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Emergence of a new disease as a result of interspecific virulence gene transfer

Abstract

New diseases of humans, animals and plants emerge regularly. Enhanced virulence on a new host can be facilitated by the acquisition of novel virulence factors. Interspecific gene transfer is known to be a source of such virulence factors in bacterial pathogens (often manifested as pathogenicity islands in the recipient organism1) and it has been speculated that interspecific transfer of virulence factors may occur in fungal pathogens2. Until now, no direct support has been available for this hypothesis. Here we present evidence that a gene encoding a critical virulence factor was transferred from one species of fungal pathogen to another. This gene transfer probably occurred just before 1941, creating a pathogen population with significantly enhanced virulence and leading to the emergence of a new damaging disease of wheat.

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Figure 1
Figure 2: The S. nodorum ToxA locus in S. nodorum.
Figure 3: The ToxA loci in S. nodorum and P. tritici-repentis.
Figure 4: Functional and genetic analysis of interaction between S. nodorum ToxA and the wheat gene Tsn1 (a) Bioassay of culture filtrates from ToxA dysfunctional mutants and controls on wheat line BG261 (ToxA-sensitive).

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References

  1. Hacker, J., Blum-Oehler, G., Muehldorfer, I. & Tschaepe, H. Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol. Microbiol. 23, 1089–1097 (1997).

    Article  CAS  Google Scholar 

  2. Rosewich, U.L. & Kistler, H.C. Role of horizontal gene transfer in the evolution of fungi. Annu. Rev. Phytopathol. 38, 325–363 (2000).

    Article  CAS  Google Scholar 

  3. Meehan, F. & Murphy, H.C. Differential phytotoxicity of metabolic by-products of Helminthosporium victoriae. Science 106, 270–271 (1947).

    Article  CAS  Google Scholar 

  4. Tatum, L.A. The Southern corn leaf blight epidemic. Science 171, 1113–1116 (1971).

    Article  CAS  Google Scholar 

  5. Walton, J.D. Horizontal gene transfer and the evolution of secondary metabolite gene clusters in fungi: An hypothesis. Fungal Genet. Biol. 30, 167–171 (2000).

    Article  CAS  Google Scholar 

  6. Faris, J., Anderson, J., Francl, L. & Jordahl, J. Chromosomal location of a gene conditioning insensitivity in wheat to necrosis-inducing culture filtrate from Pyrenophora tritici-repentis. Phytopathology 86, 459–463 (1996).

    Article  CAS  Google Scholar 

  7. Tomas, A., Feng, G.H., Reeck, G.R., Bockus, W.W. & Leach, J.E. Purification of a cultivar-specific toxin from Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Mol. Plant Microbe Interact. 3, 221–224 (1990).

    Article  CAS  Google Scholar 

  8. Ciuffetti, L.M., Tuori, R.P. & Gaventa, J.M. A single gene encodes a selective toxin causal to the development of tan spot of wheat. Plant Cell 9, 135–144 (1997).

    Article  CAS  Google Scholar 

  9. Solomon, P., Lowe, R., Tan, K.C., Waters, O. & Oliver, R. Stagonospora nodorum; cause of stagonospora nodorum blotch of wheat. Mol. Plant Pathol. 7, 147–156 (2006).

    Article  Google Scholar 

  10. Liu, Z.H. et al. Genetic and physical mapping of a gene conditioning sensitivity in wheat to a partially purified host-selective toxin produced by Stagonospora nodorum. Phytopathology 94, 1056–1060 (2004).

    Article  CAS  Google Scholar 

  11. Liu, Z.H. et al. Quantitative trait loci analysis and mapping of seedling resistance to Stagonospora nodorum leaf blotch in wheat. Phytopathology 94, 1061–1067 (2004).

    Article  CAS  Google Scholar 

  12. Ali, S. & Francl, L.J. Race structure of Pyrenophora tritici-repentis isolates obtained from wheat in South America. Plant Prot. Sci. 38, 302–304 (2002).

    Google Scholar 

  13. Lamari, L., Gilbert, J. & Tekauz, A. Race differentiation in Pyrenophora tritici-repentis and survey of physiological variation in western Canada. Can. J. Plant Pathol. 20, 396–400 (1998).

    Article  Google Scholar 

  14. Nei, M. Molecular Evolutionary Genetics (Columbia Univ. Press, New York, 1987).

    Google Scholar 

  15. Kempken, F. & Kück, U. Transposons in filamentous fungi - facts and perspectives. Bioessays 20, 652–659 (1998).

    Article  CAS  Google Scholar 

  16. Lichter, A., Gaventa, J.M. & Ciuffetti, L.M. Chromosome-based molecular characterization of pathogenic and non-pathogenic wheat isolates of Pyrenophora tritici-repentis. Fungal Genet. Biol. 37, 180–189 (2002).

