Advertisement

Mycological Progress

, 14:12 | Cite as

Phylogeny and taxonomy of grass rusts with aecia on Ranunculus and Ficaria

  • Markéta Hrabětová
  • Miroslav KolaříkEmail author
  • Jaroslava Marková
Original Article
  • 287 Downloads

Abstract

This study is focused on macrocyclic, heteroecious grass rusts (Pucciniales) with the aecial stage on Ranunculus spp. and Ficaria verna. Our aim is to study their phylogeny and host range, and evaluate differentiating morphological and molecular markers. Phylogenetic analyses of ITS-LSU rDNA recognised Puccinia perplexans, P. magnusiana, Uromyces dactylidis, U. poae, and three other lineages of uncertain taxonomic classification (U. cf. festucae and Uromyces species having aecia on Ranunculus). We showed that U. poae complex is a sister to U. dactylidis and belongs to the single clade with P. perplexans, phylogenetically distant from P. magnusiana. Of the PCR fingerprinting methods tested for species differentiation, only ISSR-PCR was found to be suitable. The analysis supported classical morphology-based taxonomic concepts of the species. Ficaria verna and Ranunculus acris were found to be the exclusive hosts of U. poae and P. perplexans, respectively. Ranunculus repens hosted U. dactylidis, P. magnusiana and an unidentified taxon from the U. poae clade. No specific differential features were found in aeciospore ornamentation, and only Uromyces cf. festucae can be distinguished based on specific aecial morphology. Based on aeciospore dimensions, only two species, U. dactylidis and P. perplexans, cannot be distinguished. All other species, including sister species U. poae and U. dactylidis, showed statistically significant differences. Because of overlapping morphological features of aecia and aeciospores, the molecular characters are necessary for their determination.

Keywords

Rust fungi Pucciniales Puccinia Uromyces Molecular identification ITS LSU rDNA 

Notes

Acknowledgments

The work was supported by European Regional Development Fund BIOCEV CZ.1.05/1.1.00/02.0109, Grant Agency of Charles University, project no. 188\2006\B-BIO\PřF, and by Institutional Support for Science and Research of the Ministry of Education, Youth and Sports of the Czech Republic, project VUKOZ-IP-00027073.

Supplementary material

11557_2015_1033_MOESM1_ESM.pdf (92 kb)
Supplementary figure 1 (PDF 91.8 kb)
11557_2015_1033_MOESM2_ESM.pdf (143 kb)
Supplementary figure 2 (PDF 142 kb)

