univ. Lab. Crittog. Pavia 2: 40. 1892.

Notes: Not much is known about this septoria-like genus, except that it is distinguished from Septoria by having setae on its pycnidia with 1-2-septate, hyaline conidia. This genus is in further need of revision once fresh material has been recollected (Citrus vulgaris, Belgiojoso, Alps).

Zymoseptoria Quaedvlieg & Crous, Persoonia 26: 64. 2011.

Conidiomata pycnidial, semi-immersed to erumpent, dark brown to black, subglobose, with central ostiole; wall of 3-4 layers of brown textura angularis. Conidiophores hyaline and smooth, 1-2-septate, or reduced to conidiogenous cells, lining the inner cavity. Conidiogenous cells are tightly aggregated and ampulliform to doliiform or subcylindrical, phialidic with periclinal thickening, or with 2-3 inconspicuous, percurrent proliferations at the apex. Conidia (Type I) solitary, hyaline, smooth, guttulate, narrowly cylindrical to subulate, tapering towards acutely rounded apex, with bluntly rounded to truncate base, transversely euseptate; hila not thickened nor darkened. On OA and PDA media plates the aerial hyphae disarticulate into phragmospores (Type II conidia) that again give rise to Type I conidia via microcyclic conidiation; yeast-like growth and microcyclic conidiation (Type III conidia) common on agar media (Quaedvlieg et al. 2011).

Type species: Z. tritici (Desm.) Quaedvlieg & Crous, Persoonia 26: 67. 2011.

Notes: Zymoseptoria was split off from Septoria s. str. and redescribed by Quaedvlieg et al. (2011) based on LSU sequence data when said authors delimitated Septoria s. str. by sequencing the ITS and LSU sequences out of S. cytisi herbarium material. Phylogenetic analysis showed that Zymoseptoria species cluster within a distinct clade inside the Mycosphaerellaceae that is closely related to Ramularia, but located distant from Septoria s. str.

Acervular forms

Asteromidium Speg., Ann. Soc. cient. argent. 26(1): 66. 1888. Figs ​Figs13,13, ​,1414.

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Fig. 13.

Conidia and conidiogenous cells of Asteromidium imperspicuum (redrawn from Sutton 1980). Scale bar = 10 μm.

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Fig. 14.

Asteromidium imperspicuum [K(M) 180228]. A. Conidiomata on host surface. B. Section through conidioma. C, D. Conidiogenous cells and conidia. Scale bars: B = 75 μm, all others = 10 μm.

Mycelium immersed, branched, septate, hyaline. Conidiomata acervular, subcuticular, separate or confluent, pulvinate to doliiform, at the base, composed of hyaline to pale brown, thin-walled textura angularis which extends laterally, finally with separate cells dispersed in a mucilaginous matrix to form the overlying wall; cuticle discoloured and occasionally pseudoparenchymatous, walls adjacent to the upper epidermal wall also discoloured; dehiscence irregular. Conidiogenous cells holoblastic, discrete, indeterminate, ± cylindrical, hyaline, smooth, with 1-2 sympodial proliferations, scars unthickened, flat, formed from the basal and lateral walls. Conidia cylindrical to fusoid, gently tapered at each end, apex obtuse, base truncate, thin-walled, guttulate to granular, hyaline, 3-septate (Sutton 1980).

Type species: A. imperspicuum Speg., Ann. Soc. cient. argent. 26(1): 66. 1888.

Specimen examined: Paraguay, on leaves of Sapindaceae, 1883, isotype K(M) 180228, ex B. Balansa Pl. du Paraguay No. 4085.

Notes: This genus has to be recollected (Sapindaceae, Paraguay) to allow for a molecular comparison to other existing genera in this complex. The morphology of the specimen examined correlates well with the description provided by Sutton (1980).

Ciferriella Petr., Ann. Mycol. 28(5/6): 409. 1930.

Type species: C. domingensis Petr. & Cif., Ann. Mycol. 28(5/6): 409. 1930.

• = Pseudocercospora Speg., Anales Mus. Nac. Hist. Nat. B. Aires, Ser. 3, 20: 437. 1910.

Pseudocercospora domingensis (Petr. & Cif.) Quaedvlieg, Verkley & Crous, comb. nov. MycoBank MB804401. Figs ​Figs15,15, ​,1616.

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Fig. 15.

Conidia and conidiogenous cells of Pseudocercospora domingensis (NY No 01048475). Scale bars = 10 μm.

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Fig. 16.

Pseudocercospora domingensis (NY No 01048475). A. Leaf spot. B, C. Conidiogenous cells. D. Conidia. Scale bars = 10 μm.

Basionym: Ciferriella domingensis Petr. & Cif., Ann. Mycol. 28(5/6): 409. 1930.

Leaf spots amphigenous, subcircular, medium brown with dark purple margin, 1.5-6 mm diam. Sporulation hypophyllous, fasciculate to sporodochial, brown, arising from a brown stroma, up to 50 μm diam. Conidiophores medium brown, smooth, subcylindrical, 0-2-septate, straight to once geniculate, 15-20 × 3-5 μm. Conidiogenous cells terminal, brown, smooth to finely verruculose, ampulliform to subcylindrical, proliferating sympodially or percurrently, tapering to a truncate apex, 2 μm diam, 10-15 × 3-4 μm. Conidia brown, smooth, straight to slightly curved, obclavate, apex subobtuse, base obconically truncate, 0-3-septate, 35-60 × 3-4 μm.

Specimen examined: Dominican Republic, on Vitex umbrosa (Lamiaceae), 26 May 1929, coll. R. Ciferri, det. F. Petrak, holotype ex N.Y. Bot. Gard. No 01048475.

Notes: The dimensions of the conidia and conidiophores correlate with the observations of Sutton (1980). However, the conidiomata are sporodochial to fasciculate, and not acervular. Ciferriella domingensis is a typical Pseudocercospora sensu Crous et al. (2013). Based on the species presently known from Vitex (Crous & Braun 2003), it appears to represent a distinct taxon, for which a new combination in Pseudocercospora is proposed.

Colletogloeum Petr., Sydowia 7: 368. 1953.

Mycelium immersed, branched, septate, hyaline to pale brown. Conidiomata acervular, epidermal to subepidermal, separate, occasionally confluent, composed of hyaline to pale brown, thin-walled textura angularis. Conidiophores hyaline to pale brown, sparsely branched, septate, smooth, cylindrical or slightly irregular, formed from the upper cells of the acervulus. Conidiogenous cells integrated or discrete, indeterminate, cylindrical or doliiform, with several percurrent proliferations at apex. Conidia hyaline to pale brown, 0-multiseptate, straight, curved or irregular, truncate at the base, obtuse at the apex, usually thin-walled, smooth, guttulate or not.

Type species: C. dalbergiae (S. Ahmad) Petr., Sydowia 7: 369. 1953. [= C. sissoo (Syd.) B. Sutton, Mycol. Pap. 97: 14. 1964.]

Notes: The exact taxonomic position of Colletogloeum was unclear for a long time as it included many species that appear to represent asexual morphs of Teratosphaeria. Crous et al. (2009a, b, c) used ITS sequence data from a specimen representative of C. sissoo (IMI 119162) to demonstate that the type of Colletogloeum clustered near the Pseudocercospora complex within the Mycosphaerellaceae.

Cylindrosporium Grev., Scott. crypt. fl. (Edinburgh) 1: pl. 27. 1822.

• = Cylindrodochium Bonord., Handb. Allgem. mykol. (Stuttgart): 132. 1851.

Mycelium immersed, branched, septate, hyaline. Conidiomata acervular, white, slimy, subcuticular, separate or confluent, formed of pale brown to hyaline, thin-walled textura angularis; dehiscence irregular. Conidiophores hyaline, parallel, branched only at the base, 1-2-septate, smooth, formed from the upper pseudoparenchyma. Conidiogenous cells enteroblastic, phialidic, integrated, cylindrical, hyaline, smooth. Conidia straight or slightly curved, aseptate, cylindrical, thin-walled, smooth, hyaline, eguttulate (Sutton 1980).