    Article  CAS  Google Scholar 

  17. Hosford, R.M. Tan spot - developing knowledge 1902–1981, virulent races and wheat differentials, methodology, rating systems, other leaf diseases, literature. in Tan Spot of Wheat and Related Diseases Workshop (ed. Hosford, R.M.) 1–24 (North Dakota Agricultural Experiment Station, Fargo, North Dakota, 1982).

    Google Scholar 

  18. Barrus, M.F. A disease of wheat newly recorded for this country - yellow spot disease of wheat in New York State. Plant Dis. Reporter 26, 246 (1942).

    Google Scholar 

  19. Johnson, A.J. Helminthosporium tritici-vulgaris on wheat in Maryland. Plant Dis. Reporter 26, 246–247 (1942).

    Google Scholar 

  20. Valder, P.G. & Shaw, D.E. Yellow spot disease of wheat in Australia. Proc. Linn. Soc. N. S. W. 77, 323–330 (1953).

    Google Scholar 

  21. Duff, A.D. A new disease of wheat in Kenya caused by a species of Pyrenophora. East Afr. Agric. J. 19, 225–228 (1954).

    Google Scholar 

  22. Bearchell, S.J., Fraaije, B.A., Shaw, M.W. & Fitt, B.D. Wheat archive links long-term fungal pathogen population dynamics to air pollution. Proc. Natl. Acad. Sci. USA 102, 5438–5442 (2005).

    Article  CAS  Google Scholar 

  23. Schurch, S., Linde, C.C., Knogge, W., Jackson, L.F. & McDonald, B.A. Molecular population genetic analysis differentiates two virulence mechanisms of the fungal avirulence gene NIP1. Mol. Plant Microbe Interact. 17, 1114–1125 (2004).

    Article  Google Scholar 

  24. Friesen, T.L., Ali, S., Klein, K.K. & Rasmussen, J.B. Population genetic analysis of a global collection of Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Phytopathology 95, 1144–1150 (2005).

    Article  CAS  Google Scholar 

  25. Friesen, T.L. & Faris, J.D. Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat. Theor. Appl. Genet. 109, 464–471 (2004).

    Article  CAS  Google Scholar 

  26. Gabriela Roca, M., Read, N. & Wheals, A. Conidial anastomosis tubes in filamentous fungi. FEMS Microbiol. Lett. 249, 191–198 (2005).

    Article  CAS  Google Scholar 

  27. Solomon, P.S., Thomas, S.W., Spanu, P. & Oliver, R.P. The utilisation of di/tripeptides by Stagonospora nodorum is dispensable for wheat infection. Physiol. Mol. Plant Pathol. 63, 191–199 (2003).

    Article  CAS  Google Scholar 

  28. Panaccione, D.G. et al. Elimination of ergovaline from a grass-Neotyphodium endophyte symbiosis by genetic modification of the endophyte. Proc. Natl. Acad. Sci. USA 98, 12820–12825 (2001).

    Article  CAS  Google Scholar 

  29. Liu, Z.H. et al. A wheat intervarietal genetic linkage map based on microsatellite and target region amplified polymorphism markers and its utility for detecting quantitative trait loci. Theor. Appl. Genet. 111, 782–794 (2005).

    Article  CAS  Google Scholar 

  30. Terauchi, R. & Kahl, G. Rapid isolation of promoter sequences by TAIL-PCR: the 5′-flanking regions of Pal and Pgi genes from yams (Dioscorea). Mol. Gen. Genet. 263, 554–560 (2000).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank J. Krupinsky and S. Ali for fungal isolates and K. Rybak, J. Hane, D. Holmes and P. Meyer for technical assistance. This work was supported by Organisation for Economic Co-operation and Development (JA00032562), Grains Research and Development Corporation Australia (UMU88, UMU00022 and UMU14), the Swiss National Science Foundation (Grant 3100A0-104145) and the USDA-ARS (CRIS 5442-22000-037-00D and CRIS 5442-22000-030-00D).

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Authors

Contributions

T.L.F. supervised the work on SN2K; carried out the phenotyping and contributed to writing the paper; Z.L. performed the TAIL PCR and generated the ToxA transformants; S.M. supervised protein blot analysis and purification of ToxA; H.L. performed purification of ToxA; J.D.F. performed all host genetic analysis, including QTL analysis; J.B.R. constructed the vectors for transformation; P.S.S. generated the SN15 knockout; B.A.M. and E.H.S. conducted the population genetic analyses of the ToxA locus in both fungi and contributed to writing the paper; and R.P.O. carried out the sequence comparisons of ToxA and S. nodorum, supervised the work on SN15 and contributed to writing the paper.

Note: Supplementary information is available on the Nature Genetics website.

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Correspondence to Richard P Oliver.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Protein blot of authentic PtrToxA and fungal extracts. (PDF 1229 kb)

Supplementary Table 1

List of isolates used for screening and sequencing. (PDF 19 kb)

Supplementary Table 2

Primer sequences. (PDF 9 kb)

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Friesen, T., Stukenbrock, E., Liu, Z. et al. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38, 953–956 (2006). https://doi.org/10.1038/ng1839

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