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Hormoconis resinae and morphologically similar taxa The large subunit matrix was assembled from the closest BLAST matches using our sequences for the three fungi of interest, S. resinae, A. resinae and S. azaleae; Golovinomyces cichoracearum was added as an out-group to root the tree. Although these sequences were put into a single matrix, there is no implication that this data set represents the diversity of the Ascomycota. The alignment was calculated using MAFFT (Katoh et al. 2002) and adjusted using Se-Al (Sequence Alignment Program v. 1.d1; http://evolve.zoo.ox.ac.uk/software/Se-Al/main.html) to maximise homology. The internal transcribed spacers alignment including Sorocybe resinae was derived from an alignment of Capronia and related anamorphs used by Davey & Currah (2007), originally produced using MAFFT. This data set was modified considerably using Se- Al to maximise homology, but still included several areas where the homology of aligned sequences was difficult to evaluate. ITS sequences of Amorphotheca resinae were used to retrieve closely related sequences using a BLAST search of GenBank, and these relevant sequences were added to an alignment of Oidiodendron Robak sequences from the study of Hambleton et al. (1998), and then adjusted using Se-Al. We attempted direct PCR from two specimens containing only the putative mononematous synanamorph of Sorocybe resinae (DAOM 228772a, 228573a), to allow comparison of sequences obtained from cultures of the synnematous synanamorph. These attempts, using the same methods outlined above, were unsuccessful. RESULTS Cultural characters and micromorphology Most micromorphological characters of the resin fungus Sorocybe resinae (Partridge & Morgan-Jones 2002), the creosote fungus Amorphotheca resinae (Parbery 1969, de Vries 1952, 1955, Ho et al. 1999) and the rhododendron fungus Seifertia azaleae (Ellis 1976, Partridge & Morgan-Jones 2002, Glawe & Hummel 2006) are well-described in the literature and will not be repeated here. The three species are readily distinguished based on growth rates and overall cultural phenotypes. Agar colonies of Sorocybe resinae are coal-black, wrinkled, and restricted in growth, no matter what agar medium is employed; even after 3 mo, the colonies are rarely more than 2 cm diam (Fig. 2C). Synnemata did not form in our cultures; in vivo, the synnemata produce branched, acropetal chains of conidia with laterally thickened walls (Figs 2D–G). No thickened, refractive or darkened secession scars were evident on individual conidia or ramoconidia. Conidial masses were removed from the mononematous and synnematous parts of a freshly collected specimen (DAOM 56088a) and grown on PDA and sterilised conifer wood. There were no discernable differences between colonies derived from the two types of conidiophores, in all cases yielding restricted black colonies, or in their microscopic characters. Therefore, we conclude that these two types of conidiophores represent synanamorphs of one fungus. An identical conclusion was reached by Partridge & Morgan-Jones (2002). We documented the occurrence of this fungus in California, Oregon, and Washington State, U.S.A. and British Columbia, Canada, on resinous exudates on Abies nobilis, Picea sitchensis, Pseudotsuga menziesii and Tsuga heterophylla. Microscopic features from the holotype specimen of Hormodendrum resinae Lindau are shown in Fig. 3. Dark, thickwalled conidiophore stipes give rise to branched, acropetally www.studiesinmycology.org developing conidial chains. The conidia are relatively darkly pigmented, and the lateral walls are more conspicuously thickened and darkened than the polar walls. There are no obvious thickened, refractive or darkened secession scars on any of the cells. Apart from the production of synnemata, the characters of the conidia and conidium ontogeny are identical in Lindau’s specimen and the synnematous specimens of Sorocybe resinae examined. In contrast, both the resin fungus and the rhododendron fungus have spreading rather than restricted agar colonies. Cultures of the resin fungus are sandy brown (Kornerup & Wanscher 1989), planar and powdery, growing 4–4.5 cm diam in 10 d on PDA (Fig. 1A). Cultures of the rhododendron fungus are slower, growing 2.5–3.5 cm diam after 21 d on MEA (not shown). They are planar and greyish brown, with an orange-brown reverse. No synnemata were observed in our cultures of the rhododendron fungus on MEA, OA or PDA, but cladosporium-like conidiation occurred in the aerial mycelium. Phylogeny The large subunit analysis (LSU) was used to demonstrate the general phylogenetic relationships of the resin fungus Sorocybe resinae (DAOM 239134), the creosote fungus Amorphotheca resinae (DAOM 170427, 194228) and the rhododendron fungus Seifertia azaleae (DAOM 239136), and subsequent analyses of the internal transcribed spacers were used to estimate more precise affinities. Fig. 4 shows the LSU analysis and demonstrates that Sorocybe resinae appears to be a member of the Herpotrichiellaceae, Chaetothyriales, A. resinae is related to the inoperculate discomycetes (Leotiomycetes) and Seifertia azaleae is most closely related to a sequence labelled Mycosphaerella mycopappi A. Funk & Dorworth, which is unrelated to Mycosphaerella s. str. For the ITS alignment of Sorocybe resinae, two preliminary parsimony analyses were conducted, one with informative characters from the full alignment, the second with a subset with 179 characters excluded from seven ambiguously aligned regions. The consistency indices (full 0.301, partial 0.324), tree topologies, and bootstrap supports for the two analyses were relatively similar. Therefore, the complete alignment was used for the tree presented here (Fig. 