A triple threat: The Parastagonospora nodorum SnTox267 effector exploits three distinct host genetic factors to cause disease in wheat

Authors: RICHARDS, JONATHAN - Louisiana State University Agcenter; SENEVIRATNE, SUDESHI - North Dakota State University; WYATT, NATHAN - Orise Fellow; Xu, Steven; LIU, ZHAOHUI - North Dakota State University; Faris, Justin; Friesen, Timothy

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/27/2021
Publication Date: 7/6/2021
Citation: Richards, J.K., Seneviratne, S., Wyatt, N., Xu, S.S., Liu, Z., Faris, J.D., Friesen, T.L. 2021. A triple threat: The Parastagonospora nodorum SnTox267 effector exploits three distinct host genetic factors to cause disease in wheat. New Phytologist. https://doi.org/10.1111/nph.17601.
DOI: https://doi.org/10.1111/nph.17601

Interpretive Summary: Parastagonospora nodorum, causal agent of septoria nodorum blotch of wheat, is a destructive pathogen that causes disease by inducing necrotic spots on the leaves that reduce the photosynthetic area, resulting in yield and quality losses to growers. Understanding how this pathogen invades wheat to complete its pathogenic life cycle is critical to successful resistance breeding and the control of the SNB disease problem. In the current work, we identified and characterized the protein SnTox267. It was previously proposed that SnTox267 was three different proteins named SnTox2, SnTox6, and SnTox7 that targeted wheat susceptibility genes Snn2, Snn6, and Snn7, respectively. Here we cloned and validated SnTox267 to show that a single protein targeted three genetically distinct host genes to cause disease. Two of these genes Snn2 and Snn6 acted cooperatively to elicit SnTox267-induced disease. SnTox267 also targeted the wheat susceptibility gene Snn7 showing that SnTox267 is hijacking at least two susceptibility pathways to cause disease. The characterization of the interactions involving SnTox267 are important to other scientists working on this and other necrotrophic pathosystems. This information is also important for wheat geneticists and breeders trying to develop durable resistance to septoria nodorum blotch.

Technical Abstract: Parastagonospora nodorum is a fungal pathogen of wheat. As a necrotrophic specialist, it deploys a suite of effector proteins that target dominant host susceptibility genes to elicit programmed cell death (PCD). Previously, nine effector – host susceptibility gene interactions were reported in this pathosystem, presumably governed by unique pathogen effectors. This study presents the characterization of the SnTox267 necrotrophic effector which was shown to hijack two separate host pathways to cause necrosis. An association mapping approach successfully identified SnTox267 and the generation of gene-disrupted mutants, and gain-of-function transformants confirmed its role in Snn2, Snn6, and Snn7 mediated necrosis. We demonstrated that the previously identified Snn2 and Snn6 host susceptibility genes function cooperatively to elicit SnTox267-induced necrosis in the same light-dependent PCD pathway. Additionally, we showed that SnTox267 targets Snn7, resulting in a light-independent necrosis. Sequence comparison among a natural population of 197 North American P. nodorum isolates identified 20 protein isoforms which conferred variable levels of quantitative virulence, indicating continuing evolutionary pressure on this effector gene. Protein isoform prevalence among discrete populations indicated that SnTox267 has likely evolved in response to local selection pressures and has diversified more rapidly in the Upper Midwest population. Deletion of SnTox267 resulted in the upregulation of the sequence unrelated effector genes SnToxA, SnTox1, and SnTox3, which provides evidence for a complex genetic compensation mechanism. Taken together, these results illustrate a novel evolutionary mechanism by which a necrotrophic fungal pathogen uses a single proteinaceous effector to hijack two host pathways to cause cell death.