Submitted to: Nature Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/8/2006
Publication Date: 7/10/2006
Citation: Friesen, T.L., Stukenbrock, E.H., Liu, Z., Meinhardt, S., Ling, H., Faris, J.D., Rasmussen, J.B., Solomon, P.S., McDonald, B.A., Oliver, R.P. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genetics. 38(8):953-956. Interpretive Summary: The ToxA gene of Pyrenophora tritici-repentis, the fungal pathogen causing tan spot of wheat, is highly important in disease development. Sensitive wheat lines are more susceptible to isolates of the pathogen expressing ToxA, which encodes a protein toxic to wheat. Stagonospora nodorum is a related fungus that also infects wheat. When the sequence of the whole genome of S. nodorum was analyzed, we found a gene that is almost identical to ToxA, called SnToxA. Disruption of SnToxA so that it couldn’t be expressed resulted in substantially reduced virulence on ToxA sensitive wheat lines. The sequences of ToxA genes from a world wide collection of isolates of P. tritici-repentis and S. nodorum were determined. The ToxA sequences from P. tritici-repentis isolates were found to be identical to each other and were very similar to the known SnToxA sequence, whereas the SnToxA sequences varied a great deal among S. nodorum isolates in the collection. In addition to ToxA, the transposase gene and flanking sequence found in S. nodorum was also present in P. tritici-repentis. These findings suggest that the gene from S. nodorum was transferred naturally to P. tritici-repentis fairly recently (“horizontal gene transfer”), resulting in the creation of a more virulent pathogen of wheat.
Technical Abstract: The ToxA gene of the ascomycete fungal pathogen Pyrenophora tritici-repentis controls specificity of the interaction with its host, wheat. Host genotypes carrying dominant alleles of Tsn1 are susceptible to isolates of the pathogen expressing ToxA. Pyrenophora tritici-repentis isolates lacking ToxA cause only minor symptoms. Stagonospora (Phaeosphaeria) nodorum is a related pathogen, which also infects wheat. Whole genome sequence analysis of Stagonospora nodorum revealed the presence of a gene that is almost identical to ToxA, called SnToxA, adjacent to a transposase-like gene. SnToxA was expressed especially during early infection of wheat. Disruption of SnToxA by gene replacement resulted in strains that failed to infect wheat lines carrying Tsn1. ToxA genes from a world wide collection of isolates of Pyrenophora tritici-repentis and Stagonospora nodorum were sequenced. The Pyrenophora tritici-repentis sequences were found to be identical to each other and very similar to the SnToxA sequence present in a West Australian isolate of StagonosporaS. nodorum. The Stagonospora nodorum sequences were highly variable and showed an excess of non-synonymous codon changes over synonymous, suggesting diversifying selection. In addition to ToxA, the transposase gene and flanking sequence comprising 11.2 kb was present in Pyrenophora tritici-repentis. These findings suggest a recent horizontal gene transfer event from Stagonospora nodorum to Pyrenophora tritici-repentis, resulting in the creation of a novel disease causing agent.