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A protein kinase–major sperm protein gene hijacked by a necrotrophic fungal pathogen triggers disease susceptibility in wheat

Zengcui Zhang, Katherine L. D. Running, Sudeshi Seneviratne, Amanda R. Peters Haugrud, Agnes Szabo‐Hever, Gongjun Shi, Robert Brueggeman, Steven S. Xu, Timothy L. Friesen, Justin D. Faris
plant journal 2021 v.106 no.3 pp. 720-732
Aegilops tauschii, Parastagonospora nodorum, Triticum aestivum, disease susceptibility, fungi, genes, mutagenesis, pathogens, protein kinases, spermatozoa, transcription (genetics), wheat, wheat allergy, Caspian Sea
Septoria nodorum blotch (SNB), a disease caused by the necrotrophic fungal pathogen Parastagonospora nodorum, is a threat to wheat (Triticum aestivum) production worldwide. Multiple inverse gene‐for‐gene interactions involving the recognition of necrotrophic effectors (NEs) by wheat sensitivity genes play major roles in causing SNB. One interaction involves the wheat gene Snn3 and the P. nodorum NE SnTox3. Here, we used a map‐based strategy to clone the Snn3‐D1 gene from Aegilops tauschii, the D‐genome progenitor of common wheat. Snn3‐D1 contained protein kinase and major sperm protein domains, both of which were essential for function as confirmed by mutagenesis. As opposed to other characterized interactions in this pathosystem, a compatible Snn3‐D1–SnTox3 interaction was light‐independent, and Snn3‐D1 transcriptional expression was downregulated by light and upregulated by darkness. Snn3‐D1 likely emerged in Ae. tauschii due to an approximately 218‐kb insertion that occurred along the west bank of the Caspian Sea. The identification of this new class of NE sensitivity genes combined with the previously cloned sensitivity genes demonstrates that P. nodorum can take advantage of diverse host targets to trigger SNB susceptibility in wheat.