Type species: C. concentricum Unger, Exanth. Pflanzen (Wien) 2: 9. 1833.

Notes: Sutton (1980), Von Arx (1983), Deighton (1987) and Braun (1990) could not agree on the taxonomic status of this genus, which is associated with light leaf spot of oil seed rape (sexual morph Pyrenopeziza brassicae). This genus is in need of revision, awaiting the recollection of fresh material of C. concentricum (on Pulmonaria officinalis, Germany).

Phloeospora Wallr., Fl. Crypt. Germ. (Norimbergae) 2: 176. 1833.

Mycelium immersed, septate, hyaline. Conidiomata acervular, subepidermal, circular, discrete or confluent, composed of hyaline to pale brown, thin-walled textura angularis; dehiscence irregular. Conidiophores reduced to conidiogenous cells or with one or two supporting cells, branched at base or not. Conidiogenous cells holoblastic, annellidic, occasionally also sympodial, discrete, indeterminate hyaline, smooth, cylindrical, with several apical inconspicuous annellations, formed from the upper cells of the acervuli. Conidia hyaline, septate, smooth, guttulate or not, cylindrical, curved, attenuated towards the apices, apex obtuse to subobtuse, base truncate, with minute marginal frill.

Type species: P. ulmi (Fr.) Wallr., Fl. Crypt. Germ. (Norimbergae) 2: 177. 1833.

Notes: Sexual morphs of Phloeospora have been linked to genera that resemble the concepts of Mycosphaerella, Didymella and Sphaerulina. Verkley & Priest (2000) already noted that this genus is heterogeneous and in need of revision. The phylogenetic analysis performed in this study confirmed that Phloeospora (based on P. ulmi) clusters close to, but separate from Septoria s. str. (Fig. 1).

Phloeosporella Höhn., Ann. Mycol. 22: 201. 1924. Fig. 17.

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Fig. 17.

Conidia and conidiogenous cells of Phloeosporella ceanothi (redrawn from Sutton 1980). Scale bar = 10 μm.

Mycelium immersed, branched, septate, hyaline. Conidiomata acervular, subepidermal, ± circular, discrete, composed of hyaline to pale brown, thin-walled textura angularis. Conidiogenous cells holoblastic, sympodial, discrete, indeterminate, hyaline, smooth, lageniform to cylindrical, with 1-2 broad, flat unthickened apical scars, formed from the upper pseudoparenchyma. Conidia hyaline, 2-euseptate, thin-walled, smooth, guttulate, straight, curved or irregular, tapered gradually to an obtuse apex and abruptly to a truncate base (Sutton 1980).

Type species: P. ceanothi (Ellis & Everh.) Höhn., Ann. Mycol. 22(1-2): 201. 1924.

Notes: Not much is known of the sexual state of this genus, but P. padi has been linked to Blumeriella jaapii (Sutton 1980). A phylogenetic analysis performed on available isolates (unpubl. data) indicated that Phloeosporella is polyphyletic. However, as the type is not known from culture (on Ceanothus, California, USA), this matter could not be resolved.

Septogloeum Sacc., Michelia 2(6): 11. 1880.

Mycelium immersed, branched, septate, hyaline. Conidiomata acervular, epidermal to subepidermal, separate or confluent, formed of pale brown thin-walled pseudoparenchyma. Conidiophores short, stout, 1-2-septate, hyaline, smooth, branched at the base, formed from the upper pseudoparenchyma. Conidiogenous cells phialidic, discrete or integrated, determinate, cylindrical, doliiform to obpyriform, hyaline, smooth, with minute collarette and prominent periclinal thickening. Conidia hyaline, 1-3-euseptate, thin-walled, smooth, eguttulate, base truncate, apex obtuse, straight or curved, constricted, obovoid (Sutton 1980).

Type species: S. carthusianum (Sacc.) Sacc., Michelia 2(6): 11. 1880.

Notes: Although more than 120 species of Septogloeum have been described, the genus was reduced to just two species by Sutton & Pollack (1974). Sexual morphs have been linked to Pleuroceras in the Diaporthales (Monod 1983). The genus is in need of revision pending fresh collections.

Xenocylindrosporium Crous & Verkley, Fungal Planet 44. 2009.

Conidiomata immersed, black, opening by irregular rupture, acervuloid, up to 300 μm diam; wall consisting of 3-4 layers of pale brown textura angularis. Conidiophores hyaline, smooth, subcylindrical, branched, septate, or reduced to ampulliform conidiogenous cells. Conidiogenous cells hyaline, smooth, ampulliform to subcylindrical, terminal or lateral on septate conidiophores, monophialidic with minute periclinal thickening. Conidia solitary, hyaline, smooth, curved, widest in middle, tapering to acutely rounded apex and truncate base, 0 -1-septate.

Type species: X. kirstenboschense Crous & Verkley, Fungal Planet 44. 2009.

Stromatic forms

Dothistroma Hulbary, Bull. Ill. Nat. Hist. Surv. 21: 235. 1941.

Mycelium immersed, branched, septate, pale brown to hyaline. Conidiomata sometimes acervular, initially subepidermal later erumpent, composed of pale brown, thin-walled textura angularis, sometimes eustromatic, multilocular and of darker brown, thick-walled tissue. Stromata are strongly erumpent and finally pulvinate. Conidiogenous cells holoblastic, discrete, determinate, ampulliform, hyaline, smooth, non-proliferating, formed from the upper cells of stroma or from inner cells of the locular walls. Conidia hyaline, straight or curved, filiform, 1-5-euseptate, continuous, thin-walled and smooth (Barnes et al. 2004).

Type species: D. pini Hulbary, Bull. Ill. Nat. Hist. Surv. 21: 235. 1941.

Notes: Dothistroma sexual morphs are mycosphaerella-like (Evans 1984), and the two species of Dothistroma that have been subjected to DNA sequencing (D. septosporum and D. pini) cluster together in the “Dothistroma clade” as described by Crous et al. (2009a, c). Because of a lack of recognisable morphological characteristics, it is virtually impossible to discriminate between D. septosporum and D. pini without molecular tools (Barnes et al. 2004). Multiple morphological varieties of both D. septosporum and D. pini have been described based on differences in conidia length alone (e.g. D. septosporum var. keniense). However, controversy exists as to whether spore size represents an adequate characteristic to distinguish among these Dothistroma varieties, as since the introduction of molecular tools only D. septosporum and D. pini have been confirmed as distinct species.

Phlyctaeniella Petr., Ann. Mycol. 20: 323. 1922. Fig. 18.

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Fig. 18.

Conidia and conidiogenous cells of Phlyctaeniella humuli (IMI 202260) (redrawn from Sutton 1980). Scale bar = 10 μm.

Mycelium immersed, branched, septate, hyaline. Conidiomata eustromatic, separate, immersed, pale brown, globose, unilocular, scarcely erumpent; side wall and base of several cell layers of hyaline, thin-walled textura angularis, above of larger pale brown tissue. Ostiole indistinct, and dehiscence by rupture of the upper wall. Conidiophores hyaline, smooth, septate, irregularly branched, especially at the base, formed from the inner cells of the stroma wall. Conidiogenous cells phialidic, integrated or discrete, determinate, hyaline, markedly tapered at the apices, smooth, with apical or lateral apertures, collarette minute, with periclinal thickening; only rarely becoming percurrent. Conidia hyaline, smooth, thin-walled, irregularly guttulate, filiform, straight, curved or irregular, multiseptate (Sutton 1980).

Type species: P. polonica Petr., Ann. Mycol. 20: 323. 1922.