References

  1. Abbasi M, Goodwin SB, Scholler M (2005) Taxonomy, phylogeny, and distribution of Puccinia graminis, the black stem rust: new insights based on rDNA sequence data. Mycoscience 46:241–247CrossRefGoogle Scholar
  2. Aime CM (2006) Toward resolving family-level relationships in rust fungi (Uredinales). Mycoscience 47:112–122CrossRefGoogle Scholar
  3. Aime CM, Matheny PB, Henk DA, Frieders EM, Nilsson RH, Piepenbring M, McLaughlin DJ, Szabo LJ, Begerow D, Sampaio JP, Bauer R, Weiß M, Oberwinkler F, Hibbett D (2006) An overview of the higher level classification of Pucciniomycotina based on combined analyses of nuclear large and small subunit rDNA sequences. Mycologia 98:896–905CrossRefPubMedGoogle Scholar
  4. Anikster Y, Szabo LJ, Eilam T, Manisterski J, Koike ST, Bushnell WR (2004) Morphology, life cycle biology, and DNA sequence analysis of rust fungi on garlic and chives from California. Phytopathology 94:569–577CrossRefPubMedGoogle Scholar
  5. Arthur JC (1934) Manual of the rusts in United States and Canada. Purdue Research Foundation, LafayetteGoogle Scholar
  6. Azbukina ZM (1974) Ržavčinnyje griby Dalnego Vostoka. MoscowGoogle Scholar
  7. Becerra V, Paredes M, Madariaga R, Bariana HS, Mellado M, Rojo C (2007) High genetic diversity in Chilean populations of wheat yellow rust (Puccinia striiformis f. sp. tritici West.) assessed by RAPD and AFLP. Aust J Agric Res 58:525–531CrossRefGoogle Scholar
  8. Blechtová A, Marková J, Urban Z (1994) Variability of Puccinia perplexans Plowr. in Czech and Slovak Republics. Novit Bot Univ Carol 7:9–21Google Scholar
  9. Bornet B, Branchard M (2001) Nonanchored inter simple sequence repeat (ISSR) markers: reproducible and specific tools for genome fingerprinting. Plant Mol Biol Report 19:209–215CrossRefGoogle Scholar
  10. Cai L, Giraud T, Zhang N, Begerow D, Cai G, Shivas RG (2011) The evolution of species concepts and species recognition criteria in plant pathogenic fungi. Fungal Divers 50:121–133CrossRefGoogle Scholar
  11. Chung WH, Tsukiboshi T, Ono Y, Kakishima M (2004) Morphological and phylogenetic analyses of Uromyces appendiculatus and U. vignae on legumes in Japan. Mycoscience 45:233–244CrossRefGoogle Scholar
  12. Cummins GB (1971) The rust fungi of cereals, grasses and bamboos. Springer, New York-Berlin-HeidelbergCrossRefGoogle Scholar
  13. Cummins GB, Hiratsuka Y (2003) Illustrated genera of rust fungi, 3rd edn. American Phytopathological Society, St. PaulGoogle Scholar
  14. Dixon LJ, Castlebury LA, Aime MC, Glynn NC, Comstock JC (2010) Phylogenetic relationships of sugarcane rust fungi. Mycol Prog 9:459–468CrossRefGoogle Scholar
  15. Edwards J, Ades PK, Parbery DG, Halloran GM, Taylor PNJ (1999) Morphological and molecular variation between Australasian isolates of Puccinia menthae. Mycol Res 103:1505–1514CrossRefGoogle Scholar
  16. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRefPubMedGoogle Scholar
  17. Gäumann E (1959) Die Rostpilze Mitteleuropas. BernGoogle Scholar
  18. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321CrossRefPubMedGoogle Scholar
  19. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  20. Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9Google Scholar
  21. Kerrigan J, Smith MT, Rogers JD, Poot GA, Douhan GW (2003) Ascobotryozyma cognata sp. nov., a new ascomycetous yeast associated with nematodes from wood-boring beetle galleries. Mycol Res 107:1110–1120CrossRefPubMedGoogle Scholar
  22. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi, 10th edn. CAB International, WallingfordGoogle Scholar
  23. Kolmer JA, Liu JQ (2000) Virulence and molecular polymorphism in international collections of the wheat leaf rust fungus Puccinia triticina. Phytopathology 90:427–436CrossRefPubMedGoogle Scholar
  24. Kropp BR, Hansen DR, Wolf PG, Flint KM, Thompson SV (1997) A study on the phylogeny of the Dyer’s woad rust fungus and other species of Puccinia from crucifers. Phytopathology 87:565–571CrossRefPubMedGoogle Scholar
  25. Lee SK, Kakishima M (1999) Aeciospore surface structures of Gymnosporangium and Rostelia (Uredinales). Mycoscience 40:109–120CrossRefGoogle Scholar
  26. Littlefield LJ, Marek SM, Tyrl RJ, Winkelman KS (2005) Morphological and molecular characterisation of Puccinia lagenophorae, now present in central North America. Ann Appl Biol 147:35–42CrossRefGoogle Scholar
  27. Liu M, Hambleton S (2010) Taxonomic study of stripe rust, Puccinia striiformis sensu lato, based on molecular and morphological evidence. Fungal Biol 114:881–899CrossRefPubMedGoogle Scholar
  28. Liu M, Hambleton S (2013) Laying the foundation for a taxonomic review of Puccinia coronata s.l. in a phylogenetic context. Mycol Prog 12:63–89CrossRefGoogle Scholar
  29. Liu M, Szabo LJ, Hambleton S, Anikster Y, Kolmer JA (2013) Molecular phylogenetic relationships of the brown leaf rust fungi on wheat, rye, and other grasses. Plant Dis 97:1408–1417CrossRefGoogle Scholar
  30. Maier W, Begerow D, Weiβ M, Oberwinkler F (2003) Phylogeny of the rust fungi: an approach using nuclear large subunit ribosomal DNA sequences. Can J Bot 81:12–23CrossRefGoogle Scholar
