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      Acremonium phylogenetic overview and revision of Gliomastix, Sarocladium, and Trichothecium

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          Abstract

          Over 200 new sequences are generated for members of the genus Acremonium and related taxa including ribosomal small subunit sequences (SSU) for phylogenetic analysis and large subunit (LSU) sequences for phylogeny and DNA-based identification. Phylogenetic analysis reveals that within the Hypocreales, there are two major clusters containing multiple Acremonium species. One clade contains Acremonium sclerotigenum, the genus Emericellopsis, and the genus Geosmithia as prominent elements. The second clade contains the genera Gliomastix sensu stricto and Bionectria. In addition, there are numerous smaller clades plus two multi-species clades, one containing Acremonium strictum and the type species of the genus Sarocladium, and, as seen in the combined SSU/LSU analysis, one associated subclade containing Acremonium breve and related species plus Acremonium curvulum and related species. This sequence information allows the revision of three genera. Gliomastix is revived for five species, G. murorum, G. polychroma, G. tumulicola, G. roseogrisea, and G. masseei. Sarocladium is extended to include all members of the phylogenetically distinct A. strictum clade including the medically important A. kiliense and the protective maize endophyte A. zeae. Also included in Sarocladium are members of the phylogenetically delimited Acremonium bacillisporum clade, closely linked to the A. strictum clade. The genus Trichothecium is revised following the principles of unitary nomenclature based on the oldest valid anamorph or teleomorph name, and new combinations are made in Trichothecium for the tightly interrelated Acremonium crotocinigenum, Spicellum roseum, and teleomorph Leucosphaerina indica. Outside the Hypocreales, numerous Acremonium-like species fall into the Plectosphaerellaceae, and A. atrogriseum falls into the Cephalothecaceae.

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          Phylogenetic classification of Cordyceps and the clavicipitaceous fungi

          Cordyceps, comprising over 400 species, was historically classified in the Clavicipitaceae, based on cylindrical asci, thickened ascus apices and filiform ascospores, which often disarticulate into part-spores. Cordyceps was characterized by the production of well-developed often stipitate stromata and an ecology as a pathogen of arthropods and Elaphomyces with infrageneric classifications emphasizing arrangement of perithecia, ascospore morphology and host affiliation. To refine the classification of Cordyceps and the Clavicipitaceae, the phylogenetic relationships of 162 taxa were estimated based on analyses consisting of five to seven loci, including the nuclear ribosomal small and large subunits (nrSSU and nrLSU), the elongation factor 1α (tef1), the largest and the second largest subunits of RNA polymerase II (rpb1 and rpb2), β-tubulin (tub), and mitochondrial ATP6 (atp6). Our results strongly support the existence of three clavicipitaceous clades and reject the monophyly of both Cordyceps and Clavicipitaceae. Most diagnostic characters used in current classifications of Cordyceps (e.g., arrangement of perithecia, ascospore fragmentation, etc.) were not supported as being phylogenetically informative; the characters that were most consistent with the phylogeny were texture, pigmentation and morphology of stromata. Therefore, we revise the taxonomy of Cordyceps and the Clavicipitaceae to be consistent with the multi-gene phylogeny. The family Cordycipitaceae is validated based on the type of Cordyceps, C. militaris, and includes most Cordyceps species that possess brightly coloured, fleshy stromata. The new family Ophiocordycipitaceae is proposed based on Ophiocordyceps Petch, which we emend. The majority of species in this family produce darkly pigmented, tough to pliant stromata that often possess aperithecial apices. The new genus Elaphocordyceps is proposed for a subclade of the Ophiocordycipitaceae, which includes all species of Cordyceps that parasitize the fungal genus Elaphomyces and some closely related species that parasitize arthropods. The family Clavicipitaceae s. s. is emended and includes the core clade of grass symbionts (e.g., Balansia, Claviceps, Epichloë, etc.), and the entomopathogenic genus Hypocrella and relatives. In addition, the new genus Metacordyceps is proposed for Cordyceps species that are closely related to the grass symbionts in the Clavicipitaceae s. s. Metacordyceps includes teleomorphs linked to Metarhizium and other closely related anamorphs. Two new species are described, and lists of accepted names for species in Cordyceps, Elaphocordyceps, Metacordyceps and Ophiocordyceps are provided.
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              The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits.

              We present a 6-gene, 420-species maximum-likelihood phylogeny of Ascomycota, the largest phylum of Fungi. This analysis is the most taxonomically complete to date with species sampled from all 15 currently circumscribed classes. A number of superclass-level nodes that have previously evaded resolution and were unnamed in classifications of the Fungi are resolved for the first time. Based on the 6-gene phylogeny we conducted a phylogenetic informativeness analysis of all 6 genes and a series of ancestral character state reconstructions that focused on morphology of sporocarps, ascus dehiscence, and evolution of nutritional modes and ecologies. A gene-by-gene assessment of phylogenetic informativeness yielded higher levels of informativeness for protein genes (RPB1, RPB2, and TEF1) as compared with the ribosomal genes, which have been the standard bearer in fungal systematics. Our reconstruction of sporocarp characters is consistent with 2 origins for multicellular sexual reproductive structures in Ascomycota, once in the common ancestor of Pezizomycotina and once in the common ancestor of Neolectomycetes. This first report of dual origins of ascomycete sporocarps highlights the complicated nature of assessing homology of morphological traits across Fungi. Furthermore, ancestral reconstruction supports an open sporocarp with an exposed hymenium (apothecium) as the primitive morphology for Pezizomycotina with multiple derivations of the partially (perithecia) or completely enclosed (cleistothecia) sporocarps. Ascus dehiscence is most informative at the class level within Pezizomycotina with most superclass nodes reconstructed equivocally. Character-state reconstructions support a terrestrial, saprobic ecology as ancestral. In contrast to previous studies, these analyses support multiple origins of lichenization events with the loss of lichenization as less frequent and limited to terminal, closely related species.
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                Author and article information

                Journal
                Stud Mycol
                simycol
                Studies in Mycology
                CBS Fungal Biodiversity Centre
                0166-0616
                1872-9797
                2011
                : 68
                : Phylogenetic revision of taxonomic concepts in the Hypocreales and other Ascomycota - A tribute to Gary J. Samuels -
                : 139-162
                Affiliations
                [1 ] Sporometrics, Inc. 219 Dufferin Street, Suite 20C, Toronto, Ont., Canada M6K 1Y9
                [2 ] Dalla Lana School of Public Health, University of Toronto, 223 College St., Toronto ON Canada M5T 1R4
                [3 ] CBS-KNAW, Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands;
                [4 ] Department of Botany, The Natural History Museum, Cromwell Road, SW7 5BD London, United Kingdom
                [5 ] Agricultural Institute of Slovenia, Hacquetova 17, 1000 Ljubljana, Slovenia, Mycology Unit, Medical School
                [6 ] IISPV, Universitat Rovira i Virgili, Reus, Spain
                Author notes
                [* ] Correspondence: Richard Summerbell, rsummerbell@ 123456sporometrics.com
                Article
                0139
                10.3114/sim.2011.68.06
                3065988
                21523192
                d9fe919b-f6a2-42a3-8197-a48be9c4a9e7
                Copyright © Copyright 2011 CBS-KNAW Fungal Biodiversity Centre

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                For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author's moral rights.

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                Plant science & Botany
                holomorph concept,cephalothecaceae,sarcopodium,sarocladium,acremonium,trichothecium,nomenclature,gliomastix,leucosphaerina

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