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PDF (Taxonomic Revision of Ustilago, Sporisorium and Macalpinomyces ) Persoonia 29, 2012: 116–132 www.ingentaconnect.com/content/nhn/pimj RESEARCH ARTICLE http://dx.doi.org/10.3767/003158512X661462 Taxonomic revision of Ustilago, Sporisorium and Macalpinomyces A.R. McTaggart1,2,3,5, R.G. Shivas1,2, A.D.W. Geering1,2,5, K. Vánky4, T. Scharaschkin1,3 Key words Abstract Morphological characters within the Ustilago-Sporisorium-Macalpinomyces complex are defined explicitly. The genera Sporisorium and Anthracocystis are emended to reflect morphological synapomorphies. smut fungi Three new genera, Langdonia, Stollia and Triodiomyces are described based on soral synapomorphies and host systematics classification. The new classification of the Ustilago-Sporisorium-Macalpinomyces complex incorporates 142 new taxonomy taxonomic combinations. Ustilaginaceae Ustilaginomycotina Article info Received: 18 May 2012; Accepted: 9 October 2012; Published: 17 December 2012. INTRODUCTION genera, Langdonia, Stollia and Triodiomyces are proposed to accommodate newly resolved clades (Fig. 1). The three genera of smut fungi, Ustilago, Sporisorium and Ma- calpinomyces, form a complex that has eluded resolution by Definitions of soral characters in the morphology (Langdon & Fullerton 1975, Vánky 1991, Piepen- Ustilago-Sporisorium-Macalpinomyces complex bring et al. 1998) and molecular phylogenetic analysis (Stoll The interpretation of soral morphology is inconsistent for many et al. 2003, 2005). Two suggestions to reconcile the taxonomy descriptions of smut species. For example, Sporisorium cons- of the complex have been proposed. The first was to break up anguineum, Macalpinomyces spermophorus and M. viridans the current taxa into several smaller genera and subgenera, were described with columellae, but these structures are not and the second to unify the three genera into a single genus, homologous with columellae in Sporisorium s.str. (McTaggart et Ustilago (Vánky 2002, Piepenbring 2004). The former solu- al. 2012a). Soral characters need accurate definition to prevent tion is dependent on finding morphological synapomorphies misinterpretation. that can delimit the genera, and the latter solution dismisses the wide morphological diversity within the group (McTaggart Columellae et al. 2012b). A columella is defined as a structure formed by both fungal and Synapomorphic morphological characters and host plant clas- host material, which proliferates after hyphal-induced growth sification delimited clades in the Ustilago-Sporisorium-Macalpi- of the host meristem, and connects the sorus to the host. The nomyces complex (McTaggart et al. 2012a). The current study columella is invariably the same length or slightly shorter than defines these synapomorphic characters and proposes a new the length of the sorus. There are two types of true columellae classification for many species currently placed in Ustilago, within the complex. Stout columellae are a synapomorphy for Sporisorium and Macalpinomyces. This approach preserves Sporisorium s.str. (Clade 1), and filiform, flexuous columellae the well-known genera Ustilago, Sporisorium and Macalpino- are a synapomorphy for Anthracocystis (Clade 4) (McTaggart myces, and enables the classification to reflect morphological et al. 2012a). The non-homologous columella-like structures diversity in the complex. found in other clades have different origins and do not satisfy the definition of columellae. In particular, care should be taken PHYLOGENY not to confuse the columella with remnants of the inflorescence, such as in Ustilago drakensbergiana. Phylogenetic analyses resolved eight clades within the Usti- lago-Sporisorium-Macalpinomyces complex (McTaggart et Sterile cells al. 2012a). Six of the clades had unique morphology or host Sterile cells are defined as the cells formed from partitioning characters. Sporisorium and Anomalomyces were accepted non-sporogenous hyphae within the sorus. Sterile cells are genera. Here Anthracocystis is reinstated, and three new an apomorphic character of the complex and were present in Macalpinomyces eriachnes, Anomalomyces panici, and Clades 1 Cooperative Research Centre for National Plant Biosecurity, GPO Box 5012, Bruce, ACT 2617, Australia; 1, 2, 3, 7 and 8 (McTaggart et al. 2012a). Sterile cells also occur corresponding author e-mail: [email protected]. in other groups of smut fungi, including Tilletia in the Exobasidio 2 Department of Agriculture, Fisheries and Forestry, Ecosciences Precinct, mycetes, and are not a valuable character for higher levels of GPO Box 267, Brisbane, Queensland 4001, Australia. classification. Cells found in the peridium are not formed from 3 EEBS, Faculty of Science and Technology, Queensland University of Technology, 2 George Street, Brisbane, Queensland 4001, Australia. partitioning hyphae and are referred to as peridial cells. Peridial 4 Herbarium Ustilaginales Vánky (HUV), Gabriel-Biel-Str. 5, D-72076 Tübin- cells are generally irregular and in chains, and are only found gen, Germany. in taxa with a fungal derived peridium. 