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Epitypification of Tilletia Ehrhartae, a Smut Fungus with Potential For

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Epitypification of Tilletia Ehrhartae, a Smut Fungus with Potential For View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Crossref Eur J Plant Pathol (2015) 143:151–158 DOI 10.1007/s10658-015-0672-1 Epitypification of Tilletia ehrhartae,asmutfungus with potential for nature conservation, biosecurity and biocontrol Marcin Piątek & Matthias Lutz & Adriaana Jacobs & Francis Villablanca & Alan R. Wood Accepted: 1 May 2015 /Published online: 21 May 2015 # The Author(s) 2015. This article is published with open access at Springerlink.com Abstract Tilletia ehrhartae, a smut fungus infecting caused by Tilletia indica (which is absent in Australia), perennial veldtgrass Ehrharta calycina,isepitypified and therefore constituting a potential risk for Australian and characterized using the Consolidated Species Con- wheat export. The current global distribution of Tilletia cept, including morphology, ecology (host plant) and ehrhartae, possible colonization history, and potential rDNA sequences (ITS and LSU). Tilletia ehrhartae is for nature conservation, biosecurity and biocontrol are native and endemic to the Cape Floral Kingdom discussed. The sequences generated in this work could (located entirely in South Africa), but it has also been serve as DNA barcodes to facilitate rapid identification introduced to the alien artificial range of Ehrharta of this important species. calycina in Australia and California. This smut has already caused some biosecurity problems in Australia Keywords Australia . California . Cape Floral as its spores were found to contaminate harvested wheat Kingdom . South Africa . Epitype . Plant pathogens . seeds, leading to confusion with Karnal bunt of wheat DNA barcodes M. Piątek (*) Department of Mycology, W. Szafer Institute of Botany, Introduction Polish Academy of Sciences, Lubicz 46, PL-31-512 Kraków, Poland The plant pathogenic teliosporic smut fungi are predom- e-mail: [email protected] inantly distributed with host plants growing in natural M. Lutz ecosystems, especially different kinds of grasslands and Plant Evolutionary Ecology, Institute of Evolution and savannas where the highest species diversity occurs. Ecology, University of Tübingen, Auf der Morgenstelle 1, These species have been intensively studied with respect D-72076 Tübingen, Germany to their biodiversity and evolutionary significance A. Jacobs (Vánky 2012). A number of smut fungi are however National Collection of Fungi, ARC-Plant Protection Research also important to different aspects of human life and Institute, P. Bag X134QueenswoodPretoria 0121, South economy, being devastating pathogens of cultivated Africa crops or ornamental plants. The clear application of F. Villablanca correct names for plant pathogens having an impact on Biological Sciences Department, California Polytechnic State plant production and the economy is of primary interest University, San Luis Obispo, CA 93407, USA for phytopathologists (Crous 2005; Wingfield et al. 2012). However, morphology often does not provide A. R. Wood ARC-Plant Protection Research Institute, P. Bag X5017, sufficient resolution for an unambiguous identification Stellenbosch 7599, South Africa of species. In recent years, application of molecular 152 Eur J Plant Pathol (2015) 143:151–158 methods has revealed a considerable degree of cryptic specimens collected in Australia. The main constraint of species amongst plant pathogens (Shivas and Cai 2012). these sequences is that they were generated from spec- Thus, the combination of morphological, ecological and imens collected outside South Africa, i.e., from where molecular characters are valuable for correct species Tilletia ehrhartae was described as new to science and identification. This polyphasic approach has often been also from non-native range of the host plant, and there- used to differentiate fungal species including smuts fore none of the respective specimens was an appropri- (Lutz et al. 2008; Bauer et al. 2008;Piątek et al. 2012, ate candidate to be designated as the epitype. Further- 2013; Savchenko et al. 2013, 2014; Vasighzadeh et al. more, it cannot entirely be excluded that, under different 2014), and it was recently named the Consolidated environmental conditions, some local, morphologically Species Concept (Quaedvlieg et al. 2014). Strictly de- similar species jumped to Ehrharta calycina and that fined species, with reference sequences deposited in Australian (and Californian) specimens do not represent public repositories (such as NCBI’sGenBank),arees- Tilletia ehrhartae. The Californian material was not sential for progress in plant pathology. The ideal situa- sequenced so far. tion is when the reference sequences are from type This study aimed to epitypify