Note: Fresh material needs to be collected of this taxon (on Aruncus silvestris, Austria), before its taxonomy can be resolved.

Septocyta Petr., Ann. Mycol. 25: 330. 1927. Figs ​Figs19,19, ​,2020.

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Fig. 19.

Conidia and conidiogenous cells of Septocyta ramealis (PDD 51271). Scale bars = 10 μm.

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Fig. 20.

Septocyta ramealis (PDD 51271). A. Conidiomata on host tissue. B, C. Conidiogenous cells. D. Conidia. Scale bar = 10 μm.

Mycelium immersed, branched, septate, hyaline to pale brown. Conidiomata eustromatic, immersed, separate, erumpent, dark brown to black, finally opening widely, unilocular, multilocular or convoluted, thick-walled; wall of pale brown, thin-walled textura angularis except in the dehiscent region which is darker brown and more thick-walled. Ostiole absent, dehiscence by breakdown of the upper wall. Conidiogenous cells are holoblastic, sympodial with 1-3 apical, scarcely protruding, unthickened denticles, indeterminate, discrete, ampulliform to lageniform, hyaline, smooth, formed from the inner cells of the locular walls. Conidia hyaline, 1-3 euseptate, smooth, straight or slightly curved, acicular, apex obtuse, base truncate, often with minute guttules associated with septa (Sutton 1980).

Type species: S. ramealis (Roberge ex Desm.) Petr., Ann. Mycol. 25: 330. 1927.

Septocyta ramealis (Roberge ex Desm.) Petr., Ann. Mycol. 25: 330. 1927.

Conidiomata eustromatic to pycnidial, black, up to 160 μm diam, aggregated in clusters, erumpent through ruptures in epidermis, convulated; wall of 3-8 layers of brown textura angularis. Conidiophores lining the inner cavity, reduced to conidiogenous cells, or one or two supporting cells. Conidiogenous cells hyaline, smooth, ampulliform, proliferating sympodially and percurrently near apex, also with lateral denticle-like protrusions, 6-12 × 2.5-4 μm. Conidia hyaline, smooth, guttulate, (9-)20-30(-35) × 1.5(-2) μm, 1(-3)-septate, irregularly curved, subcylindrical, apex obtuse, base tapering slightly to truncate hilum, 0.5 μm diam.

Specimen examined: Germany, Brandenberg, on Rubus fructicosus (Rosaceae), 7 June 1923, coll. P. Sydow, det. H. Sydow, Sydow Mycoth. Germ. PDD 51271.

Notes: Septocyta ramealis, the type of Septocyta, has a long list of synonyms. The specimen examined here (PDD 51271), differs somewhat from the description provided by Sutton (1980), and appears to represent a species of Septoria s. str., as the mode of conidiogenesis is not that different. Presently there is a single ITS sequence labelled as S. ruborum available on GenBank (JN133277.1), placing it in the middle of Septoria s. str. As no type material of S. ramealis could be located, this matter remains unresolved.

Septopatella Petr., Ann. Mycol. 23: 128. 1925.

Mycelium immersed, branched, septate, hyaline to subhyaline. Conidiomata superficial, often subtended by a superficial, pale brown, septate, branched mycelium, pulvinate, separate to occasionally aggregated, dark brown to black, finally opening widely, cupulate; basal wall of small-celled, brown, thin-walled textura angularis, becoming textura porrecta as it merges into the periclinal walls; a hypostroma attaches the conidioma to the substrate; Ostiole absent. Conidiophores hyaline, septate, branched at the base, thin-walled, cylindrical, formed from the gelatinized basal wall of the conidioma. Conidiogenous cells holoblastic, sympodial, integrated, indeterminate, cylindrical, hyaline, smooth, produced as 2-3 branches from the apex of the conidiophores. Conidia hyaline, 3-4-euseptate, thin-walled, smooth, minutely guttulate, straight or curved, occasionally irregularly filiform (Dyko & Sutton 1979, Sutton 1980).

Type species: S. septata (Jaap) Petr., Ann. Mycol. 23: 129. 1925.

Note: Not much is known about this genus, and as no cultures of S. septata are presently available (on Pinus montana, Czech Republic) this matter cannot be resolved.

Stictosepta Petr., Sydowia 17: 230. 1964. [1963]. Fig. 21.

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Fig. 21.

Conidia and conidiogenous cells of Stictosepta cupularis (redrawn from Sutton 1980). Scale bar = 10 μm.

Mycelium immersed, branched, septate, hyaline. Conidiomata eustromatic, immersed, globose to collabent, papillate, unilocular, often convoluted, hyaline; walls thick, of hyaline, thin-walled textura intricata. Ostiole central and circular, single, furfuraceous. Conidiophores hyaline, septate, branched, anastomosing, formed from the inner cells of the locular wall. Conidiogenous cells sympodial or synchronous, integrated, indeterminate, hyaline, thin-walled, with usually two small, unthickened, apical, slightly protuberant conidiogenous loci. Conidia hyaline, thin-walled, smooth, multiseptate, slightly constricted at the septa, each cell medianly guttulate, straight or curved, base truncate, apex obtuse (Sutton 1980).

Type species: S. cupularis Petr., Sydowia 17: 230. 1964. [1963].

Note: Not much is known about this genus, but as no isolate of S. cupularis is presently available (on stems of Fraxinus, Czech Republic), it will not be treated here.

Sexual morphs linked to Septoria

Several sexual genera have been linked to Septoria and allied genera in literature, but very few have been confirmed in culture. Most sexual states cluster in the Mycosphaerella complex.

Mycosphaerella Johanson, Öfvers. K. Svensk. Vetensk.-Akad. Förhandl. 41(no. 9): 163. 1884.

• = Ramularia Unger, Exanth. Pflanzen (Wien): 119. 1833.

Mycelium immersed to superficial, septate, hyaline, branched. Caespituli usually whitish to greyish on host tissue. Conidiophores fasciculate to synnematal, rarely solitary, or forming small sporodochia, emerging through stomata, from inner hyphae or stromata; conidiophores straight, subcylindric to geniculate-sinuous, aseptate or septate, hyaline, occasionally branched, smooth, rarely rough. Conidiogenous cells integrated, terminal, polyblastic, elongating sympodially, apex more or less straight to geniculate-sinuous or strongly curved, cicatrized, conidial scars hardly to conspicuously thickened, but always darkened, refractive. Conidia solitary to catenate, sometimes in branched chains, 0-4(-multi)-septate, hyaline, ellipsoid-ovoid to cylindrical-fusoid, rarely filiform, occasionally constricted at the septa, smooth to verruculose-echinulate; hila distinct, slightly to conspicuously thickened, darkened, refractive; conidial secession schizolytic. Ascomata immersed to superficial, uniloculate, globose to subglobose with papillate, central, periphysate ostiole, dark brown to black, scattered or gregarious. Peridium of 3-6 layers of thin- to thick-walled textura angularis, dark brown to black. Hamathecium dissolves at maturity, and no stromatic tissue remains between the asci. Asci bitunicate, fissitunicate, 8-spored, cylindrical to cylindric-clavate, ovoid to ampulliform or saccate, sessile to subsessile, apex rounded with distinct or indistinct ocular chamber. Ascospores bi- to tri- or multiseriate, ellipsoid-fusoid to obclavate or subcylindrical, hyaline, medianly 1-septate, often constricted at the septum, smooth-walled, granular to guttulate, mostly lacking any sheath.

Type species: Ramularia pusilla Unger, Exanth. Pflanzen (Wien): 169. 1833.

