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Runa, F., Park, M. S., and Pryor, B. M. 2009. Ulocladium Systematics

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Runa, F., Park, M. S., and Pryor, B. M. 2009. Ulocladium Systematics Mycol Progress (2009) 8:35–47 DOI 10.1007/s11557-008-0576-y ORIGINAL ARTICLE Ulocladium systematics revisited: phylogeny and taxonomic status Farhana Runa & Myung Soo Park & Barry M. Pryor Received: 15 June 2008 /Revised: 3 October 2008 /Accepted: 17 October 2008 / Published online: 13 November 2008 # German Mycological Society and Springer-Verlag 2008 Abstract The genus Ulocladium represents phaeodic- in shape. However, A. cheiranthi and E. indefessa also tyosporic Hyphomycetes that produce conidia that are clustered within this group with high bootstrap support but essentially obovoid in shape. Previous molecular studies did not posses this diagnostic feature. This paraphyletic that included Ulocladium and related taxa in Alternaria, clade resolved basal to the core Alternaria clade with high Embellisia, and Stemphylium revealed a conflict between bootstrap support, unlike previous studies in which its morphology and phylogeny, and Ulocladium was supported position was imbedded within the primary Alternaria clade. as polyphyletic with a paraphyletic core group. Moreover, Thus, the status of the genus as an independent lineage and the genus consistently resolved within a larger Alternaria/ a unique taxon is strongly supported. As previously Ulocladium clade, resulting in paraphyly of Alternaria and reported, U. alternariae and U. oudemansii, which posses questions as to the taxonomic status of Ulocladium. In the the key conidium characteristics of Ulocladium, clustered present study, 13 Ulocladium species and three genetic loci as a separate clade sister to the core Ulocladium clade. were included for a more comprehensive systematic Further studies are necessary to determine if these taxa analysis of the genus than had previously been conducted. represent an independent lineage or share a common Total genomic DNA was extracted from representative taxa ancestor with other Ulocladium species. Obovoid conidia and sequences were determined for the nuclear internal were poorly represented in the isolate of U. lanuginosum transcribed spacer region, including the 5.8S rDNA gene, that was included in these analyses (the only U. lanugino- and the protein-coding genes glyceraldehyde-3-phosphate sum isolate currently available), and the isolate resolved as dehydrogenase and Alt a1. Subsequent phylogenetic anal- A. radicina based upon all three loci sequenced. Based yses based on maximum parsimony and Bayesian methods upon these data and the origin of the isolate, which was included related Alternaria, Embellisia, and Stemphylium originally deposited as A. malvae, a reassessment of its spp. Results supported previous findings of polyphyletic identity is supported. and paraphyletic relationships of Ulocladium among other taxa. Ten Ulocladium species clustered into a core Keywords Ulocladium . ITS . gpd . Alt a1 . Parsimony. Ulocladium clade and all taxa possessed the key diagnostic Bayesian inference feature of Ulocladium, namely, conidia essentially obovoid Introduction F. Runa : M. S. Park : B. M. Pryor (*) Department of Plant Sciences, Division of Plant pathology The genus Ulocladium represents anamorphic fungi in the and Microbiology, University of Arizona, Tucson, AZ 85721–0036, USA Pleosporaceae, mostly found as common saprobes on plant e-mail: [email protected] material and in soil. Species can also be recovered from diverse substrates, such as plant debris, lumber, paper, and Present address: water-damaged building materials (Gravesen et al. 1999; M. S. Park Korea Research Institute of Chemical Technology, Simmons 1967; Andersen and Hollensted 2008). Ulocla- Yusong, PO Box 107, Daejon, Korea dium spores are primarily dispersed by air and are known to 36 Mycol Progress (2009) 8:35–47 be common airway allergens (Al-Suwaine et al. 1999). In Embellisia revealed by Simmons (1992) proposed a close addition, some species have been reported as opportunistic relationship to Alternaria and other allied genera in the human pathogens (de Hoog and Horre 2002). Pleosporaceae. However, the synonomies required during The genus Ulocladium was first established by Preuss the erection of Embellisia suggested taxonomic placement (1851) with U. botrytis as the type. Species are represented may not be without some taxonomic uncertainty. by dematiaceous phaedictyosporic Hyphomycetes with In most previous studies involving Ulocladium, the conidia essentially obovoid in shape. Related genera such phylogenetic status of the genus has only peripherally been as Alternaria and Stemphylium are also been characterized discussed as such studies were focused primarily on allied by the production of dematiaceous phaedictyospores (Nees taxa of