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Discovery of Thecaphora schwarzmaniana on Rheum ribes in Iran and Turkey: implications for the diversity and phylogeny of leaf smuts on rhubarbs

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Abstract

A leaf smut discovered on wild rhubarb Rheum ribes in Iran and Turkey is evaluated to identify the species. Based on morphological analyses using light and scanning electron microscopy and molecular phylogenetic analyses using ITS and LSU ribosomal DNA sequences, it is shown that the smut fungus belongs to Thecaphora schwarzmaniana, a rare species previously known on Rheum cordatum, R. lobatum, R. macrocarpum, and R. turkestanicum in some central Asian countries. This is the first documented case of Thecaphora schwarzmaniana on Rheum ribes and significantly expands the range of the species on the Asian continent. The ITS and LSU sequences of the Iranian and Turkish material differed from sequences of Thecaphora schwarzmaniana from Rheum palmatum from China. The re-study of the morphology of the respective specimen revealed morphological differences allowing the conclusion that Thecaphora on Rheum palmatum belongs to a distinct species. The new species is not described here due to the paucity of available material. Molecular phylogenetic analyses, based on ITS and LSU sequences, recovered Thecaphora on Rheum spp. in a clade including species on host plants from diverse unrelated families, indicating that multiple inter-family host jumps took place in the course of evolution of Thecaphora species. Vast similarity of ITS and LSU sequences of Thecaphora spp. on Rheum spp. point to their close relation suggesting that co-evolution could shape the diversification of Thecaphora species on Polygonaceae following an initial host jump from another host plant family.

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Notes

  1. (Oberwinkler 2012) introduced the term “false smuts” to species having a similar life strategy like smut fungi but classified in the pucciniomycotinous order Microbotryales. It should be noted that the term “false smuts” is also commonly used for species of the ascomycetous genus Ustilaginoidea Bref. that have similar appearance like smut fungi.

References

  • Andrade O, Muñoz G, Galdames R, Durán P, Honorato R (2004) Characterization, in vitro culture, and molecular analysis of Thecaphora solani, the causal agent of potato smut. Phytopathology 94:875–882

    Article  CAS  PubMed  Google Scholar 

  • Bai HC, Wang SR (1991) Taxonomic study on the genus Thecaphora in China. J Gansu Agric Univ 26(3):283–287 (in Chinese)

    Google Scholar 

  • Bai HC, Wang SR (1993) Discovery of Thecaphora schwarzmaniana in China. Acta Mycol Sin 12:251–252 (in Chinese)

    Google Scholar 

  • Bauer R, Lutz M, Piątek M, Vánky K, Oberwinkler F (2007) Flamingomyces and Parvulago, new genera of marine smut fungi (Ustilaginomycotina). Mycol Res 111:1199–1206

    Article  CAS  PubMed  Google Scholar 

  • Bauer R, Lutz M, Begerow D, Piątek M, Vánky K, Bacigálová K, Oberwinkler F (2008) Anther smut fungi on monocots. Mycol Res 112:1297–1306

    Article  PubMed  Google Scholar 

  • Begerow D, Bauer R, Oberwinkler F (1997) Phylogenetic studies on nuclear LSU rDNA sequences of smut fungi and related taxa. Can J Bot 75:2045–2056

    Article  CAS  Google Scholar 

  • Begerow D, Bauer R, Boekhout T (2000) Phylogenetic placements of ustilaginomycetous anamorphs as deduced from nuclear LSU rDNA sequences. Mycol Res 104:53–60

    Article  CAS  Google Scholar 

  • Begerow D, Stoll M, Bauer R (2006) A phylogenetic hypothesis of Ustilaginomycotina based on multiple gene analyses and morphological data. Mycologia 98:906–916

    Article  PubMed  Google Scholar 

  • Carris LM, Castlebury LA, Huang GM, Alderman SC, Luo JF, Bao XD (2007) Tilletia vankyi, a new species of reticulate-spored bunt fungus with non-conjugating basidiospores infecting species of Festuca and Lolium. Mycol Res 111:1386–1398