Notes: Species of Ramularia (including the Mycosphaerella sexual morph) have evolved over a broad developmental and physiological adaptation range that includes endophytes, saprophytes and symbionts. However, for a major part Ramularia consists of a wide range of narrow host range, foliicolous plant pathogens which are the cause of significant economical losses in both temperate and tropical crops worldwide (Crous et al. 2001). Verkley et al. (2004) showed that Mycosphaerella s. str. (linked to M. punctiformis) was in fact restricted to species with Ramularia anamorphs, leaving many “Mycosphaerella” species to be disposed to other genera. In employing the one fungus = one name concept (Hawksworth et al. 2011, Wingfield et al. 2012), the choice is to use Ramularia over Mycosphaerella, as the former is monophyletic and recently monographed (Braun 1995, 1998), while Mycosphaerella is poly- and paraphyletic, and consists of more than 40 genera, many as yet untreated (Crous et al. 2009c)

Sphaerulina Sacc., Michelia 1(no. 4): 399. 1878.

Ascomata pseudothecial, immersed, subepidermal, erumpent at the top, single to clustered, globose, papillate. Ostiole central, with hyaline periphyses; wall of textura angularis, composed of 2-4 layers of brown cells. Hamathecium dissolving at maturity. Asci bitunicate, fissitunicate, clustered, cylindrical to obclavate, rounded at apex, with or without a shallow apical chamber, short-stipitate or sessile, with 8 biseriate to triseriate ascospores. Ascospores subcylindrical to fusiform, rounded at ends, slightly tapered, straight or slightly curved, 1-3-septate, with a primary septum nearly median, hyaline, smooth, without sheath or appendages.

Type species: Sphaerulina myriadea (DC.) Sacc., Michelia 1(no. 4): 399. 1878.

Notes: The genus Sphaerulina was chiefly separated from Mycosphaerella on the basis of ascospore septation (Crous et al. 2011). Sphaerulina myriadea, which occurs on hosts in the Fagaceae, appears to be a species complex. Results in this paper show that Sphaerulina myriadea clusters together with many septoria-like species in a clade that is distinct, but very closely related to Septoria s. str. The septoria-like species in this Sphaerulina clade were subsequently rediscribed in Sphaerulina. Species including ones with 1-septate ascospores and septoria-like asexual morphs are treated below and by Verkley et al. (2013).

Treatment of phylogenetic clades

Based on the phylogenetic data generated in this study, we were able to delineate several clades in the Septoria complex. Recognised clades, as well as novel species and genera, are described and discussed below. Taxa with descriptions that are freely available online in MycoBank or open access journals, are not repeated here.

Clade 1: Septoria

Description: See above.

Type species: S. cytisi Desm., Ann. Sci. Nat. Bot. 8: 24. 1847.

Septoria cf. agrimoniicola Bondartsev, Mater. mikol. obslêed. Ross. 2: 6. 1921.

Leaf spots on the upper leaf surface, distinct, scattered, brown with purplish margin, circular to angular, sometimes vein-limited, discrete lesions 2-4 mm diam, reaching 10 mm wide when confluent, finally the center becoming pale colored to nearly whitish; on the lower leaf surface similar but discoloured (Shin & Sameva 2004). On sterile Carex leaves on WA. Conidiomata pycnidial, separate but frequently aggregated and linked by brown stromatic tissue in a stroma; globose, black, exuding a creamy conidial mass via a central ostiole; conidiomata up to 350 μm diam; wall of 6-12 layers of dark brown, thick-walled textura angularis. Conidiophores reduced to conidiogenous cells or 1-2 supporting cells, hyaline, subcylindrical, lining the inner layer of conidioma. Conidiogenous cells hyaline, smooth, subcylindrical to ampulliform, 10-17 × 3-4 μm; proliferating sympodially but also percurrently near apex. Conidia hyaline, smooth, guttulate, filiform, apex subobtuse, base long obconically truncate, 1-4-septate, (20-)25-35(-40) × 1.5-2(-2.5) μm; microcyclic conidiation observed.

Culture characteristics: Colonies on PDA flat, undulate with sparse, white aerial mycelium, surface olivaceous-black, reverse olivaceous-black, after 14 d, 3.5 cm diam; on MEA with sparse white aerial mycelium, surface olivaceous-black, reverse olivaceous-black, after 14 d, 5 cm diam; on OA with sparse white aerial mycelium, surface olivaceous, reverse olivaceous, after 14 d, 3 cm diam.

Specimen examined: South Korea, Guri, on leaves of Agrimonia pilosa (Rosaceae), 11 Jul. 2009, H.D. Shin (CBS H-21279, culture CBS 128602 =KACC 44644 = SMKC 24292).

Notes: This fungus was first reported from Korea by Shin & Sameva (2002) as S. agrimoniicola, and fits well with the original description of this European taxon. However, fresh European collections and cultures are required for comparison, as S. agrimoniicola may well be restricted to Europe.

Septoria cf. stachydicola Hollós, Mathem. Természettud. Közlem. Magg. Tudom. Akad. 35(1): 60. 1926.

Leaf spots on the upper leaf surface distinct, scattered, brown with purplish margin, circular to angular, sometimes vein-limited, discrete lesions 2-4 mm diam, reaching 10 mm wide when confluent, finally the center becoming paler or nearly whitish; on the lower leaf surface similar but discoloured (Shin & Sameva 2004). On OA. Conidiomata solitary to aggregated, black, globose, becoming somewhat papillate, up to 250 μm diam, opening by means of central ostiole, up to 40 μm diam; wall of 6-8 layers of thick-walled, brown textura angularis; exuding a creamy conidial mass. Conidiophores reduced to conidiogenous cells. Conidiogenous cells lining the inner wall layer, hyaline, discrete, ampulliform to lageniform, 4-10 × 3-5 μm, proliferating sympodially or percurrently with inconspicuous proliferations. Conidia filiform, curved or flexuous, rarely straight, (60-)65-75(-90) × 1.5-2(-3) μm, hyaline, guttulate, 4-7(-11)-septate, apex subobtuse, slightly tapering from basal septum to truncate base, 1.5-2 μm.

Culture characteristics: Colonies on PDA erumpent, with feathery margin, with sparse white aerial mycelium, surface greenish-black, reverse olivaceous-black, after 14 d, 2.5 cm diam; on MEA with sparse white aerial mycelium, surface cinnamon to olivaceous-black in the younger patches, reverse cinnamon to olivaceous-black in patches, after 14 d, 4 cm diam; on OA with sparse white aerial mycelium, surface greenish-black, reverse fuscous-black, after 14 d, 3 cm diam.

Specimen examined: South Korea, Incheon, leaf of Stachys riederi var. japonica (Lamiaceae), 14 Aug. 2008, H.D. Shin (CBS H-21278, culture CBS 128668 =KACC 44796 = SMKC 24663).

Note: The Korean collection was originally identified as Septoria stachydicola, which fits the original description provided for this taxon (Shin & Sameva 2004). However, authentic European material is required for a comparison to confirm this identification, as we suspect S. stachydicola may be restricted to Europe.

Septoria cretae Quaedvlieg, Verkley & Crous, sp. nov. MycoBank MB804402. Figs ​Figs22,22, ​,2323.

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Fig. 22.

Conidia and conidiogenous cells of Septoria cretae (CBS 135095). Scale bar = 10 μm.

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Fig. 23.

Septoria cretae (CBS 135095). A. Colony sporulating in culture. B-F. Conidiophores and conidiogenous cells giving rise to conidia. G. Conidia. Scale bars = 10 μm.

Etymology: Named after Crete, the island from where it was collected.

On sterile Carex leaves on WA. Conidiomata up to 250 μm diam, brown, immersed, subepidermal, pycnidial, subglobose with central ostiole, exuding creamy conidial mass; wall of 2-3 layers of brown textura angularis. Conidiophores reduced to conidiogenous cells, or with a supporting cell that gives rise to several conidiogenous cells. Conidiogenous cells phialidic, hyaline, smooth, aggregated, lining the inner cavity, ampulliform to subcylindrical, straight to curved, proliferating sympodially near apex, 10-20 × 2-3.5 μm. Conidia hyaline, smooth, thin-walled, subcylindrical to narrowly obclavate, granular, with subobtuse apex and obconically truncate to truncate base, 1-3-septate, (8-)15-22(-27) × 2(-3) μm.