5). The data matrix included 57 taxa, with 352 of 752 characters phylogenetically informative. Sorocybe resinae clearly is related to Capronia and allied anamorph genera, as suggested by the LSU analysis. In the ITS analysis (Fig. 6) it forms a wellsupported clade with C. villosa Samuels, that is a well-supported sister group to species now in three different anamorph genera, Phaeococcomyces nigricans (M.A. Rich & A.M. Stern) de Hoog, Ramichloridium cerophilum, and an undescribed species of Heteroconium Petr. The ITS matrix for A. resinae included 42 taxa, with 171 phylogenetically informative characters in the 530 base alignment. The phylogenetic analysis confirmed the relationship of this species with the Leotiomycetes, and provided a more precise hypothesis of its family-level relationships (Fig. 6). Amorphotheca resinae DAOM 170427 and 194228 had identical ITS sequences to another strain of the same species reported in GenBank (AY251067, from Braun et al. 2003), and one bp substitution from a second strain (AF393726 based on the isotype ATCC 200942 = CBS 406.68). These four sequences formed a sister group to two sequences of “Cladosporium” breviramosum Morgan- Jones (AF393683, AF393684). The well-supported clade of A. resinae and C. breviramosum, which represent the proposed family Amorphothecaceae, was previously noted by Braun et al. (2003). The nesting of this clade within two well-supported 241
Seifert et al. 100 76 99 99 100 AY064704 Neofabraea alba AF281377 Neofabraea alba AF281397 Neofabraea perennans AF281388 Neofabraea malicorticis AF281365 Neofabraea krawtzewii AY129289 Pseudeurotium ovale var. ovale AY129290 Pseudeurotium ovale var. milkoi AY129287 Pseudeurotium bakeri AY129286 Pseudeurotium zonatum AY129288 Pseudeurotium desertorum AF307760 Geomyces pannorum AJ390390 Geomyces asperulatus AY789290 Heyderia abietis Z81441 Piceomphale bulgarioides AY781230 Leptodontidium elatius AY348594 Calycina herbarum AF062802 Oidiodendron periconioides 99 100 79 99 88 100 100 89 88 100 98 100 AF062787 Oidiodendron pilicola AF062798 Oidiodendron maius AF062790 Oidiodendron citrinum AF062789 Oidiodendron chlamydosporicum AF062797 Oidiodendron griseum AF307774 Oidiodendron tenuissimum AF062792 Oidiodendron flavum AF062810 Myxotrichum arcticum AF062809 Oidiodendron truncatum AF062808 Oidiodendron tenuissimum AF062805 Oidiodendron setiferum AF062788 Oidiodendron cerealis AJ635314 Oidiodendron myxotrichoides AF062811 Myxotrichum cancellatum AF062817 Byssoascus striatisporus AF062803 Oidiodendron rhodogenum AF062814 Myxotrichum deflexum 88 A. resinae DAOM 170427, 194228, EU030278-9 AF393726 Amorphotheca resinae isotype AY251067 Amorphotheca resinae AF393684 Cladosporium breviramosum AF393683 Cladosporium breviramosum AF062813 Myxotrichum chartarum AF062812 Myxotrichum carminoparum AF062816 Myxotrichum stipitatum 5 changes Fig. 5. Parsimony analysis of internal transcribed spacers sequences, demonstrating the position of Amorphotheca resinae (shown in bold) in the ascomycete family Myxotrichaceae. One of 44 equally parsimonious trees (645 steps, CI = 0.460, RI = 0.758, RC = 0.349, HI = 0.540) with mid-point rooting. Bootstrap values above 70 % are shown at the relevant nodes; branches with thick lines occurred in all equally parsimonious trees. Myxotrichaceae Pseudeurotiaceae clades of Myxotrichum spp. and the associated anamorph genus Oidiodendron, which comprise the family Myxotrichaceae, has not been documented previously. The ITS sequences of two strains of Seifertia azaleae were 474 bp and differed by one bp. BLAST searches with these sequences revealed significant homologies only with unidentified fungi, and lower probability matches with various members of the Dothideomycetes. Therefore, no taxonomically meaningful phylogenetic analysis can be presented with these ITS sequences. The species does seem to have affinities with the Dothideomycetes, but the putative relationship with Mycosphaerella, suggested by the LSU analysis, could not be confirmed with the ITS analysis. DISCUSSION Micromorphological comparisons, differences in culture characters, and phylogenetic analysis all support the conclusion that the mononematous synanamorph of Sorocybe resinae, the resin fungus, is different from the anamorph of Amorphotheca resinae, the creosote fungus. Based on ribosomal DNA sequences, the creosote fungus is related to the family Myxotrichaceae, the genus Myxotrichum and its Oidiodendron anamorphs (Fig. 5). In this gene tree, Myxotrichum and the Myxotrichaceae are paraphyletic, with Amorphotheca and the Amorphothecaceae nested within them. Sorocybe appears to be an additional anamorph genus phylogenetically associated with Capronia (Herpotrichiellaceae, Chaetothyriales, Fig. 6). The genetic connection between the synnematous and mononematous morphs of S. resinae was verified by morphological comparison of polyspore isolates derived from the two synanamorphs. However, the living cultures are no longer available and the connection was not confirmed with single conidium isolations. The type specimen of Hormodendrum resinae (Fig. 3) is the basis for the application of the most frequently used anamorph epithet for the creosote fungus. This specimen represents the mononematous synanamorph of Sorocybe resinae, not the anamorph of Amorphotheca resinae. It is difficult to understand how these two fungi were confused when their micromorphologies are so different. The conidia are of the same general size and shape, but in both morphs of Sorocybe resinae (Figs 2D–G, 3C), the lateral walls are conspicuously thickened, a condition not present in the creosote fungus (Fig. 1C), and the conidia are much darker. In his monograph of Cladosporium, de Vries (1952) noted that single conidium isolates of C. avellaneum gave rise to four different colony types. In 1955, he extended these observations and decided that the much darker resin fungus was 242