    Article  CAS  PubMed  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Conforto C, Cazón I, Fernández FD, Marinelli A, Oddino C, Rago AM (2013) Molecular sequence data of Thecaphora frezii affecting peanut crops in Argentina. Eur J Plant Pathol 137:663–666

    Article  Google Scholar 

  • Curran HR, Roets F, Dreyer LL (2009) Anther-smut fungal infection of South African Oxalis species: spatial distribution patterns and impacts on host fecundity. South Afr J Bot 75:807–815

    Article  Google Scholar 

  • Davis PH (ed) (1967) Flora of Turkey and the Easy Aegean Islands, 2nd edn. University Press, Edinburgh

    Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Gatesy J, DeSalle R, Wheeler W (1993) Alignment-ambiguous nucleotide sites and the exclusion of systematic data. Mol Phylogenet Evol 2:152–157

    Article  CAS  PubMed  Google Scholar 

  • Giribet G, Wheeler WC (1999) On gaps. Mol Phylogenet Evol 13:132–143

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Rannala B (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst Biol 53:904–913

    Article  PubMed  Google Scholar 

  • Huelsenbeck JP, Larget B, Miller RE, Ronquist F (2002) Potential applications and pitfalls of Bayesian inference of phylogeny. Syst Biol 51:673–688

    Article  PubMed  Google Scholar 

  • Jafari A, Taheri G, Baradaran B, Bahrami AR (2012) Rheum khorasanicum (Polygonaceae), a new species from Iran. Ann Bot Fenn 49:255–258

    Article  Google Scholar 

  • Karatygin IV, Azbukina ZM (1989) Opredeliteľ gribov SSSR. Porjadok Golovnevye. Vyp. 1. Semejstvo Ustilagovye (Definitorium fungorum URSS. Ordo Ustilaginales. Fasc. 1. Familia Ustilaginaceae). Nauka, Leningrad

    Google Scholar 

  • Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program (outlines version 6). Brief Bioinform 9:286–298

    Article  CAS  PubMed  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kemler M, Göker M, Oberwinkler F, Begerow D (2006) Implications of molecular characters for phylogeny of the Microbotryaceae (Basidiomycota: Urediniomycetes). BMC Evol Biol 6:35

    Article  PubMed Central  PubMed  Google Scholar 

  • Kemler M, Lutz M, Göker M, Oberwinkler F, Begerow D (2009) Hidden diversity in the non-caryophyllaceous plant-parasitic members of Microbotryum (Pucciniomycotina: Microbotryales). Syst Biodivers 7:297–306

    Article  Google Scholar 

  • Korbonskaia IAI (1990) Griby Tadzhikistana. Donish, Dushanbe

    Google Scholar 

  • Krishnaiah D, Sarbatly R, Nithyanandam R (2011) A review of the antioxidant potential of medicinal plant species. Food Bioprod Process 89:217–233

    Article  CAS  Google Scholar 

  • Lozina-Lozinskaya A (1936) Polygonaceae. In: Komarov VL (ed) Flora of USSR 5. Izdateľstvo Akademii Nauk SSSR, Moskva, pp 442–704

    Google Scholar 

  • Lutz M, Bauer R, Begerow D, Oberwinkler F, Triebel D (2004) Tuberculina: rust relatives attack rusts. Mycologia 96:614–626

    Article  PubMed  Google Scholar 

  • Lutz M, Göker M, Piątek M, Kemler M, Begerow D, Oberwinkler F (2005) Anther smuts of Caryophyllaceae: molecular characters indicate host-dependent species delimitation. Mycol Prog 4:225–238

    Article  Google Scholar 

  • Lutz M, Piątek M, Kemler M, Chlebicki A, Oberwinkler F (2008) Anther smuts of Caryophyllaceae: molecular analyses reveal further new species. Mycol Res 112:1280–1296

    Article  PubMed  Google Scholar 

  • Lutz M, Vánky K, Bauer R (2012) Melanoxa, a new genus in the Urocystidales (Ustilaginomycotina). Mycol Prog 11:149–158