Culture characteristics: Colonies on PDA erumpent, with feathery margin, lacking aerial mycelium, surface fuscous-black, reverse olivaceous-black, after 14 d, 3.5 cm diam; on MEA surface fuscous-black, reverse olivaceous-black, after 14 d, 4 cm diam; on OA surface fuscous-black, reverse fuscous-black, after 14 d, 3.5 cm diam.

Specimen examined: Greece, Crete, on leaves of Nerium oleander (Apocynaceae), 7 Jul. 2012, U. Damm, (holotype CBS H-21277, culture ex-type CBS 135095).

Notes: Several species of Septoria are known on Nerium oleander, namely S. juliae [conidia 1-6(-7)-septate, 26-54 × 2.5-5.5 μm], S. neriicola (conidia 1-septate, 30-40 × 0.7-1 μm), S. oleandriicola [conidia 1-3-septate, 12.5-22.5-37.5(-40) × 2.5-3(-4.5) μm], S. oleandrina (conidia 0-1-septate, 9-19 × 1-1.5 μm), and S. roll-hansenii (conidia 0-4-septate, 25-39 × 3-4 μm) (Bedlan 2011), which differ from S. cretae based on conidial dimensions and septation.

Septoria glycinicola Quaedvlieg, H.D. Shin, Verkley & Crous, sp. nov. MycoBank MB804403. Fig. 24.

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Fig. 24.

Septoria glycinicola (CBS 128618). A, B. Colonies sporulating on PDA. C. Conidiogenous cells. D. Conidia. Scale bars = 10 μm.

Etymology: Named after the host genus on which it was collected, Glycine.

On OA. Conidiomata forming in concentric circles, pycnidial, separate, black, globose, up to 150 μm diam, opening by a central ostiole, up to 30 μm diam, exuding a creamy conidial mass; wall consisting of 3-6 layers of brown textura angularis. Conidiophores reduced to conidiogenous cells. Conidiogenous cells lining the inner cavity, hyaline, smooth, ampulliform, 10-16 × 2.5-3.5 μm, proliferating sympodially near apex, holoblastic. Conidia hyaline, smooth, guttulate to granular, subcylindrical to narrowly obclavate, irregularly to gently curved, apex subobtuse, base long obconically truncate, 3-6-septate, (33-)45-55(-65) × (1.5-)2 μm.

Culture characteristics: Colonies on PDA flat, circular, with sparse black aerial mycelium with black tufts, surface patches of olivaceous-black to fawn in the younger parts, reverse with patches of olivaceous-black in the older parts to mouse-grey and pale purplish grey in the younger mycelium, after 14 d, 6.5 cm diam, pinkish exudate; on OA lobate, with sparse white aerial mycelium, surface patches of vinaceous to olivaceous-black, reverse fuscous-black to vinaceous-buff; after 14 d, 8.5 cm diam, pinkish exudate; on MEA with radial lobes, very short white aerial mycelium, surface fuscous-black, reverse olivaceous-black; after 14 d, 4.5 cm diam.

Specimen examined: South Korea, Namyangju, on leaves of Glycine max (Fabaceae), 22 Sep. 2008, H.D. Shin (holotype CBS H-21270, culture ex-type CBS 128618 =KACC 43091 = SMKC 22879).

Notes: Septoria glycines is the common Septoria species associated with brown spot of soybeans. Septoria glycinicola is distinct from S. glycines (conidia 1-4 septate, 21-45 × 1.5-2 μm) in that it has larger conidia.

Septoria oenanthicola Quaedvlieg, H.D. Shin, Verkley & Crous, sp. nov. MycoBank MB804405. Fig. 25.

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Fig. 25.

Septoria oenanthicola (CBS 128649). A. Colony sporulating on MEA. B. Section through conidiomata. C-G. Conidiogenous cells. H. Conidia. Scale bars: B = 200 μm, all others = 10 μm.

Etymology: Named after the host genus from which it was collected, Oenanthe.

On sterile Carex leaves on WA. Conidiomata pycnidial, separate but aggregated, black, globose, up to 200 μm diam, opening by central ostiole, up to 20 μm diam, exuding a creamy conidial mass; wall consisting of dark brown, thickened, 6-10 layers of textura angularis. Conidiophores reduced to conidiogenous cells or to one supporting cell. Conidiogenous cells hyaline, smooth, 3-5 × 3-7 μm, ampulliform, proliferating sympodially near apex, holoblastic. Conidia hyaline, smooth, guttulate, subcylindrical to narrowly obclavate, apex subobtuse, base long obconically truncate, 1-6-septate, (17-)25-45(-55) × (2-)2.5(-3) μm.

Culture characteristics: Colonies on PDA flat, undulate with sparse, white aerial mycelium, surface olivaceous-grey, reverse olivaceous, after 14 d, 2.5 cm diam; on MEA with sparse, white aerial mycelium, surface olivaceous-grey, reverse olivaceous-black, after 14 d, 5 cm diam; on OA with sparse white aerial mycelium, surface olivaceous-grey, reverse olivaceous, after 14 d, 3 cm diam.

Specimen examined: South Korea, Yangpyeong, on leaves of Oenanthe javanica (Apiaceae), 25 May 2006, H.D. Shin (holotype CBS H-21281, culture ex-type CBS 128649 =KACC 42394 = SMKC 21807).

Notes: This fungus was originally recorded from Korea by Shin (1998) as Septoria oenanthis. However, conidia of Korean specimens (30-60 ×1.5-2.5 μm; Shin & Sameva 2004) are much larger than that of the American type collection (20-35 × 1.5-2 μm; Saccardo 1895), and therefore better treated as a separate taxon.

Septoria pseudonapelli Quaedvlieg, H.D. Shin, Verkley & Crous, sp. nov. MycoBank MB804404. Fig. 26.

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Fig. 26.

Septoria pseudonapelli (CBS 128664). A. Colony sporulating on PDA. B. Section through conidioma. C-E. Conidiogenous cells. F. Conidia. Scale bars: B = 125 μm, all others = 10 μm.

Etymology: Named after its morphological similarity to Septoria napelli.

Leaf spots on the upper leaf surface, scattered to confluent, distinct, angular to irregular, usually vein-limited, small to large, up to 30 mm when confluent, at first appearing small angular brown discoloration, later turning blackish brown with or without distinct border line, finally central area becoming blackish and surrounded by pale greenish margin; on the lower leaf surface similar but discoloured (Shin & Sameva 2004). On sterile Carex leaves on WA. Conidiomata pycnidial, separate, black, globose, papillate with short neck (at times 1-2 necks develop), up to 250 μm wide, 500 μm high with central ostiole; wall of 5-7 layers of brown textura angularis. Conidiophores reduced to conidiogenous cells. Conidiogenous cells ampulliform, lining the inner cavity, hyaline, smooth, with sympodial or apical percurrent proliferation, 10-13 × 5-7 μm. Conidia filiform, curved to flexuous, (50-)75-90(-100) × (2.5-)3(-3.5) μm, hyaline, guttulate, 4-10-septate, apex subobtuse, base obconically truncate, 2 μm diam.

Culture characteristics: Colonies on PDA flat, undulate with sparse, white aerial mycelium, surface olivaceous-black, reverse olivaceous-black, after 14 d, 2 cm diam; on MEA with sparse white aerial mycelium, surface olivaceous-black, reverse olivaceous-black, after 14 d, 4 cm diam; on OA with sparse white aerial mycelium, surface olivaceous, reverse olivaceous, after 14 d, 2 cm diam.