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Studies in Mycology 58 (2007) The g
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Studies in Mycology The Studies in
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CONTENTS P.W. Crous, U. Braun and J
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lectotype for the genus by Clements
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Schubert K (2005a). Morphotaxonomic
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Crous et al. Table 1. Isolates for
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Crous et al. Table 1. (Continued).
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Crous et al. 100 10 changes 65 100
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Crous et al. Treatment of phylogene
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Crous et al. Teratosphaeria bellula
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Crous et al. 6. Conidiophores short
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Crous et al. Habit plant pathogenic
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Crous et al. Fig. 7. Catenulostroma
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Crous et al. system, consisting of
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Crous et al. Fig. 9. Penidiella col
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Crous et al. Fig. 12. Penidiella ri
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Crous et al. conidiophores, about 1
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Crous et al. have conidiomata rangi
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Crous et al. Schizothyriaceae clade
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Crous et al. Fig. 21. Stigmidium sc
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Crous et al. Gams W, Verkley GJM, C
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Crous et al. Table 1. Isolates for
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Crous et al. 100 61 100 52 100 10 c
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Crous et al. Fig. 3. Rachicladospor
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Crous et al. Fig. 4. Toxicocladospo
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Crous et al. Fig. 5. Verrucocladosp
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Crous et al. Fig. 7. Stenella aragu
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Crous et al. Helotiales, incertae s
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Crous et al. Fig. 10. Ochrocladospo
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Crous et al. Fig. 12. Rhizocladospo
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Crous et al. 7. Conidiophores unbra
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Crous et al. 33. Terminal conidioge
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Crous et al. Crous PW, Kang JC, Bra
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Arzanlou et al. To date 26 species
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Arzanlou et al. Table 1. (Continued
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Arzanlou et al. 10 changes Athelia
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Arzanlou et al. Athelia epiphylla A
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Arzanlou et al. Fig. 3. Periconiell
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Arzanlou et al. Cultural characteri
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Arzanlou et al. Fig. 10. A. Ramichl
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Arzanlou et al. Ramichloridium musa
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Arzanlou et al. Fig. 20. Rhinocladi
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Arzanlou et al. Fig. 22. Rhinocladi
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Arzanlou et al. Rhinocladiella mack
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Arzanlou et al. Fig. 26. Veronaea c
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Arzanlou et al. Fig. 30. Myrmecridi
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Arzanlou et al. Fig. 32. Radulidium
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Arzanlou et al. Fig. 34. Rhodoveron
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Arzanlou et al. even further, thoug
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available online at www.studiesinmy
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Dichocladosporium gen. nov. 10 chan
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Dichocladosporium gen. nov. Fig. 3.
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Dichocladosporium gen. nov. to intr
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Dichocladosporium gen. nov. Czechos
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Cladosporium herbarum species compl
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Cladosporium sphaerospermum species
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Crous et al. The aim of the present
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Crous et al. 10 changes Athelia epi
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Page 230 and 231: Cladophialophora carrionii complex
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Page 246 and 247: Hormoconis resinae and morphologica
Page 252 and 253: Fig. 6 Hormoconis resinae and morph
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Page 258 and 259: Fusicladium phillyreae, 189 c , 191
Page 260 and 261: Ramichloridium epichloës, 60, 89 P
Page 262: Trimmatostroma salicis, 3 t , 5, 6
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