Mycopathologia

, Volume 166, Issue 1, pp 1–16 | Cite as

Domain II Hairpin Structure in ITS1 Sequences as an Aid in Differentiating Recently Evolved Animal and Plant Pathogenic Fungi

  • P. D. Bridge
  • T. Schlitt
  • P. F. Cannon
  • A. G. Buddie
  • M. Baker
  • A. M. Borman
Article

Abstract

The hypothesis that ITS structural features can be used to define fungal groups, where sequence analysis is unsatisfactory, was examined in plant and animal pathogenic fungi. Structural models of ITS1 regions were predicted for presumed closely related species in Colletotrichum and Trichophyton anamorphs of Arthroderma species. Structural alignment of models and comparison with ITS sequence analysis identified a variable region in a conserved hairpin formed from a common inverted repeat. Thirteen different hairpin structure models were obtained for Colletotrichum species and five different models were obtained for Trichophyton species. The different structure types could be matched to individual species and species complexes as defined by ITS sequence analysis.

Keywords

Colletotrichum Trichophyton Arthroderma ITS Structural models Sequence analysis 

References

  1. 1.
    Bridge PD, Spooner BM, Roberts PJ. The impact of molecular data in fungal systematics. Adv Bot Res 2005;42:33–67.CrossRefGoogle Scholar
  2. 2.
    Edel V, Steinberg C, Gautheron N, Alabouvette C. Evaluation of restriction analysis of polymerase chain reaction (PCR)-amplified ribosomal DNA for the identification of Fusarium species. Mycol Res 1996;101:179–87.CrossRefGoogle Scholar
  3. 3.
    Bridge PD, Waller JM, Davies D, Buddie AG. Variability of Colletotrichum kahawae in relation to other Colletotrichum species from tropical perennial crops and the development of diagnostic techniques. J Phytopathol 2008. doi:10.1111/j.1439-0434.2007.01354.x.Google Scholar
  4. 4.
    Tymon AM, Shah PA, Pell JK. PCR-based molecular discrimination of Pandora neoaphidis isolates from related entomopathogenic fungi and development of species-specific diagnostic primers. Mycol Res 2004;108:419–33.PubMedCrossRefGoogle Scholar
  5. 5.
    Xue B, Goodwin PH, Annis SL. Pathotype identification of Leptosphaeria maculans with PCR and oligonucleotide primers from ribosomal internal transcribed spacer sequences. Physiol Mol Plant Pathol 1992;41:179–88.CrossRefGoogle Scholar
  6. 6.
    Brown AE, Muthumeenakshi S, Sreenivasaprasad S, Mills PR, Swinburne TR. A PCR primer-specific to Cylindrocarpon heteronema for detection of the pathogen in apple wood. FEMS Microbiol Lett 1993;108:117–20.PubMedCrossRefGoogle Scholar
  7. 7.
    Sreenivasaprasad S, Mills PR, Meehan BM, Brown AE. Phylogeny and systematics of 18 Colletotrichum species based on ribosomal DNA spacer sequences. Genome 1996;39:499–512.PubMedCrossRefGoogle Scholar
  8. 8.
    Makimura K, Tamura Y, Mochizuki T, Hasegawa A, Tajiri Y, Hanazawa R, Uchida K, Saito H, Yamaguchi H. Phylogenetic classification and species identification of dermatophyte strains based on DNA sequences of nuclear ribosomal internal transcribed spacer 1 regions. J Clin Microbiol 1999;37:920–4.PubMedGoogle Scholar
  9. 9.
    van Neus RW, Rientjes JM, van der Sande CA, Zerp SF, Sluiter C, Venema J, Planta RJ, Raue HA. Separate structural elements within the internal transcribed spacer 1 of Saccharomyces cerevisiae precursor ribosomal RNA direct the formation of 17S and 26S rRNA. Nucl Acid Res 1994;22:912–9.CrossRefGoogle Scholar
  10. 10.
    Gottschling M, Plötner J. Secondary structure models of the nuclear internal transcribed spacer regions and 5.8S rRNA in Calciodinelloideae (Peridiniaceae) and other dinoflagellates. Nucl Acid Res 2004;32:307–15.CrossRefGoogle Scholar
  11. 11.
    Lalev AI, Nazar RN. Structural equivalence in the transcribed spacers of pre-rRNA transcripts in Schizosaccharomyces pombe. Nucl Acid Res 1999;27:3071–8.CrossRefGoogle Scholar
  12. 12.
    Campbell CS, Wright WA, Cox M, Vining TF, Major CS, Arsenault MP. Nuclear ribosomal DNA internal transcribed spacer 1 (ITS1) in Picea (Pinaceae): sequence divergence and structure. Mol Phylogen Evol 2005;35:165–85.CrossRefGoogle Scholar
  13. 13.
    Won H, Renner SS. The internal transcribed spacer on nuclear ribosomal DNA in the gymnosprem Gnetum. Mol Phylogenet Evol 2005;36:581–97.PubMedCrossRefGoogle Scholar
  14. 14.
    Gonzalez P, Labarère J. Sequence and secondary structure of the mitochondrial small-subunit rRNA V4, V6 and V9 domains reveal highly species-specific variations within the genus Agrocybe. Appl Environ Microbiol 1998;64:4149–60.PubMedGoogle Scholar
  15. 15.
    Tuckwell DS, Nicholson MJ, McSweeney SS, Theodorou MK, Brookman JL. The rapid assignment of ruminal fungi to presumptive genera using ITS1 and ITS2 RNA secondary structures to produce group-specific fingerprints. Microbiology 2005;151:1557–67.PubMedCrossRefGoogle Scholar
  16. 16.