Specimen examined: South Korea, Chuncheon, on leaves of Aconitum pseudolaeve var. erectum (Ranunculaceae), 4 Sep. 2008, H.D. Shin (holotype CBS H-21280, culture ex-type CBS 128664 =KACC 43952 = SMKC 23638).

Notes: This taxon was originally reported as Septoria napelli from Korea by Shin & Sameva (2004), and broadly corresponds with the original description provided for this taxon (Petrak 1957). However, we have examined European material authentic for the name (see Verkley et al. 2013, this issue), from which the Korean fungus is genetically different. Based on these observations we describe the Korean collection as new.

Clade 2: Sphaerulina

Sphaerulina Sacc., Michelia 1(no. 4): 399. 1878.

Description: See above.

Type species: Sphaerulina myriadea (DC.) Sacc., Michelia 1(no. 4): 399. 1878.

Specimens examined: Germany, Driesen, Lasch [Rabenhorst, Fungi Eur. no. 149] (L). Japan, Aomori, Tsugaru, Kidukuri, Bense-marsh (40°51’53” N, 140°17’42”E), on leaves of Q. dentata, 21 Apr. 2007, K. Tanaka 2243 (HHUF 29940; single ascospore culture CBS 124646 =JCM 15565). UK, on leaves of Quercus robur (Fagaceae), J.E. Vize [Microfungi Brit. Ex. No. 195] (ex IMI 57186, K(M) 167735). USA, California: Sequoia National Park. alt. 2590 m, on leaves of Castanopsis sempervirens, 18 Jun. 1931, H.E. Parks (BPI 623686); Lake Co., Hoberg’s Resort, on leaves of Q. kelloggii, 15 May 1943, V. Miller (BPI 623707); Maryland, Marlboro, on leaves of Q. alba, 26 Apr. 1929, C.L. Shear (BPI 623705); Texas, Houston, on leaves of Q. alba, 8 Apr. 1869, H.W. Ravenel (BPI 623704).

Notes: Sivanesan (1984) linked Sphaerulina to Septoria, Cercospora and Cercosporella asexual morphs, though these were never confirmed based on DNA data. The latter two genera have since been shown to be distinct (Crous et al. 2013, Groenewald et al. 2013; this volume), which leaves septoria-like asexual morphs such as Sphaerulina rubi Demaree & Wilcox (linked to Cylindrosporium rubi Ellis & Morgan), and S. rehmiana (linked to Septoria rosae), which confirms the results obtained here (Fig. 1).

Sphaerulina abeliceae (Hiray.) Quaedvlieg, Verkley & Crous, comb. nov. MycoBank MB804406.

Basionym: Septoria abeliceae Hiray., Mem. Col. Agr. Kyoto. Imp. Univ. 13(3): 33. 1931.

Specimen examined: South Korea, Jeonju, on leaves of Zelkova serrata (Ulmaceae), 29 Oct. 2006, H.D. Shin, CBS 128591 =KACC 42626.

Sphaerulina amelanchier Quaedvlieg, Verkley & Crous, sp. nov. MycoBank MB804407. Figs ​Figs27,27, ​,2828.

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Fig. 27.

Conidia, conidiogenous cells, ascospore and ascus of Sphaerulina amelanchier (CBS 135110). Scale bars = 10 μm.

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Fig. 28.

Sphaerulina amelanchier (CBS 135110). A. Colony on PDA. B. Conidiogenous cells. C. Ascomata on host tissue. D. Germinating ascospore. E, F. Asci. G. Ascospores. H. Conidia. Scale bars = 10 μm.

Etymology: Named after the host genus from which it was collected, Amelanchier.

On sterile Carex leaves on WA. Conidiomata pycnidial, brown, separate, immersed, globose, up to 150 μm diam, exuding a creamy conidial mass via central ostiole; wall of 3-6 layers of brown textura angularis. Conidiophores reduced to conidiogenous cells. Conidiogenous cells hyaline, smooth, subcylindrical, irregularly curved, branched to once geniculate-sinuous, 5-20 × 3-4 μm; proliferating sympodially. Conidia hyaline, smooth, guttulate, filiform, narrowly obclavate, apex subacutely rounded, base long obconically truncate, 1-8-septate, (25-)40-55(-60) × (1.5-)2(-2.5) μm; microcyclic conidiation common. Ascomata globose, brown, separate, immersed to erumpent, up to 150 μm diam. Asci broadly ellipsoid to obclavate, 22-35 × 7-9 μm; apical chamber visible, 1-1.5 μm diam. Ascospores fusoid-ellipsoid, hyaline, smooth, granular, not to slightly constricted at median septum, widest just above septum, prominently curved, (13-)17-20(-25) × (2.5-)3(-3.5) μm. Ascospores germinating from both ends, with germ tubes parallel to the long axis, developing lateral branches and becoming constricted at septum, 3-4 μm diam.

Culture characteristics: Colonies on PDA radially striate with lobate edge, sparse white aerial mycelium, surface fuscous-black to buff for the younger tissue, reverse cinnamon to olivaceous-black, after 14 d, 3 cm diam; on MEA surface patches of hazel to fawm to fuscous-black, reverse sepia to olivaceous-black, after 14 d, 4.5 cm diam; on OA surface pale-vinaceous to fuscous-black, reverse cinnamon to fuscous-black, after 14 d, 3 cm diam.

Specimen examined: Netherlands, Houten, on leaf litter of Amelanchier sp. (Rosaceae), 28 Mar. 2012, S. Videira (holotype CBS H-21282, culture ex-type CBS 135110 =MP8 = S544).

Note: Presently there are no known species of septoria-like fungi known from Amelanchier. Phylogenetically, it is similar to Sphaerulina rhabdoclinis (conidia 8-30 × 1.5-2 μm), which infects needles of Pseudotsuga menziesii. Phylogenetically similar isolates occur on Betula, Castanea and Quercus. More isolates and molecular data are required to resolve this complex.

Sphaerulina azaleae (Voglino) Quaedvlieg, Verkley & Crous, comb. nov. MycoBank MB804408.

Basionym: Septoria azaleae Voglino, Syll. Fung. (Abellini) 14(2): 976. 1899.

• ≡ Phloeospora azaleae (Voglino) Priest, Fungi of Australia: 224. 2006.

Specimens examined: Belgium, on leaves of Rhododendron sp. (Ericaceae), J. van Holder, CBS 352.49. South Korea, Hongcheon, on leaves of Rhododendron sp., 18 Oct. 2009, H.D. Shin, KACC 44865 = CBS 128605.

Sphaerulina berberidis (Niessl) Quaedvlieg, Verkley & Crous, comb. nov. MycoBank MB804409.

Basionym: Septoria berberidis Niessl, in Rabenhorst, Bot. Ztg. 24: 411. 1866.

• = Sphaerella berberidis Auersw., in Gonnermann & Rabenhorst, Mycol. eur. Abbild. Sämmtl. Pilze Eur. 5-6: 3. 1869 (nom. nov. for Sphaeria berberis Nitschke ex Fuckel).

  • ≡ Mycosphaerella berberidis (Auersw.) Lindau, in Engler & Prantl, Nat. Pflanzenfam., Teil. I (Leipzig) 1(1): 424. 1897.

Description in vitro (CBS 116724): Colonies on OA 16-20 mm diam after 14 d, with an even, colourless margin; colonies spreading to restricted, somewhat elevated in the centre, the surface covered by a dense mat of pure white, woolly aerial mycelium; reverse in the centre dark brick to brown vinaceous, surrounded by cinnamon tinges; small amounts of a yellow to greenish pigment diffusies into the surrounding medium. Colonies on MEA 8-10 mm diam after 14 d, with an even to slighlty ruffled vinaceous buff margin; colonies restricted, pustulate, the surface ochraceous or darker, with diffuse to locally more dense finely felted grey aerial mycelium; reverse brown vinaceous to vinaceous buff. Culture remained sterile.