5 Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, Ecosciences Precinct, GPO Box 267, Brisbane, Queensland Sterile cells formed from non-sporogenous hyphae within the 4001, Australia. sorus are a useful character for delimitation of genera within © 2012 Nationaal Herbarium Nederland & Centraalbureau voor Schimmelcultures You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. 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. A.R. McTaggart et al.: Taxonomic revision of Ustilago, Sporisorium and Macalpinomyces 117 Moesziomyces bullatus Macalpinomyces eriachnes 100/100 Lan. aristidicola Lan. fraseriana Lan. confusa Langdonia 1.0 Lan. aristidae /78 Mac. eragrostiellae Spo. veracruzianum Mac. spermophorus Ustilago austroafricana 97/92 Mac. viridans Ust. ixophori Mac. neglectus CLADE 7 1.0 Ust. crameri Spo. panici Ust. affinis Ust. drakensbergiana Ust. syntherismae Ust. echinata Melanopsichium pennsylvanicum Ustilago esculenta sub-clade Ust. esculenta Ust. schmidtiae Ust. tragana 89/96 Spo. aegyptiacum /75 Spo. modestum Ustilago davisii Ust. filiformis sub-clade Ust. davisii Ust. schroeteriana Ust. trichophora Ust. nuda Ust. avenae Ust. hordei CLADE 6 Ust. phrygica Ust. tritici Ust. bullata Ustilago 84/97 Ust. pamirica Ust. turcomanica sensu stricto 0.96 Ust. bromivora sub-clade Ust. calamagrostidis Ust. striiformis Ust. sporoboli-indici 0.96 Ust. cynodontis Ust. sparsa Ust. xerochloae 80/87 Tri. lituana Tri. triodiae Tri. altilis Triodiomyces 0.99 Tri. inaltilis Anomalomyces panici Ant. mexicana Ant. provinciale Ant. elionuri Ant. loudetiae-pedicellatae Ant. bothriochloae Ant. apludae Ant. abscondita Ant. cymbopogonis-bombycini Ant. heteropogonicola Ant. everhartii Ant. apludae-aristatae Ant. sehimatis Ant. anthistiriae Ant. mutabile Ant. trispicatae Ant. hwangense 85/90 Ant. chrysopogonis Ant. themedae-arguentis Anthracocystis 1.0 Ant. polliniae Ant. caledonica Ant. setariae Ant. whiteochloae Ant. cenchri-elymoidis Ant. xerofasciculata Ant. penniseti Ant. anthracoideispora Ant. enteromorpha Ant. ovaria Ant. cenchri Ant. panici-leucophaei Ant. destruens Ant. formosana Ant. fallax Ant. tumefaciens 81/95 Stollia bursa Stollia 0.96 Stollia ewartii Ust. bouriquetii /84 Ust. maydis Mac. mackinlayi Mac. arundinellae-setosae Ust. vetiveriae CLADE 2 Spo. trachypogonis 100/99 Mac. simplex Systemic Mac. trichopterygis group 1.0 Mac. tristachyae Spo. scitamineum Spo. nealii Spo. andropogonis Spo. occidentale Spo. tenue Spo. holwayi Spo. lanigeri Spo. vermiculum Spo. queenslandicum Spo. trachypogonicola Spo. vanderystii Spo. paspali Spo. porosum Spo. rarum Spo. ryleyi Spo. wynaadense Spo. erythraeense Spo. doidgeae 90/92 Spo. pulverulentum Sporisorium Spo. cruentum sensu stricto 1.0 Spo. moniliferum Spo. sorghi Spo. foveolati Spo. nervosum Spo. mitchellii Spo. iseilematis-ciliati Spo. culmiperdum Spo. spinulosum Spo. dimeriae-ornithopodae Spo. lepturi Spo. monakai Spo. manilense Spo. arthraxonis Spo. lacrymae-jobi Spo. pseudechinolaenae Spo. ophiuri Spo. reilianum Spo. fastigiatum Fig. 1 Phylogram obtained from a phylogenetic analysis by McTaggart et al. (2012a). Maximum likelihood support values (> 70 %) from RAxML 1 000 boot- strap replicates and PhyML aRLT values shown above the nodes. Posterior probabilities (> 0.95) from Bayesian inference shown below the nodes. Resolved genera within the complex are listed on the right hand side. Unresolved clades are numbered according to McTaggart et al. (2012a). Type species of known genera are in bold. 118 Persoonia – Volume 29, 2012 the Ustilago-Sporisorium-Macalpinomyces complex. Taxa that Challinor, A.D.W. Geering, M.D.E. & R.G. Shivas, BRIP 51811; Western lack sterile cells occur in two monophyletic groups, namely Australia, Kununurra, Mulligan Lagoon Road, Sorghum timorense, 9 Apr. Anthracocystis and the subgroup, Ustilago s.str. (McTaggart 2008, A.R. McTaggart, V.L. Challinor, A.D.W. Geering,
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