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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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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).

Author information

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.

Competing interests

The authors declare no competing financial interests.

Correspondence to Richard P Oliver.

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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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).