Alternaria, Embellisia,orStemphylium. Based on 1816; Elliot 1917; Joly 1964; Neegard 1945; Simmons the analysis of the nuclear internal-transcriber spacer (ITS), 1967; and Wiltshire 1933) and early taxonomy for this mitochondrial small subunit (mt SSU), glyceraldehydes-3- group of fungi was complicated because of gross similar- phosphate dehydrogenase (gpd) sequences and the Alter- ities in conidium morphology among genera. As a naria allergen gene Alt a1 (Pryor and Gilbertson 2000; consequence, many species have been placed into more Chou and Wu 2002; de Hoog and Horre 2002; Pryor and than one of these genera since their initial description and Bigelow 2003; Hong and Pryor 2005), a large monophy- the taxonomy of these fungi, especially Ulocladium, letic clade comprising Alternaria, Ulocladium, and Embel- evolved with considerable historical controversy. For lisia was supported with Stemphylium as the sister taxa. example, before a formal description of the genus Ulocla- Ulocladium was revealed as polyphyletic within the para- dium, the type, Ulocladium botrytis, had been known by the phyletic clade of Alternaria, Ulocladium, and Embellisia.A synonyms Stemphylium botryosum Wallr. var. Ulocladium core Ulocladium clade was revealed that included four Sacc., v.s. and Stemphylium botryosum Wallr. var. botrytis species of Ulocladium, which possess the key taxonomic (Pr.) Lindau, v.s. Following circumscription of the genus by character of obovoid conidia, but also two other species, Preuss with two described species, few additional taxa were Alternaria cherianthi and Embellisia indefessa, which do added in the years following and the genus was infrequent- not possess the key taxonomic character. In addition, U. ly mentioned. In 1967, the genus Ulocladium was reviewed alternariae, which does possess the key taxonomic charac- by Simmons in his seminal paper “Typification of Alter- ter, did not cluster within the core Ulocladium clade. naria, Stemphylium and Ulocladium” (Simmons 1967). Moreover, the primary Ulocladium clade appeared to be Species of these three genera were reviewed based upon imbedded within a larger Alternaria clade resulting in morphological characteristics and compared with the type paraphyly of Alternaria and uncertainty as to the phyloge- for each genus. It was concluded that several atypical netic status of a distinct Ulocladium genus. Indeed, in a Alternaria and Stemphylium species should actually be recent study by Xue and Zhang (2007), which was focused classified as Ulocladium and seven additional species were primarily on Ulocladium and was perhaps the most included in the genus, the first additions in over 100 years. comprehensive review of the genus to date (seven previ- Simmons highlighted that the fundamentally obovoid and ously described species and one newly described species), nonbeaked conidia (i.e., do not taper distally) are the principal molecular data based on the nuclear ITS rDNA region and morphological characteristics that distinguishes Ulocladium the glyceraldehyde-3-phospate dehydrogenase (gpd) gene from Alternaria and other related genera (Simmons 1967). continued to support a polyphyletic and paraphyletic However, this distinguishing character is often best viewed Ulocladium lineage which did not resolve independent only in immature conidia and may subsequently be lost as the from the genus Alternaria. Thus, as continued conflict was conidia mature. Moreover, ellipsoidal and spherical forms revealed between morphology and phylogeny of Ulocla- may also be common in some species, particularly among dium species, it became important to further examine the mature conidia. In regard to Stemphylium, species could be phylogenetic status of Ulocladium and its relationship with readily differentiated from Ulocladium on the basis of the allied taxa and provide additional perspectives on the conidiophores apex and the percurrently proliferating conid- disposition of the genus, especially as it relates to iophore, which are the major morphological characteristic Alternaria. that distinguishes Stemphylium from other phaedictyosporic The objective of the present study was to continue to Hyphomycetes (Simmons 1969). explore phylogeny and the taxonomic status of Ulocladium Another genus with ties to Ulocladium, Alternaria and species based on additional taxa and additional genetic loci Stemphylium is Embellisia Simmons. These phaeosporic for phylogenetic analyses. Relationships among most Hyphomycetes have conidia that are morphologically described Ulocladium spp. and a number of related reminiscent of both phragmosporic Helminthosporium Alternaria, Embellisia and Stemphylium spp. were exam- species and dictyosporic Alternaria species (Simmons ined based on sequences from nuclear rDNA internal 1971). Description of the diagnostic characteristics of transcriber spacer (ITS) region and two protein
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