Specimen examined: Switzerland, Kt. Graubünden, Rodels-Realta, on Berberis vulgaris (Berberidaceae), 2 Jun. 1951, E. Müller, specimen CBS-H4984, culture CBS 324.52.

Sphaerulina betulae (Pass.) Quaedvlieg, Verkley & Crous, comb. nov. MycoBank MB804410.

Basionym: Septoria betulae Pass., Primo Elenc. Funghi Parm.: no. 52. 1867.

Specimens examined: Netherlands, Olst, leaves of Betula pubescens (Betulaceae), Sep. 2004, S. Green, CBS 116724. South Korea, Hongcheon, leaves of B. platyphylla var. japonica, 27 May 2008, H.D. Shin, CBS 128600 =KACC 43769.

Sphaerulina cercidis (Fr.) Quaedvlieg, Verkley & Crous, comb. nov. MycoBank MB804411.

Basionym: Septoria cercidis Fr., in Léveillé, Ann. Sci. Nat., Bot., Sér. 3 9: 251. 1848.

• = Septoria provencialis Crous, Stud. Mycol. 55: 127. 2006.

Specimens examined: Argentina, La Plata, on Cercis siliquastrum (Caesalpiniaceae), 12 Feb. 2008, H.D. Shin, KACC 43596 = CBS 129151; on C. siliquastrum, 1 Sep. 2007, H.D. Shin, KACC 44497 = CBS 128634. France, Provence, Cheval Blanc camping site, on leaves of Eucalyptus sp., 29 Jul. 2005, P.W. Crous, holotype of S. provincialis, CBS H-19701, culture ex-type CBS 118910. Netherlands, on C. siliquastrum, Sep. 1950, G. van den Ende, CBS 501.50.

Sphaerulina menispermi (Thüm.) Quaedvlieg, Verkley & Crous, comb. nov. MycoBank MB804412.

Basionym: Septoria menispermi Thüm., Pilzflora Siber.: no. 818. 1880.

Specimens examined: South Korea, Chuncheon, on leaves of Menispermum dauricum (Menispermaceae), 16 Jun. 2008, H.D. Shin, KACC 43848 = CBS 128761; Pyeongchang, on leaves of M. dauricum, 23 Sep. 2008, H.D. Shin, KACC 43968 = CBS 128666.

Sphaerulina musiva (Peck) Quaedvlieg, Verkley & Crous, comb. nov. MycoBank MB804413.

Basionym: Septoria musiva Peck, Ann. Rep. N.Y. St. Mus. Nat. Hist. 35: 138. 1883 [1881]

• = Mycosphaerella populorum G.E. Thomps., Phytopathology 31: 246. 1941.

  • ≡ Davidiella populorum (G.E. Thomps.) Aptroot, CBS Diversity Ser. (Utrecht) 5: 164. 2006.

• = Cylindrosporium oculatum Ellis & Everh., J. Mycol. 5(3): 155. 1889.

Specimen examined: Canada, Quebec, leaf spot of Populus deltoids (Salicaceae), J. LeBoldus, CBS 130570.

Sphaerulina oxyacanthae (Kunze & J.C. Schmidt) Quaedvlieg, Verkley & Crous, comb. nov. MycoBank MB804414. Figs ​Figs29,29, ​,3030.

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Fig. 29.

Conidia and conidiogenous cells of Sphaerulina oxyacanthae (CBS 135098). Scale bars = 10 μm.

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Fig. 30.

Sphaerulina oxyacanthae (CBS 135098). A. Leaves with leaf spots. B. Close-up of conidiomata. C. Section though conidioma. D-F. Conidiogenous cells. G. Conidia (note appendages). Scale bars: C = 150 μm, all others = 10 μm.

Basionym: Septoria oxyacanthae Kunze & J.C. Schmidt, Myk. Hefte (Leipzig) 2: 108. 1823.

• ≡ Phloeospora oxyacanthae (Kunze & J.C. Schmidt) Wallr., Fl. Crypt. Germ. (Norimbergae) 2: 117. 1833.

Leaf spots amphigenous, medium to dark brown, subcircular to angular, 1-6 mm diam, with dark brown border. Conidiomata epiphyllous, up to 150 μm diam, brown, immersed, subepidermal, opening by irregular rupture of upper layer, with 3-4 apical flaps, exuding a long crystalline flame-like cirrhus of conidia; wall 3-8 layers of brown textura angularis. On sterile Carex leaves on WA. Conidiophores reduced to conidiogenous cells, or with one supporting cell that can become fertile, forming a lateral conidiogenous locus just below the septum, 10-20 × 2.5-4 μm. Conidiogenous cells hyaline, smooth, aggregated, lining the inner cavity, terminal and lateral, ampulliform, 5-10 × 2.5-3.5 μm; proliferating several times percurrently near apex. Conidia hyaline, smooth, guttulate, 6-12-septate, falcate, widest in lower third of conidium, flexuous, apical cell tapering to subacute apex, forming a curved apical appendage-like elongation, 10-17 μm long, median cells are 5-10 μm long, basal cell forming an eccentric appendage that tapers to a subacutely rounded base, scar approximately 2-4 μm below basal septum; basal cell (incl. appendage) 11-20 μm long, conidia (60-)75-90(-100) × 2(-2.5) μm.

Culture characteristics: Colonies on PDA umbonate with undulate edge and sparse, white aerial mycelium, surface isabelline, reverse greyish sepia, after 14 d, 3 cm diam; similar on MEA and PDA.

Specimen examined: Netherlands, Wageningen, 51°57’50.43”N 5°41’0.41”E, on leaves of Crataegus sp. (Rosaceae), Sep. 2012, W. Quaedvlieg (CBS H-21291, culture CBS 135098 =S654).

Notes: Several septoria-like species have been described from leaves of Crataegus (Farr & Rossman 2013). The present collection matches the description of Septoria oxyacanthae (leaf spots on Crataegus oxyacantha in Germany, conidia 8-12-septate; conidial dimensions not given). Unfortunately we have been unable to locate type material of this species.

Sphaerulina patriniae (Miura) Quaedvlieg, Verkley & Crous, comb. nov. MycoBank MB804415.

Basionym: Septoria patriniae Miura, Flora of Manchuria and East Mongolia, III Cryptogams, Fungi (Industr. Contr. S. Manch. Rly 27) 3: 465. 1928.

Specimen examined: South Korea, Pocheon, on leaves of Patrinia scabiosaefolia (Valerianaceae), 20 Aug. 2006, H.D. Shin, KACC 42518 = CBS 128653.

Sphaerulina populicola (Peck) Quaedvlieg, Verkley & Crous, comb. nov. MycoBank MB804416.

Basionym: Septoria populicola Peck, Ann. Rep. N.Y. St. Mus. 40: 59. 1887.

• = Septoria populicola House, Bull. N.Y. St. Mus.: 59. 1920. (nom. illegit.)

• = Mycosphaerella populicola C.H. Thomps., Phytopathology 31: 251. 1941.

Specimen examined: USA, Washington, Puyallup, on Populus trichocarpa (Salicaceae), 2 May 1997, G. Newcombe, CBS 100042.

Sphaerulina pseudovirgaureae Quaedvlieg, Verkley & Crous, sp. nov. MycoBank MB804417. Figs ​Figs31,31, ​,3232.

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Fig. 31.

Conidia, conidiogenous loci on a hypha, and conidiogenous cells of Sphaerulina pseudovirgaureae (CBS 135109). Scale bars = 10 μm.

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Fig. 32.

Sphaerulina pseudovirgaureae (CBS 135109). A. Conidiomata forming in culture. B. Conidiogenous cells. C. Microcyclic conidiation. D. Conidia. Scale bars = 10 μm.

Etymology: Named after its similarity to Septoria virgaureae.