  31. Maier W, Wingfield BD, Mennicken M, Wingfield MJ (2007) Polyphyly and two emerging lineages in the rust genera Puccinia and Uromyces. Mycol Res 111:176–185CrossRefPubMedGoogle Scholar
  32. Majewski T (1977) Rdzawnikowe (Uredinales) 1. – In: Flora Polska. Grzyby (Mycota) IX. Warszawa, KrakówGoogle Scholar
  33. Majewski T (1979) Rdzawnikowe (Uredinales) 2. – In: Flora Polska XI. Warszawa, KrakówGoogle Scholar
  34. Marková J, Urban Z (1998) The rust fungi of grasses in Europe. 6. Puccinia persistens Plow., P. perplexans Plow., and P. elmi Westend. Acta Univ Carol Biol 41:329–402Google Scholar
  35. Menzies JG, Bakkeren G, Metheson F, Procunier JD, Woods S (2003) Use of inter-simple sequence repeats and amplified fragment length polymorphism to analyze genetic relationships among small grain-infecting species of Ustilago. Phytopathology 93:167–175CrossRefPubMedGoogle Scholar
  36. Morton CO, Mauchline TH, Kerry BR, Hirsch PR (2003) PCR based DNA fingerprinting indicates host-related genetic variation in the nematophagous fungus Pochonia chlamydosporia. Mycol Res 107:198–205CrossRefPubMedGoogle Scholar
  37. O’Donnell KL (1993) Fusarium and its near relatives. In: Reynolds D, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, pp 225–233Google Scholar
  38. Poelt J, Zwetko P (1997) Die Rostpilze Österreichs. 2., revidierte und erweiterte Auflage des Catalogus Florae Austriae, III Teil, Heft 1, Uredinales. Osterreichische Akademie der Wissenschaft, WienGoogle Scholar
  39. Sato T, Sato S (1982) Aeciospore surface structure of the Uredinales. Trans Mycol Soc Jpn 23:51–63Google Scholar
  40. Savile DBO (1973) Aeciospore types in Puccinia and Uromyces attacking Cyperaceae, Juncaceae and Poaceae. Rept Tottori Mycol Inst 10:225–241Google Scholar
  41. Săvulescu T (1953) Monografia uredinalelor din Republica Populara Romana. BucurestiGoogle Scholar
  42. Schoeller M (1996) Die Erysiphales, Pucciniales und Ustilaginales der Vorpommerschen Boddenlandschaft. Regensb Mykologische Schriftenr 6:1–325Google Scholar
  43. Spackman ME, Ogbonnaya FC, Brown JS (2010) Hypervariable RAPD, ISSR and SSR markers generate robust taxonomic groups among Puccinia striiformis formae speciales of importance to Australian agriculture. Australas Plant Pathol 39:226–233CrossRefGoogle Scholar
  44. Szabo LJ (2006) Deciphering species complexes Puccinia andropogonis and Puccinia coronata, examples of differing modes of speciation. Mycoscience 47:130–136CrossRefGoogle Scholar
  45. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedCentralPubMedGoogle Scholar
  46. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedCentralPubMedGoogle Scholar
  47. Urban Z (1966) Československé travní rzi, I.-III. Ms. - habilitation thesis, Dept. Botany Charles Univ. PragueGoogle Scholar
  48. Urban Z, Marková J (2009) Catalogue of rust fungi of the Czech and Slovak Republics. Charles University in Prague. Karolinum Press, PragueGoogle Scholar
  49. Van der Merwe M, Ericson L, Walker J, Thrall PH, Burdon JJ (2007) Evolutionary relationships among species of Puccinia and Uromyces (Pucciniaceae, Uredinales) inferred from partial protein coding gene phylogenies. Mycol Res 111:163–175CrossRefPubMedGoogle Scholar
  50. Van der Merwe M, Walker J, Ericson L, Burdon JJ (2008) Coevolution with higher taxonomic host groups within the Puccinia/Uromyces rust lineage obscured by host jumps. Mycol Res 112:1387–1408CrossRefPubMedGoogle Scholar
  51. Vassart G, Georges M, Monsieur R, Brocas H, Lequarre AS, Christophe DA (1987) Sequence in M13 phage detects hypervariable minisatellites in human and animal DNA. Science 235:683–684CrossRefPubMedGoogle Scholar
  52. Versalovic J, Koeuth T, Lupski R (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerpriting of bacterial genomes. Nucleic Acids Res 19:6823–6831CrossRefPubMedCentralPubMedGoogle Scholar
  53. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar
  54. Wingfield BD, Ericson L, Szaro T, Burdon JJ (2004) Phylogenetic patterns in the Uredinales. Australas Plant Pathol 33:327–335CrossRefGoogle Scholar
  55. Zambino PJ, Szabo LJ (1993) Phylogenetic relationships of selected cereal and grass rusts based on rDNA sequence analysis. Mycologia 85:401–414CrossRefGoogle Scholar
  56. Zhou S, Smith DR, Stanosz GR (2001) Differentiation of Botryosphaeria species and related anamorphic fungi using Inter Simple or Short Sequence Repeat (ISSR) fingerprinting. Mycol Res 105:919–926CrossRefGoogle Scholar
  57. Zietkiewicz E, Rafalski A, Labuda D (1994) Genome fingerprinting by simple sequence repeat (SSR)-anchored polymerase chain reaction amplification. Genomics 20:176–183CrossRefPubMedGoogle Scholar

Copyright information

© German Mycological Society and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Markéta Hrabětová
    • 1
    • 2
  • Miroslav Kolařík
    • 3
    Email author
  • Jaroslava Marková
    • 1
  1. 1.Department of Botany, Faculty of ScienceCharles University in PraguePrague 2Czech Republic
  2. 2.The Silva Tarouca Research Institute for Landscape and Ornamental GardeningPrůhoniceCzech Republic
  3. 3.Institute of Microbiology of the ASCRPrague 4Czech Republic

Personalised recommendations