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

Abstract

Septoria nodorum blotch (SNB), a disease caused by the necrotrophic fungal pathogen Parastagonospora nodorum, is a threat to wheat 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 down-regulated by light and up-regulated by darkness. Snn3-D1 likely emerged in Ae. tauschii due to a ~218 kb insertion that occurred along the west bank of the Caspian Sea. The identification of this new class of NE sensitivity gene combined with the previously cloned sensitivity genes demonstrates that P. nodorum can take advantage of diverse host targets to trigger SNB susceptibility in wheat.