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Rechecking of the Genus Scleroderma (Gasteromycetes) from Macedonia Using Barcoding Approach

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Rechecking of the Genus Scleroderma (Gasteromycetes) from Macedonia Using Barcoding Approach Turkish Journal of Botany Turk J Bot (2014) 38: 375-385 http://journals.tubitak.gov.tr/botany/ © TÜBİTAK Research Article doi:10.3906/bot-1301-36 Rechecking of the genus Scleroderma (Gasteromycetes) from Macedonia using barcoding approach 1, 1 2 3 Katerina RUSEVSKA *, Mitko KARADELEV , Cherdchai PHOSRI , Margarita DUEÑAS , 4 3 Roy WATLING , María Paz MARTÍN 1 Institute of Biology, Faculty of Natural Science and Mathematics, Ss. Cyril and Methodius University, Skopje, Macedonia 2 Division of Science, Faculty of Liberal Arts and Science, Nakhon Phanom University, 167 Naratchakouy Sub-District, Muang District, Nakhon Phanom, Thailand 3 Department of Mycology, Real Jardín Botánico, RJB-CSIC, Madrid, Spain 4 Caledonian Mycological Enterprises, Edinburgh, UK Received: 16.01.2013 Accepted: 04.12.2013 Published Online: 17.01.2014 Printed: 14.02.2014 Abstract: In order to verify some doubtful collections of Scleroderma Pers. species from Macedonia, 54 specimens were revised using morphological and molecular analyses. The 12 internal transcribed spacer of nuclear ribosomal DNA (ITS nrDNA) sequences obtained in this study were compared with previously published sequences included in public databases. According to the barcoding sequences, some Macedonian Scleroderma specimens were confirmed to belong to 4 species:S. areolatum Ehrenb., S. bovista Fr., S. meridionale Demoulin & Malençon, and S. verrucosum (Vaill.) Pers. Key words: Sclerodermatales, taxonomy, molecular identification, ITS nrDNA 1. Introduction species, Sesli and Denchev, 2008; Kaya, 2009; Demirel et al., Scleroderma Pers. species are ectomycorrhizal with a 2010; Alli, 2011; Doğan et al. 2012; Solak et al., 2013), while worldwide distribution. The genus Scleroderma was erected only 1 species (S. verrucosum) is known from the European by Persoon (1801) with 11 species. Guzmán (1970) cited part of Turkey (Stojchev et al., 1998). 21 species and the revision by Sims et al. (1995) included Being in the barcoding era, we aim to exploit this 25 species. Phosri et al. (2009), based on morphological approach and clarify the diversity of the Scleroderma species characters compared with internal transcribed spacer mentioned by Karadelev et al. (2008), rechecking the 54 of nuclear ribosomal DNA (ITS nrDNA) analyses of a specimens mentioned in this paper under morphological number of Scleroderma spp. from different geographical and molecular analysis of ITS nrDNA and following the origins, observed a good relationship among phylogenetic methodology described by Phosri et al. (2009). clades and basidiospore ornamentation. In Macedonia, 3 species have been cited frequently: Scleroderma areolatum 2. Materials and methods Ehrenb. (Karadelev et al., 2003b; Karadelev and Rusevska, 2.1. Taxon sampling and morphological studies 2004), S. citrinum Pers. (Karadelev, 2000; Karadelev et al., All collections are deposited in the Macedonian Collection 2002b, 2003a, 2004), and S. verrucosum (Vaill.) Pers. (Pilát of Fungi (MCF) at the Mycological Laboratory, Institute and Lindtner, 1939; Tortić, 1988; Karadelev et al., 2002a; of Biology, Faculty of Natural Sciences and Mathematics, Rusevska and Karadelev, 2004). Karadelev