Variability in an effector gene promoter of a necrotrophic fungal pathogen dictates epistasis and effector-triggered susceptibility in wheat

<jats:p>The fungus <jats:italic>Parastagonospora nodorum</jats:italic> uses proteinaceous necrotrophic effectors (NEs) to induce tissue necrosis on wheat leaves during infection, leading to the symptoms of septoria nodorum blotch (SNB). The NEs Tox1 and Tox3 induce necrosis on wheat possessing the dominant susceptibility genes <jats:italic>Snn1</jats:italic> and <jats:italic>Snn3B1/Snn3D1</jats:italic>, respectively. We previously observed that <jats:italic>Tox1</jats:italic> is epistatic to the expression of <jats:italic>Tox3</jats:italic> and a quantitative trait locus (QTL) on chromosome 2A that contributes to SNB resistance/susceptibility. The expression of <jats:italic>Tox1</jats:italic> is significantly higher in the Australian strain SN15 compared to the American strain SN4. Inspection of the <jats:italic>Tox1</jats:italic> promoter region revealed a 401 bp promoter genetic element in SN4 positioned 267 bp upstream of the start codon that is absent in SN15, called PE401. Analysis of the world-wide <jats:italic>P</jats:italic>. <jats:italic>nodorum</jats:italic> population revealed that a high proportion of Northern Hemisphere isolates possess PE401 whereas the opposite was observed in representative <jats:italic>P</jats:italic>. <jats:italic>nodorum</jats:italic> isolates from Australia and South Africa. The presence of PE401 removed the epistatic effect of <jats:italic>Tox1</jats:italic> on the contribution of the SNB 2A QTL but not <jats:italic>Tox3</jats:italic>. PE401 was introduced into the <jats:italic>Tox1</jats:italic> promoter regulatory region in SN15 to test for direct regulatory roles. <jats:italic>Tox1</jats:italic> expression was markedly reduced in the presence of PE401. This suggests a repressor molecule(s) binds PE401 and inhibits <jats:italic>Tox1</jats:italic> transcription. Infection assays also demonstrated that <jats:italic>P</jats:italic>. <jats:italic>nodorum</jats:italic> which lacks PE401 is more pathogenic on <jats:italic>Snn1</jats:italic> wheat varieties than <jats:italic>P</jats:italic>. <jats:italic>nodorum</jats:italic> carrying PE401. An infection competition assay between <jats:italic>P</jats:italic>. <jats:italic>nodorum</jats:italic> isogenic strains with and without PE401 indicated that the higher <jats:italic>Tox1</jats:italic>-expressing strain rescued the reduced virulence of the lower <jats:italic>Tox1</jats:italic>-expressing strain on <jats:italic>Snn1</jats:italic> wheat. Our study demonstrated that <jats:italic>Tox1</jats:italic> exhibits both ‘selfish’ and ‘altruistic’ characteristics. This offers an insight into a complex NE-NE interaction that is occurring within the <jats:italic>P</jats:italic>. <jats:italic>nodorum</jats:italic> population. The importance of PE401 in breeding for SNB resistance in wheat is discussed.</jats:p>