Conidiomata pycnidial, separate, erumpent, globose, up to 120 μm diam, dark brown, exusing a creamy conidial cirrhus through central ostiole, somewhat papillate; wall of 2-3 laters of brown textura angularis. Conidiophores reduced to conidiogenous cells or with one supporting cell, subcylindrical, 0-1-septate, branched below or not, pale brown at base, 10-20 × 3-5 μm. Conidiogenous cells integrated, hyaline, but pale brown at base, smooth, proliferating sympodially near apex, 7-17 × 2-3 μm. Conidia solitary, hyaline, smooth, guttulate, subcylindrical to narrowly obclavate, scolecosporous, irregularly curved, apex subobtuse, base truncate or narrowly obconically truncate, 3-10-septate, (30-)40-60(-80) × 2.5(-3) μm.

Culture characteristics: Colonies spreading, erumpent with sparse aerial mycelium and smooth, lobate margin and folded surface; reaching 13 mm diam after 2 wk. On MEA surface saffron with patches of dirty white, reverse saffron to orange; on PDA surface and reverse saffron; on OA surface saffron.

Specimen examined: Netherlands, Nijmegen, de Duffelt, on leaves of Solidago gigantea (Asteraceae), Aug. 2012, S. Videira (holotype CBS H-21327, culture ex-type CBS 135109 =S669).

Notes: Several septoria-like species have been recorded on Solidago (Farr & Rossman 2013). Of these taxa Sphaerulina pseudovirgaureae is most similar to Septoria virguareae (conidia 80-100 × 1.5 μm) except that its conidia are shorter and wider.

Sphaerulina quercicola (Desm.) Quaedvlieg, Verkley & Crous, comb. nov. MycoBank MB804419. Figs ​Figs33,33, ​,3434.

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Fig. 33.

Ascospores and asci of Sphaerulina quercicola (CBS 113266). Scale bar = 10 μm.

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Fig. 34.

Sphaerulina quercicola (CBS 663.94). A. Leaves with leaf spots. B. Close-up of lesion. C. Conidiogenous cells. D. Conidia. Scale bars = 10 μm.

Basionym: Septoria incondita var. quercicola Desm., Ann. Sci. nat., Sér. 3, Bot. 20: 95. 1853.

• • ≡ Septoria quercicola (Desm.) Sacc., Michelia 1: 174. 1879.

  • ≡ Phleospora quercicola (Desm.) Sacc., in P. A. Saccardo & D. Saccardo, 1906. Syll. Fung. 18: 490. 1906.

• = Septoria quercina Fautr., in Fautrey & Lambotte, Revue Mycol. 17: 170. 1895 (nom. illeg., art. 53; non Desmazières, 1847). Nom. nov. pro Septoria quercicola f. macrospora Roum., Revue Mycol. 13: 80. 1891.

Description in vivo. Symptoms definite, small hologenous leaf spots, scattered or in clusters, in the centre orange brown, pale yellowish brown to white, usually delimited by a blackened, somewhat elevated zone, the surrounding leaf tissues becoming red or yellow. Conidiomata pycnidial or acervuloid, one to a few in each leafspot, scattered, semi-immersed, predominantly hypophyllous, pale to dark brown, lenticular to globose, 100-200 μm diam; ostiolum often not well-developed, initially circular, central, soon opening widely, lacking distinctly differentiated cells; conidiomatal wall composed of textura angularis without distinctly differentiated layers and sometimes only well-developed in the lower part of the conidioma, mostly 10-15 μm thick, the outer cells with brown, somewhat thickened walls and 4.5-8 μm diam, the inner cells hyaline, thin-walled, 3-8 μm diam. Conidiogenous cells hyaline, discrete or integrated in simple, short, (1-)3-5-septate conidiophores which may be branched at the base, doliiform, cylindrical, or ampuliform, hyaline, holoblastic, proliferating percurrently with one to several, more or less distinct annellations, or sympodially, sometimes both types of proliferation occurring in a single conidiogenous cell, 4.5-16(-22.5) × 3-4.5 μm. Conidia cylindrical, curved or flexuous, broadly rounded at the apex which is provided with a cap of mucilaginous material, attenuated gradually to a broadly or more narrowly truncate base which often is also provided with an amorphous mass of mucilaginous material, hyaline, (0-)1-3-septate, constricted around the septa, sometimes at one or more septa also some amorphous mucilaginous material may be present, contents with numerous small oil droplets, (32.5-)38-50(-65) × 3-4 μm. Ascomata not clearly associated with leaf spots, pseudothecial, predominantly hypophyllous, black, subepidermal, erumpent to superficial, globose, 100-150 μm diam; apical ostiole 5-10 μm wide; wall consisting of 2-3 layers of medium brown textura angularis. Asci aparaphysate, fasciculate, bitunicate, subsessile, broadly ellipsoidal to subcylindrical, straight to slightly curved, 8-spored, 35-50 × 9-12 μm. Ascospores tri- to multiseriate, overlapping, hyaline, guttulate, thin-walled, curved, rarely straight, fusoid-ellipsoidal with obtuse ends, widest at septum or just above, medianly 1-septate, not constricted at the septum, tapering towards both ends, (13-)15-18(-20) × (3.5-)4-4.5(-5) μm (av. 17 × 4.5 μm).

Culture characteristics: Colonies on OA reaching 5-7 mm diam in 21 d, with an even to undulating, colourless margin; colonies restricted, irregularly pustulate, immersed mycelium appearing dark greyish to olivaceous black, rosy buff near the margin, covered mostly with a dense mat of woolly, pure white or greyish aerial mycelium; reverse in the centre brown vinaceous or more greyish black, surrounded by brick to rosy buff. Pycnidia developing on the agar surface in the centre, releasing droplets of rosy-buff conidial slime. Colonies on MEA reaching 4-6(-8) mm diam in 21 d, with an even, to irregularly undulating margin which is mostly hidden under the aerial mycelium; colonies restricted, irregularly pustulate, the surface mostly blackish or very dark grey, covered by dense to diffuse, finely felted, white aerial mycelium; reverse mostly olivaceous black, near the margin cinnamon to buff. Numerous single and aggregated pycnidia developing on the colony surface in the centre, releasing milky white to rosy buff conidial slime. Conidia as in planta (CBS 663.94) though on average considerably longer, 51.5-74.5 × 3-4(-4.5) μm (OA), the apex, base and area around septa normally both provided with mucilaginous material as described above, (0-)1-3(-5)-septate.

Specimens examined: Austria, endophyte culture ex twig of Quercus petraea (Fagaceae), Aug. 1991, E. Halmschlager 212 (H. A. van der Aa 10986), CBS 456.91. France, loc. unknown, on leaves of Quercus sp. (“divers Chênes”), distributed in Desmazières, Pl. crypt. Fr., Fasc. 43, no. 2193 (PC, type of Septoria incondita var. quercicola Desm.). Netherlands, Utrecht, Baarn, on living leaves of Q. robur, 11 Aug. 1994, G. Verkley 225 (CBS H-21188), living culture CBS 663.94; prov. Utrecht, Soest, De Stompert, on living leaves of Q. rubra, 15 Aug. 1995, G. Verkley 310 (CBS H-21189), CBS 791.95; Same loc., dead fallen leaves of Q. robur, Apr. 2003, G. Verkley s.n., single ascospore-isolate CBS 113266 (’Crous 3’); Same loc., G. Verkley & I. van Kempen, endophyte isolates ex green leaves of Q. robur CBS 115016, 115136, 115137; Prov. Gelderland, Amerongen, Park Kasteel Amerongen, leaf spot of Q. rubra, 11 Jul. 2000, G. Verkley 973 (CBS H-21231), living culture CBS 109009; Prov. Utrecht, Amelisweerd, on dead leaves of Q. robur, 25 Apr. 2005, G. Verkley 3108A, culture CBS 117803, CPC 12097.