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 representative P. nodorum isolates from Australia and South Africa. The presence of PE401 removed 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 wheat 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 complex NE-NE interaction that is occurring within the P. nodorum population. The importance of PE401 in breeding for SNB resistance in wheat is discussed.
Highlights
Breeding for effective resistance to fungal diseases in crops is a continual challenge
This element, called PE401 was absent in the Australian P. nodorum SN15 and SN2000 isolates that were associated with a higher level of Tox1 expression (Fig 1A) [16,31,34]
PE401 was examined for features of a mobile genetic element (MGE), as they are known to modulate the expression of proximal fungal genes [38,39,40,41]
Summary
Breeding for effective resistance to fungal diseases in crops is a continual challenge. Namely biotrophs and hemibiotrophs, evolve ways to overcome host resistance by masking themselves to evade pathogen-triggered immunity This can occur through mutations in Avr-effector genes, leading to the loss of recognition and the subsequent breakdown of host resistance that results in ‘boom and bust’ cycles [1]. Necrotrophic fungal pathogens often possess multiple NEs that exploit different dominant-susceptibility genes carried by the host [7] These functional redundancies often require breeders to remove multiple host genes or stack the required number of desirable disease resistance alleles to be effective [8,9]. These situations make it difficult for breeders to provide long-lasting and durable resistance
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