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

Abstract

The fungus Parastagonospora nodorum 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 Snn1 and Snn3B1/Snn3D1, respectively. We previously observed that Tox1 is epistatic to the expression of Tox3 and a quantitative trait locus (QTL) on chromosome 2A that contributes to SNB resistance/susceptibility. The expression of Tox1 is significantly higher in the Australian strain SN15 compared to the American strain SN4. Inspection of the Tox1 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 P. nodorum population revealed that a high proportion of Northern Hemisphere isolates possess PE401 whereas the opposite was observed in the Southern Hemisphere. The presence of PE401 ablates the epistatic effect of Tox1 on the contribution of the SNB 2A QTL but not Tox3. PE401 was introduced into the Tox1 promoter regulatory region in SN15 to test for direct regulatory roles. Tox1 expression was markedly reduced in the presence of PE401. This suggests a repressor molecule(s) binds PE401 and inhibits Tox1 transcription. Infection assays also demonstrated that P. nodorum which lacks PE401 is more pathogenic on Snn1 varieties than P. nodorum carrying PE401. An infection competition assay between P. nodorum isogenic strains with and without PE401 indicated that the higher Tox1-expressing strain rescued the reduced virulence of the lower Tox1-expressing strain on Snn1 wheat. Our study demonstrated that Tox1 exhibits both selfish and altruistic characteristics. This offers an insight into a NE arms race that is occurring within the P. nodorum population. The importance of PE401 in breeding for SNB resistance in wheat is discussed.

Surface frustration re-patterning underlies the structural landscape and evolvability of fungal orphan candidate effectors

“…Another layer of complexity emerges from interference between the activity of several effectors, either through epistatic interactions (John et al, 2022) or by cross-suppression of immune recognition (Martel et al, 2022;Lazar et al, 2022). Finally, effectors may promote virulence not by directly targeting host processes but rather by altering the host microbiota (Snelders et al, 2020(Snelders et al, , 2021.…”

Chromatin-immunoprecipitation reveals the PnPf2 transcriptional network controlling effector-mediated virulence in a fungal pathogen of wheat

“…These studies have also described a consistent pattern: the expression of these genes is maximal two to four days after infection and then declines. Furthermore, expression levels can vary by the presence or absence of their matching wheat receptors, as well as by epistasis, whereby one effector gene causes suppression of another (8)(9)(10). Yet relatively little is known concerning the mechanisms governing the effector gene regulation.…”