    Article  Google Scholar 

  • Matheny PB, Gossmann JA, Zalar P, Arun Kumar TK, Hibbett DS (2006) Resolving the phylogenetic position of the Wallemiomycetes: an enigmatic major lineage of Basidiomycota. Can J Bot 84:1794–1805

    Article  CAS  Google Scholar 

  • McTaggart AR, Shivas RG, Geering ADW, Callaghan B, Vánky K, Scharaschkin T (2012) Soral synapomorphies are significant for the systematics of the Ustilago-Sporisorium-Macalpinomyces complex (Ustilaginaceae). Persoonia 29:63–77

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • O’Donnell KL (1992) Ribosomal DNA internal transcribed spacers are highly divergent in the phytopathogenic ascomycete Fusarium sambucinum (Gibberella pulicaris). Curr Genet 22:213–220

    Article  PubMed  Google Scholar 

  • O’Donnell KL (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, pp 225–233

    Google Scholar 

  • Oberwinkler F (2012) Evolutionary trends in Basidiomycota. Stapfia 96:45–104

    Google Scholar 

  • Piątek M, Lutz M, Smith PA, Chater AO (2011) A new species of Antherospora supports the systematic placement of its host plant. IMA Fungus 2:135–142

    Article  Google Scholar 

  • Piątek M, Lutz M, Ronikier A, Kemler M, Świderska-Burek U (2012a) Microbotryum heliospermae, a new anther smut fungus parasitic on Heliosperma pusillum in the mountains of the European Alpine System. Fungal Biol 116:185–195

    Article  PubMed  Google Scholar 

  • Piątek M, Piątek J, Mossebo DC (2012b) Recently discovered collections extend the geographical range of the smut fungus Sphacelotheca polygoni-serrulati to Cameroon and Zambia. Pol Bot J 57:285–293

    Google Scholar 

  • Piątek M, Lutz M, Chater AO (2013a) Cryptic diversity in the Antherospora vaillantii complex on Muscari species. IMA Fungus 4:5–19

    Article  PubMed Central  PubMed  Google Scholar 

  • Piątek M, Lutz M, Kemler M (2013b) Microbotryum silenes-saxifragae sp. nov. sporulating in the anthers of Silene saxifraga in southern European mountains. IMA Fungus 4:29–40

    Article  PubMed Central  PubMed  Google Scholar 

  • Piepenbring M (2000) New species of smut fungi from the neotropics. Mycol Res 105:757–767

    Article  Google Scholar 

  • Piepenbring M (2002) Morphology of Liroa emodensis (Microbotryales, Basidiomycota) on Polygonum chinense. Fungal Sci 17:55–64

    Google Scholar 

  • Prillinger H, Wuczkowski M, Lopandic K, Bauer R, Molnár O, Sterflinger K (2009) Schizonella caricis-atratae (Ustilaginomycetes): a new cryptic species on Carex atrata from Austria. Mycol Prog 8:157–164

    Article  Google Scholar 

  • Roets F, Dreyer LL, Wingfield MJ, Begerow D (2008) Thecaphora capensis sp. nov., an unusual new anther smut on Oxalis in South Africa. Persoonia 21:147–152

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Roets F, Curran HR, Dreyer LL (2012) Morphological and reproductive consequences of an anther smut fungus on Oxalis. Sydowia 64:267–280

    Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed Central  PubMed  Google Scholar 

  • Roux C, Almaraz T, Durrieu G (1998) Phylogénie de champignons responsables des charbons des végétaux à partir de ľanalyse des séquences ITS. C R Acad Sci III Sci Vie 321:603–609

    Article  CAS  Google Scholar 

  • Savchenko KG, Lutz M, Piątek M, Heluta VP, Nevo E (2013) Anthracoidea caricis-meadii is a new North American smut fungus on Carex sect Paniceae. Mycologia 105:181–193

    Article  PubMed  Google Scholar 

  • Schwarzman SR (1960) Golovnevye griby (Smut fungi). In: Flora sporovych rastenij Kazachstana. Tom 2. Izdateľstvo Akademii Nauk Kazachskoi SSR, Alma Ata

  • Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337

    Article  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771

    Article  PubMed  Google Scholar 

  • Sun YS, Wang AL, Wan DS, Wang Q, Liu JQ (2012) Rapid radiation of Rheum (Polygonaceae) and parallel evolution of morphological traits. Mol Phylogenet Evol 63:150–158

    Article  PubMed  Google Scholar 

  • Uljanishchev VI (1968) Opredeliteľ golovnevyh gribov SSSR (Key to the smut fungi of the USSR). Izdateľstvo Nauka, Leningrad

    Google Scholar 

  • Vánky K (1994) European smut fungi. G. Fischer Verlag, Stuttgart-Jena, New York

    Google Scholar 

  • Vánky K (1998) The genus Microbotryum (smut fungi). Mycotaxon 67:33–60

    Google Scholar 

  • Vánky K (2000) New taxa of Ustilaginomycetes. Mycotaxon 74(2):343–356

    Google Scholar 

  • Vánky K (2002) Illustrated genera of smut fungi, 2nd edn. APS Press, St. Paul, Minnesota

    Google Scholar 

  • Vánky K (2008) Taxonomic studies on Ustilaginomycetes – 28. Mycotaxon 106:133–178

    Google Scholar 

  • Vánky K (2012) Smut fungi of the world. APS Press, St. Paul, Minnesota

    Google Scholar 

  • Vánky K (2013) Illustrated genera of smut fungi, 3rd edn. APS Press, St. Paul, Minnesota

    Google Scholar 

  • Vánky K, Berbee M (1988) Are there Thecaphora species (Ustilaginales) on Gramineae? Mycotaxon 33:281–282

    Google Scholar 

  • Vánky K, Lutz M (2007) Revision of some Thecaphora species (Ustilaginomycotina) on Caryophyllaceae. Mycol Res 111:1207–1219

    Article  PubMed  Google Scholar 

  • Vánky K, Oberwinkler F (1994) Ustilaginales on Polygonaceae – a taxonomic revision. Nova Hedwig Beih 107:1–96

    Google Scholar 

  • Vánky K, Lutz M, Bauer R (2008a) About the genus Thecaphora (Glomosporiaceae) and its new synonyms. Mycol Prog 7:31–39

    Article  Google Scholar 

  • Vánky K, Lutz M, Bauer R (2008b) Floromyces, a new genus of Ustilaginomycotina. Mycotaxon 104:171–184

    Google Scholar 

  • Wang AL, Yang MH, Liu JQ (2005) Molecular phylogeny, recent radiation, and evolution of gross morphology of the rhubarb genus Rheum (Polygonaceae) inferred from chloroplast DNA trnL-F sequences. Ann Bot 96:489–498

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Chen X, Li Y (2009) Survey and pathogen identification of rhubarb diseases in Gansu province. Zhongguo Zhong Yao Za Zhi 34(8):953–956 (in Chinese)

    PubMed  Google Scholar 

  • Weiss M, Bauer R, Begerow D (2004) Spotlights on heterobasidiomycetes. In: Agerer R, Blanz P, Piepenbring M (eds) Frontiers in Basidiomycote Mycology. IHW-Verlag, Eching, pp 7–48

    Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

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Acknowledgements

We thank Mahmood Bahador (Hamedan, Iran) and Kálmán Vánky (Tübingen, Germany) for providing specimens, Michael Weiß, Sigisfredo Garnica and Robert Bauer (Tübingen, Germany) for providing facilities for molecular analyses, Jolanta Piątek (Kraków, Poland) for preparing the world map and the drawing of germinating spores, and Anna Łatkiewicz (Kraków, Poland) for her help with the SEM pictures. The work of Marcin Piątek was partly financed through the statutory fund of the W. Szafer Institute of Botany of the Polish Academy of Sciences, Kraków.

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Vasighzadeh, A., Zafari, D., Selçuk, F. et al. Discovery of Thecaphora schwarzmaniana on Rheum ribes in Iran and Turkey: implications for the diversity and phylogeny of leaf smuts on rhubarbs. Mycol Progress 13, 881–892 (2014). https://doi.org/10.1007/s11557-014-0972-4

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