Tilletia ehrhartae using specimens, which is usually realized when a new spe- recently collected material in South Africa, to provide a cies is described based on recently collected material, detailed morphological and molecular characterization but is difficult for species described during historical of the epitype specimen, and to compare the epitype ITS times and when the original type materials are inappro- and LSU sequences with those obtained from Australian priate for sequencing. That dilemma, however, may be and Californian specimens in order to confirm their abrogated by epitypification of known species, with conspecificity. Both the South African and Californian reference sequences obtained from a recently collected material are used to provide DNA barcodes, and to specimen that serves as the epitype. Ideally, such discuss the current distribution of Tilletia ehrhartae in epitypifications should include material collected on its natural and introduced range. the same host plant and in the same geographical area from where the species was described (Hyde and Zhang 2008). Materials and methods Karnal bunt of wheat caused by Tilletia indica is a disease with minor yield impact for wheat production Morphological examination but important economic losses could result from quar- antine regulations and export restrictions from infected Sori, spores, and sterile cells of the South African ma- regions (Carris et al. 2006). Three smut fungi with quite terial were studied using dried herbarium material. The similar morphology could impede correct identification herbarium specimens are deposited in KRAM F, KR-M, of Tilletia indica,namelyT. ehrhartae, T. horrida and and PREM. The material was examined by light T. walkeri (Carris et al. 2006). Notably, none of these microscopy (LM) and scanning electron microscopy important bunt pathogens have ITS sequences generated (SEM). The species description and measurements are from type specimens (the ITS sequences of Tilletia based on holotype and epitype specimens. For LM, walkeri in GenBank cannot be unequivocally linked to small pieces of sori were mounted in 80 % lactic acid, the type specimen). Tilletia ehrhartae, a species infect- heated to boiling point and cooled, and then examined ing perennial veldtgrass (Ehrharta calycina), is native under a Nikon Eclipse 80i light microscope. LM micro- and endemic to South Africa (Vánky 2012), but has graphs were taken with a Nikon DS-Fi1 camera. Fifty been introduced to Australia and California. This smut spores and at least 10 sterile cells were measured from has already caused some biosecurity problems in Aus- each of the holotype and epitype, at a magnification of tralia as its spores were found to contaminate harvested ×1000, using NIS-Elements BR 3.0 imaging software. wheat seeds, leading to confusion with Tilletia indica Except for the walls of spores, the remaining measure- (which is absent in Australia), and therefore constituting ments are adjusted to the nearest 0.5 μm. For SEM, a potential risk for Australian wheat export (Pascoe et al. spores and sterile cells were mounted on carbon tabs 2005; Vánky and Shivas 2008; Wright 2012). All pre- and fixed to an aluminium stub with double-sided trans- viously generated sequences deposited in GenBank (one parent tape. The stubs were sputter-coated with carbon ITS: AY770433, and one LSU: AY819013) are from using a Cressington sputter-coater and viewed under a Eur J Plant Pathol (2015) 143:151–158 153 Hitachi S-4700 scanning electron microscope, with a Parasitic on Ehrharta calycina, infection systemic, working distance of ca. 12 mm. SEM micrographs were infected culms dwarfed. Sori in all ovaries in the inflo- taken in the Laboratory of Field Emission Scanning rescences, causing a moderate hypertrophy of the ova- Electron Microscopy and Microanalysis at the Institute ries, ovoid to broadly fusiform, 2–7 mm long, 1.5–2mm of Geological Sciences of Jagiellonian University, wide, partly or rarely completely hidden by the glumes, Kraków (Poland). at first enclosed by a dirty green pericarp of host origin that in maturity ruptures irregularly exposing a blackish DNA extraction, PCR, and sequencing brown, granular powdery mass of spores mixed with sterile cells. Spores brown to chestnut-brown, rarely Genomic DNA for the South African epitype was iso- pale brown, regular in shape and size, globose or lated directly from the herbarium specimen. The Cali- subglobose, (17.5–)18.0–22.0 (−23.0)×17.5–21.0 μm fornia sample is from a specimen in the frozen tissue [av. ± SD, 19.9±1.3×19.3±1.1 μm, n=50] for the collection (FC – 712) at California Polytechnic State epitype, (17.0–)18.0–22.0 (−23.5)×17.5–21.0 μm[av. University, San Luis Obispo, CA. For methods of iso- ± SD, 19.5±1.4×19.3±1.1 μm, n=50] for the holotype; lation and crushing of fungal material, DNA extraction,
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