Genetics of variable disease expression conferred by inverse gene-for-gene interactions in the wheat-Parastagonospora nodorum pathosystem

Authors: PETERS HAUGRUD, A - North Dakota State University; Zhang, Zengcui; RICHARDS, J - North Dakota State University; Friesen, Timothy; Faris, Justin

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/24/2019
Publication Date: 5/1/2019
Publication URL: http://handle.nal.usda.gov/10113/6477325
Citation: Peters Haugrud, A.R., Zhang, Z., Richards, J.K., Friesen, T.L., Faris, J.D. 2019. Genetics of variable disease expression conferred by inverse gene-for-gene interactions in the wheat-Parastagonospora nodorum pathosystem. Plant Physiology. 180(1):420-434. https://doi.org/10.1104/pp.19.00149.
DOI: https://doi.org/10.1104/pp.19.00149

Interpretive Summary: The disease known as Septoria nodorum blotch is caused by a fungal pathogen and causes severe yield losses in wheat worldwide. Research in past years has revealed that the pathogen produces molecules that, when recognized by specific genes in the wheat plant, causes responses in the plant that allow the pathogen to grow and proliferate, ultimately leading to disease. Therefore, recognition of the pathogen by the plant leads to disease susceptibility as opposed to resistance, and these interactions are therefore considered the inverse of typical plant-pathogen interactions. The genetic components in both the plant and the pathogen have been discovered for a few of these interactions, but studies to determine how the interactions contribute to disease susceptibility in the presence of other interactions has not been determined. Here, we conducted genetic analysis using several different strains of the pathogen to study the combined and individual effects of interactions involving three wheat genes that each specifically recognize three different pathogen molecules to cause disease. The results indicated that the effects of the three interactions in causing disease varied among the different pathogen strains tested, and molecular tests showed that this variation corresponded to the levels of expression of the genes responsible for coding the pathogen molecules, i.e. increased expression of a pathogen molecule caused the corresponding plant gene-pathogen molecule interaction to account for relatively higher levels of disease than when the pathogen molecule was expressed at a lower level. Analysis also indicated not only that different pathogen strains produce these molecules at different levels, but the expression of some of the molecules in some strains led to decreased expression of others. In conclusion, the results of this study indicate that the levels of expression of the pathogen molecules dictates the levels of disease that develops on wheat plants with the corresponding recognition gene, and that the regulation of expression of these molecules is complex. This work furthers our understanding of this plant-pathogen system and will help to devise novel strategies to control yield losses attributed to Septoria nodorum blotch.

Technical Abstract: The wheat-Parastagonospora nodorum 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 (NETS) and ultimately the disease septoria nodorum blotch (SNB). Here, we used multiple pathogen isolates to individually evaluate the effects of the host gene-NE interactions Tsn1-SnToxA, Snn1-SnTox1, and Snn3-B1-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 with three P. nodorum isolates that produce all three NEs indicated that the Tsn1-SnToxA and Snn3-B1-SnTox3 interactions contributed to disease caused by all four isolates, but their effects varied and ranged from epistatic to additive. The Snn1-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 SnTox1 was differentially expressed between these three isolates post infection. Further analysis of NE gene-knockout isolates showed that effects of some interactions can 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 NETS in the wheat-P. nodorum pathosystem vary in their effects depending on the genetic backgrounds of the pathogen as well as the host, and interplay among the interactions is complex and intricately regulated.