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Soral Synapomorphies Are Significant for the Systematics of the <I Persoonia 29, 2012: 63–77 www.ingentaconnect.com/content/nhn/pimj RESEARCH ARTICLE http://dx.doi.org/10.3767/003158512X660562 Soral synapomorphies are significant for the systematics of the Ustilago-Sporisorium-Macalpinomyces complex (Ustilaginaceae) A.R. McTaggart1,2,3,5, R.G. Shivas1,2, A.D.W. Geering1,2,5, B. Callaghan2, K. Vánky4, T. Scharaschkin1,3 Key words Abstract The genera Ustilago, Sporisorium and Macalpinomyces are a polyphyletic complex of plant pathogenic fungi. The four main morphological characters used to define these genera have been considered homoplasious columella and not useful for resolving the complex. This study re-evaluates character homology and discusses the use of maximum likelihood these characters for defining monophyletic groups recovered from a reconstructed phylogeny using four nuclear morphology loci. Generic delimitation of smut fungi based on their hosts is also discussed as a means for identifying genera peridium within this group. Morphological characters and host specificity can be used to circumscribe genera within the smut fungi Ustilago-Sporisorium-Macalpinomyces complex. spore balls sterile cells Article info Received: 18 May 2012; Accepted: 3 October 2012; Published: 4 December 2012. systematics Ustilaginales INTRODUCTION Within the sorus, columellae form a central axis of fungal and host origin (Vánky 2002); sterile cells, either derived from non- Three genera of smut fungi (subphylum Ustilaginomycotina), sporogenous hyphae or a fungal peridium, are found with the Ustilago, Sporisorium and Macalpinomyces, contain about spores (Langdon & Fullerton 1975, 1978); spore balls appear 530 described species that all infect grasses (Vánky 2012). as either an ephemeral or permanent agglomeration of spores Several phylogenetic studies have demonstrated that Ustilago (Vánky 2002). A peridium is the outer layer of the sorus and can and Sporisorium together form a monophyletic group within be composed of host or fungal material (Vánky 2002). Soral the Ustilaginomycotina (Swann & Taylor 1995, Bauer et al. characters have had different interpretations by mycologists 1997, Begerow et al. 1997, 2004b, 2006, Stoll et al. 2003, (Stoll et al. 2005). For example, the columella in Ustilago po- 2005). Macalpinomyces has an ambiguous position in the Us- rosa was considered absent by Langdon (1962) but present by tilaginales as the type species, M. eriachnes, sits outside the Vánky & Shivas (2001). Similarly, Sporisorium consanguineum Ustilago-Sporisorium group (Begerow et al. 2006). Morphologi- was considered to have a columella by Langdon & Fullerton cal characters have proven inadequate for separation of species (1975), but not by Vánky & Shivas (2008). Subsequently, soral among the three genera. The three genera are polyphyletic morphology has been considered too variable to serve as a (Stoll et al. 2003, 2005), and collectively form an unresolved reliable character that can separate Ustilago, Sporisorium and complex. Morphological studies (Langdon & Fullerton 1975, Macalpinomyces (Piepenbring 2004, Stoll et al. 2005). Vánky 1991, Piepenbring et al. 1998) and molecular phylo- The current study discusses morphological characters in the genetic analyses (Stoll et al. 2003, 2005) have not identified Ustilago-Sporisorium-Macalpinomyces complex. A re-evalua- characters that define monophyletic groups amongst species tion of their homology is provided in light of the phylogenetic within this complex. results obtained. The merits of using host specificity and soral Smut fungi in the Ustilago-Sporisorium-Macalpinomyces com- synapomorphies are discussed as a basis for delimiting genera. plex either partially or completely destroy the inflorescence of grasses, forming a sorus that contains fungal spores. Four Materials AND METHODS characteristics of the sorus, namely columellae, sterile cells, spore balls and peridia, have been used traditionally to sepa- Taxon selection rate Ustilago, Sporisorium and Macalpinomyces (Vánky 2002). Taxa were selected to represent the main groups recovered in 1 Cooperative Research Centre for National Plant Biosecurity, GPO Box previous studies (Stoll et al. 2003, 2005), with increased sam- 5012, Bruce, ACT 2617, Australia; pling of under-represented groups, for example species of Ma- corresponding author e-mail: [email protected]. calpinomyces and smut fungi occurring on Aristida. In total, this 2 Department of Agriculture, Fisheries and Forestry, Ecosciences Precinct, study included 136 species (14 species of Macalpinomyces, 81 GPO Box 267, Brisbane, Queensland 4001, Australia. 