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

Authors: Zhang, Zengcui; RUNNING, KATHERINE - North Dakota State University; SUDESHI, SENEVIRATNE - Orise Fellow; PETERS HAUGRUD, AMANDA - North Dakota State University; SZABO-HEVER, AGNES - Orise Fellow; SHI, GONGJUN - North Dakota State University; BRUEGGEMAN, ROBERT - Washington State University; Xu, Steven; Friesen, Timothy; Faris, Justin

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/8/2021
Publication Date: 2/11/2021
Citation: Zhang, Z., Running, K.L., Sudeshi, S., Peters Haugrud, A.R., Szabo-Hever, A., Shi, G., Brueggeman, R.S., Xu, S.S., Friesen, T.L., Faris, J.D. 2021. A protein kinase-major sperm protein gene hijacked by a necrotrophic fungal pathogen triggers disease susceptibility in wheat. Plant Journal. 106(3):720-732. https://doi.org/10.1111/tpj.15194.
DOI: https://doi.org/10.1111/tpj.15194

Interpretive Summary: Septoria nodorum blotch (SNB) is a foliar disease of wheat that threatens production worldwide, and it is caused by a fungus that feeds on dead or dying leaf tissue. Susceptibility to SNB is governed by specific genes in the wheat plant that recognize specific molecules produced by the fungus, and when recognition takes place, disease ensues. Here, researchers conducted genetic and molecular biology experiments to identify one of the wheat genes responsible for recognizing one of the fungal molecules. The gene, designated Snn3-D1, contained two major features. One feature, known as a protein kinase domain, is known to be involved in molecular signaling within the plant cell and is likely involved in initiation of cell death, which would lead to SNB susceptibility. The second feature identified within the Snn3-D1 gene was a major sperm protein domain. The function of this feature has not yet been characterized in plants, but it is known to be involved in the motility of sperm in nematodes. Additional characterization of the Snn3-D1 gene revealed that it is down-regulated by light and up-regulated by darkness, and the gene likely originated in a relative of wheat that grows native in the Middle East. This research shows that the fungus that causes SNB can take advantage of the molecular functions of diverse plant genes to trigger disease susceptibility.

Technical 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 have been shown to play major roles in causing SNB. Cloning and characterization of wheat sensitivity genes will further our understanding of the wheat-P. nodorum pathosystem. We conducted high-resolution mapping and chromosome walking to identify candidate genes conferring sensitivity to the P. nodorum-produced NE SnTox3. The wheat gene that recognizes SnTox3 to confer susceptibility, named Snn3-D1, was cloned and validated by mutagenesis. Snn3-D1 contains a protein kinase (PK) and a major sperm protein (MSP) domain, both of which are critical for Snn3-D1 gene function. A compatible Snn3-D1-SnTox3 interaction is light independent, but Snn3-D1 transcriptional expression is down-regulated by light and up-regulated under darkness. Genes with PK and MSP domains appear to exist only in monocot plants. In Ae. tauschii, the D-genome progenitor of wheat, Snn3-D1 likely emerged 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 and pathways to trigger SNB susceptibility in wheat.