et al. (2008) Ss. Cyril and Methodius University (Table 1). The included a total of 8 species for Macedonia [including morphological revision of the specimens has been done Scleroderma bovista Fr., S. cepa Pers., S. meridionale according to Guzmán (1970), Jülich (1984), Breitenbach and Demoulin & Malençon, S. polyrhizum (J.F.Gmel.) Pers., and Kränzlin (1986), Pegler et al. (1995), Hansen and Knudsen S. septentrionale Jeppson]; this is a number quite similar to (1997), Calonge (1998), and Krieglsteiner (2000). The those of other Mediterranean areas, such as in Catalonia (6 most important morphological features of the basidiomata species, Martín, 1988) and the rest of the Iberian Peninsula defining the genus Scleroderma are spore morphology (7 species, Calonge, 1998), as well as in Asia Minor (7 (size, ornamentation), peridium (thickness, scaliness), and * Correspondence: [email protected] 375 RUSEVSKA et al. / Turk J Bot Table 1. Total Macedonian collection of Scleroderma included in this study. Complete data for each specimen including accession number in MCF, country name, precise locality, altitude (meters above sea level, m a.s.l.), habitats, date of collection, and results of molecular analyses are given. Asterisk indicates the new sequences obtained in this study. Date Taxon name Specimen ID Country Locality Habitat description Molecular results collected Scleroderma Jakupica Mountain: Orashche Quercetum Contamination: MCF 99/2293 Macedonia 15-Jul-1999 areolatum village, 800–900 m a.s.l. frainetto-cerris Candida spp. Osogovski Planini Mountain: Quercus and S. areolatum MCF 02/4202 Macedonia 3-Sep-2002 HF933231* Konopnica village, 1100 m a.s.l. Fagus forest Baba Mountain (Pelister): Not PCR S. areolatum MCF 04/4954 Macedonia Pasture 26-Oct-2004 Rotino village, 1000 m a.s.l. product Skopje (vicinity): Vodno, near Not PCR S. areolatum MCF 05/5300 Macedonia Deciduous forest 16-Oct-2005 Krushopek village, 800 m a.s.l. product Skopska Crna Gora Mountain: Ljubanci vill., Querco-Carpinetum Contamination: S. areolatum MCF 05/5455 Macedonia 9-Oct-2009 around St. Nikola monastery, 800 m a.s.l. orientalis Candida spp. Dobra Voda Mountain: Jagol village Quercetum Not PCR S. areolatum MCF 07/8552 Macedonia 1-Nov-2007 (above) frainetto-cerris product Kozhuf Mountain: Oreovica village Contamination: S. bovista MCF 98/4525 Macedonia 19-Jul-1998 (above), 850 m a.s.l. Candida spp. Baba Mountain (Pelister): Gjavato, S. bovista MCF 01/168 Macedonia Abieti-Fagetum 9-Oct-2001 HF933234* 1000 m a.s.l. Kozhuf Mountain: Smrdliva Voda, S. bovista MCF 05/788 Macedonia Fagus forest 23-Oct-2005 HF933235* 800 m a.s.l. Jablanica Mountain: Gorna Belica village (below), S. bovista MCF 05/5304 Macedonia Fagus forest 16-Oct-2005 HF933236* 1300 m a.s.l. Juglando-Platanetum Not PCR S. bovista MCF 06/330 Macedonia Bogdanci: Bolovan, 250 m a.s.l. 11-Nov-2006 orientalis product Edge of deciduous S. bovista MCF 09/11184 Serbia Leskovac town (vicinity): Vuchje 12-Sep-2009 HF933242* forest Baba Mountain (Pelister): Gjavato, Contamination: S. cepa MCF 01/5503 Macedonia Abieti-Fagetum 9-Oct-2011 1000 m a.s.l. Candida spp. Contamination: S. cepa MCF 05/800 Macedonia Galichica Mountain: Trpejca village 22-Oct-2005 Candida spp. Skopska Crna Gora Mountain: Ljubanci vill., At roadsides, grassy Contamination: S. cepa MCF 05/5161 Macedonia 11-Sep-2005 around St. Nikola monastery, 800 m a.s.l. place; silicate soil Candida spp. Skopje city: Gazi Baba, Botanical Garden Contamination: