Genetics of Variable Disease Expression Conferred by Inverse Gene-For-Gene Interactions in the Wheat- Parastagonospora nodorum Pathosystem

The wheat- pathosystem involves the recognition of pathogen-secreted necrotrophic effectors (NEs) by corresponding wheat NE sensitivity genes. This inverse gene-for-gene recognition leads to necrotrophic effector-triggered susceptibility and ultimately septoria nodorum blotch disease. Here, we used multiple pathogen isolates to individually evaluate the effects of the host gene-NE interactions -Stagonospora nodorum ToxinA ( -SnToxA), -Stagonospora nodorum Toxin1 ( -SnTox1), and -Stagonospora nodorum Toxin3 ( -SnTox3), alone and in various combinations, to determine the relative importance of these interactions in causing disease. Genetic analysis of a recombinant inbred wheat population inoculated separately with three isolates, all of which produce all three NEs, indicated that the -SnToxA and -SnTox3 interactions contributed to disease caused by all four isolates, but their effects varied and ranged from epistatic to additive. The -SnTox1 interaction was associated with increased disease for one isolate, but for other isolates, there was evidence that this interaction inhibited the expression of other host gene-NE interactions. RNA sequencing analysis in planta showed that was differentially expressed between these three isolates after infection. Further analysis of NE gene-knockout isolates showed that the effect of some interactions could be masked or inhibited by other compatible interactions, and the regulation of this occurs at the level of NE gene transcription. Collectively, these results show that the inverse gene-for-gene interactions leading to necrotrophic effector-triggered susceptibility in the wheat- pathosystem vary in their effects depending on the genetic backgrounds of the pathogen and host, and interplay among the interactions is complex and intricately regulated.