    Landis FC, Gargas A. Using ITS2 secondary structure to create species-specific oligonucleotide probes for fungi. Mycologia 2007;99:681–92.PubMedCrossRefGoogle Scholar
  17. 17.
    Cannon PF, Bridge PD, Monte E. Linking the past, present, and future of Colletotrichum systematics. In: Prusky D, Freeman S, Dickman M, editors. Colletotrichum: host specificity, pathology, and host-pathogen interaction. St Paul Minnesota: American Phytopathological Society, 2000. p. 1–20.Google Scholar
  18. 18.
    Sreenivasaprasad S, Brown AE, Mills PR. DNA sequence variation and interrelationships among Colletotrichum species causing strawberry anthracnose. Physiol Mol Plant Pathol 1992;41:265–81.CrossRefGoogle Scholar
  19. 19.
    Sreenivasaprasad S, Mills PR, Brown AE. Nucleotide sequence of the rDNA spacer 1 enables identification of isolates of Colletotrichum as C. acutatum. Mycol Res 1994;98:186–8.CrossRefGoogle Scholar
  20. 20.
    Summerbell RC, Haugland RA, Li A, Gupta AK. rRNA gene internal transcribed spacer 1 and 2 sequences of asexual, anthropophilic dermatophytes related to Trichophyton rubrum. J Clin Microbiol 1999;37:4005–11.PubMedGoogle Scholar
  21. 21.
    Kirk PM, Cannon PF, David JC, Stalpers JA, editors. Ainsworth & Bisby’s dictionary of the fungi. 9th ed. Wallingford: CAB International; 2001.Google Scholar
  22. 22.
    Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acid Res 1994;22:4673–80.CrossRefGoogle Scholar
  23. 23.
    Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucl Acid Res 2003;31:3406–15.CrossRefGoogle Scholar
  24. 24.
    Clamp M, Cuff J, Searle SM, Barton GJ. The Jalview Java Alignment Editor. Bioinformatics 2004;20:426–7.PubMedCrossRefGoogle Scholar
  25. 25.
    Höchsmann, M. The tree alignment model: Algorithms, implementations and applications for the analysis of RNA secondary structures. PhD Thesis Bielefeld University, 2005. (available as .pdf file at http://bibiserv.techfak.uni-bielefeld.de/rnaforester/diss_hoechsmann.pdf).
  26. 26.
    Höchsmann M, Voss B, Giegerich R. Pure multiple RNA secondary structure alignments: a progressive profile approach. IEEE/ACM Trans Comput Biol Bioinform 2004;1:53–62.PubMedCrossRefGoogle Scholar
  27. 27.
    Felsenstein J. PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, 2005.Google Scholar
  28. 28.
    Page RDM. TREEVIEW: An application to display phylogenetic trees on personal computers. Computer Appl Biosci 1996;12:357–8.Google Scholar
  29. 29.
    Freeman S, Minz D, Jurkevitch E, Maymon M, Shabi E. Molecular analyses of Colletotrichum species from almond and other fruits. Phytopathology 2000;90:608–14.CrossRefPubMedGoogle Scholar
  30. 30.
    Afanador-Kafuri L, Minz D, Maymon M, Freeman S. Characterization of Colletotrichum isolates from Tamarillo, Passiflora, and Mango in Colombia and identification of a unique species from the genus. Phytopathology 2003;93:579–87.CrossRefPubMedGoogle Scholar
  31. 31.
    Makimura K, Mochizuki T, Hasegawa A, Uchida K, Saito H, Yamaguchi H. Phylogenetic classification of Trichophyton mentagrophytes complex strains based on DNA spacers of nuclear ribosomal internal transcribed spacer 1 regions. J Clin Microbiol 1998;36:2629–33.PubMedGoogle Scholar
  32. 32.
    Gräser Y, de Hoog GS, Kuijpers AFA. Recent advances in the molecular taxonomy of dermatophytes In: Kushwaha RKS, Guarro J, editors. Biology of Dermatophytes and other Keratinophilic fungi. Bilbao Spain: Revista Iberoamericana de Micologia (suppl.), 2000, p. 17–21.Google Scholar
  33. 33.
    Mathews DH, Sabina J, Zuker M, Turner DH. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. JMol Biol 1999;288:911–40.CrossRefGoogle Scholar
  34. 34.
    Goertzen LR, Cannone JJ, Gutell RR, Jansen RK. ITS secondary structure derived from comparative analysis: implications for sequence alignment, phylogeny of the Asteraceae. Mol Phylogenet Evol 2003;29:216–34.PubMedCrossRefGoogle Scholar
  35. 35.
    Gardner PP, Giegerich R. A comprehensive comparison of comparative RNA structure prediction approaches. BMC Bioinformatics 2004;5:140.PubMedCrossRefGoogle Scholar
  36. 36.
    Mayol M, Rossello JA. Why ribosomal DNA spacers (ITS) tell different stories in Quercus. Mol Phylogenet, Evol 2001;19:167–76.CrossRefGoogle Scholar
  37. 37.
    Liu JS, Schardl CL. A conserved sequence in internal transcribed spacer 1 of plant nuclear rRNA genes. Plant Mol Biol 1994;26:775–8.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • P. D. Bridge
    • 1
  • T. Schlitt
    • 1
  • P. F. Cannon
    • 2
  • A. G. Buddie
    • 2
  • M. Baker
    • 3
  • A. M. Borman
    • 4
  1. 1.Biological Sciences DivisionBritish Antarctic SurveyCambridgeUK
  2. 2.CABI Europe – UKEghamUK
  3. 3.East Kent Microbiology ServiceThe William Harvey HospitalAshfordUK
  4. 4.Mycology Reference Laboratory, Health Protection Agency South-West Regional LaboratoryBristolUK

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