S. cepa MCF 06/6180 Macedonia (Faculty of Natural Science and Mathematics), Park 20-Oct-2006 Candida spp. 250 m a.s.l. Juniperus excelsa Contamination: S. cepa MCF 07/8290 Macedonia Valandovo: Chalakli village, 200 m a.s.l. 26-Oct-2007 forest Candida spp. Contamination: S. cepa MCF 07/8355 Macedonia Tetovo town (vicinity) Nov-2007 Candida spp. Dobra Voda Mountain: Gorica, west of Quercetum Contamination: S. cepa MCF 08/4530 Macedonia 8-Nov-2008 Popovjane village, 800–850 m a.s.l. frainetto-cerris Candida spp. Skopska Crna Gora Mountain: Kuchevishte Roof construction, old Not PCR S. cepa MCF 09/10600 Macedonia 12-May-2005 village, St. Arhangel monastery, 700 m a.s.l. guest house product 376 RUSEVSKA et al. / Turk J Bot Table 1. (Continued). Date Taxon name Specimen ID Country Locality Habitat description Molecular results collected Skopska Crna Gora Mountain: Ljubanci vill., Oak forest with 29-Aug- S. cf. septentrionale MCF 06/5993 Macedonia HF933240* above St. Nikola monastery, 900 m a.s.l. Castanea plantings 2006 S. citrinum MCF 89/4709 Macedonia Bogdanci (vicinity), 150 m a.s.l. Meadow 5-Jul-1989 HF933237* Pinetum sylvestris Contamination: S. citrinum MCF 02/5498 Macedonia Nidze Mountain: r. Prava Reka, 1400 m a.s.l. 16-Jul-2002 macedonicum Candida spp. Dobra Voda Mountain: between Tuin village Contamination: S. citrinum MCF 02/7981 Macedonia Oak forest 10-Oct-2002 and Popovjane village, 800–1100 m a.s.l. Candida spp. Contamination: S. citrinum MCF 06/6069 Macedonia Tetovo town, 450 m a.s.l. Yard 11-Oct-2006 Candida spp. Skopska Crna Gora Mountain: Ljubanci vill., Edge of Quercus and Contamination: S. citrinum MCF 06/6268 Macedonia 29-Oct-2006 above St. Nikola monastery, 800–900 m a.s.l. Carpinus forest Candida spp. Skopje city: Gazi Baba, above Faculty of Contamination: S. citrinum MCF 06/6291 Macedonia Oak-planted forest 18-Oct-2006 Natural Science and Mathematics, 250 m a.s.l. Candida spp. Meadow in Coccifero- HF933238* S. meridionale MCF 05/5505 Macedonia Bogdanci, 150 m a.s.l. 12-Dec-2005 Carpinetum orientalis HF933239* Coccifero-Carpinetum Contamination: S. meridionale MCF 08/10263 Macedonia Bogdanci: Strelishte, 150 m a.s.l. 14-Nov-2008 orientalis Candida spp. MCF 01/10050 (TR Contamination: S. meridionale Turkey Ağacaltı village: Ihlara Vadisi Near stream or river 16-Apr-2001 2010) Candida spp. Bogdanci: Kuchalat (vicinity), 200–300 Coccifero-Carpinetum Contamination: S. polyrhizum MCF 03/4749 Macedonia 2-Jan-2003 m a.s.l. orientalis Candida spp. Skopska Crna Gora Mountain: Ljubanci village, Contamination: S. polyrhizum MCF 05/1199 Macedonia Meadow 9-Oct-2005 Zgurovci, 800 m a.s.l. Candida spp. Skopska Crna Gora Mountain: Ljubanci Contamination: S. polyrhizum MCF 05/5507 Macedonia village, between St. Nikola monastery and Roadsides 2-Oct-2005 Candida spp. Zgurovci, 800 m a.s.l. Skopska Crna Gora Mountain: Ljubanci Forest edges (Querco- Contamination: S. polyrhizum MCF 05/5508 Macedonia 2-Oct-2005 village, Zgurovci, 800 m a.s.l. Carpinetum orientalis) Candida spp. Dobra Voda Mountain: Jagol village Meadow in Quercetum Contamination: S. polyrhizum MCF 07/8229 Macedonia 24-Oct-2007 (above), 850 m a.s.l. frainetto-cerris Candida spp. Contamination: S. polyrhizum MCF 07/8354 Macedonia Kichevo town: Rashtanski Pat Meadow 6-Nov-2007 Candida spp. Skopska Crna Gora Mountain: Ljubanci At roadsides, near S. verrucosum MCF 07/7984 Macedonia Jan-2007 HF933232* vill., near st.
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