3 EEBS, Faculty of Science and Technology, Queensland University of species of Sporisorium and 38 species of Ustilago), 35 of which Technology, 2 George Street, Brisbane, Queensland 4001, Australia. had not previously been evaluated in systematic studies (Table 4 Herbarium Ustilaginales Vánky (HUV), Gabriel-Biel-Str. 5, D-72076 Tübin- 1). Two distinctive members of the complex, Anomalomyces gen, Germany. panici and Melanopsichium pennsylvanicum, were also included. 5 Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, Ecosciences Precinct, GPO Box 267, Brisbane, Queensland Moesziomyces bullatus was included as an outgroup to the 4001, Australia. complex based on a relationship reported by Stoll et al. (2005). © 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. 64 Persoonia – Volume 29, 2012 – – – – – – – – – – – – – – – – – – – – – – – – – – – – HQ013063 – – – – – – HQ013057 HQ013058 HQ013059 HQ013055 HQ013065 – HQ013056 HQ013061 – HQ013064 HQ013066 HQ013068 HQ013060 GAPDH HQ013062 – – HQ013067 α – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – HQ013028 HQ013027 HQ013029 – HQ013034 HQ013035 HQ013026 HQ013031 HQ013032 HQ013033 – HQ013036 HQ013030 EF-1 – – – – 1 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 GenBank no. – AY740089 AY740090 – AY740109 – – AY740092 – AY740093 AY740153 AY740129 AY740095 AY740097 AY740098 AY740099 AF453943 AY740131 AF453939 AF133580 AY747077 – AY740132 – – – AY740102 – – AY740133 AY740134 DQ459347 HQ013131 FQ013130 – – – HQ013122 – – – HQ013127 – – – HQ013132 HQ013126 HQ013125 LSU – – – – 1 2 2 2 2 2 2 2 2 2 2 2 8 2 2 2 2 8 8 8 8 8 3 8 2 2 2 2 2 4 8 8 GU014817 AY740171 – HQ013088 AY740157 AY740158 AY344978 AY740036 AY344977 AY740049 AY333940 HQ013086 – HQ013094 AY344975 HQ013099 AY740042 HQ013087 AY740152 AY740164 HQ013090 – HQ013091 HQ013092 HQ013093 HQ013095 AY998100 – AY344979 AY740153 AY740045 AY740037 AY740159 AY344970 AY740039 HQ013089 AY740056 AY740154 ITS AY344973 AY344976 AY740151 AY740044 – AY344972 HQ013096 AY740047 AY740040 DQ459348 AY740046 HQ013096 HQ013098 AY344974 India Australia Unknown Australia Australia India Bolivia South Africa India Australia Nicaragua Australia Australia Country Australia Honduras Australia Australia Australia Zimbabwe Bolivia India Australia Iran Ecuador Australia India Australia Australia Australia Australia Mexico Australia Cuba Taiwan Germany South Africa Australia India Sri Lanka Romania South Africa Papua New Guinea Australia Nicaragua Australia Australia India Australia China Australia Australia United States sp. sp. sp. Eragrostiella bifaria Eulalia mackinlayi Eragrostis ferruginea Sporobolus australasicus Chrysopogon fallax Dimeria ornithopoda Elionurus muticus Themeda triandra Hackelochloa granularis Chrysopogon fallax Andropogon angustatus Arundinella nepalensis Arundinella nepalensis Host Cenchrus elymoides Andropogon gerardii Cymbopogon bombycinus Eriachne aristidea Sarga timorense Loudetia simplex Loudetiopsis chrysothrix Paspalum distichum Schizachyrium fragile Schismus arabicus Bothriochloa saccharoides Themeda triandra Apluda mutica Aristida jerichoensis Dichanthium sericeum Heteropogon contortus Aristida queenslandica Tripsacum Bothriochloa ewartiana Andropogon virginicus Panicum repens Setaria pumila dregeana Trichopteryx Sporobolus actinocladus Themeda quadrivalvis Chrysopogon fulvus Panicum miliaceum Loudetia flavida Pseudoraphis spinescens Aristida Cenchrus pilosus Aristida Capillipedium spicigerum Polygonum glabrum Panicum trachyrachis Arthraxon lanceolatus Aristida hygrometrica Aristida hygrometrica Sorghum halepense Ust. Exs. 960 52549 BRIP 13634 H.U.V. 51858 BRIP 51865 BRIP Ust. Exs. 472 2601 MP M 55602 Ust. Exs. 849 27687 BRIP 1976 MP BRIP 47958 BRIP 51868 BRIP Specimen no. BRIP 26491 BRIP 2060 MP 52511 BRIP M 54573 51818 BRIP M 56577 2630 MP Ust. Exs. 833 49648 BRIP Ust. Exs. 756 M 56588 49775 BRIP M 56590 26930 BRIP 51819 BRIP 28043 51854/BRIP BRIP 42670 BRIP 20560 H.U.V. 49669 BRIP 2270 MP Ust. Exs. 688 RB 2056 M 56578 49133 BRIP Ust. Exs. 844 Ust. Exs. 407 Ust. Exs. 472 M 56576 39176 BRIP 51871 BRIP 1974 MP 52755 BRIP M 56595 H.U.V. 17548 H.U.V. BRIP 46421 BRIP M 56592 51839 BRIP 27723
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