Protein kinase-major sperm protein (PK-MSP) genes mediate recognition of the fungal necrotrophic effector SnTox3 to cause septoria nodorum blotch in wheat

Authors: Zhang, Zengcui; RUNNING, KATHERINE - North Dakota State University; SENEVIRATNE, SUDESHI - North Dakota State University; Peters Haugrud, Amanda; SZABO-HEVER, AGNES - North Dakota State University; SINGH, GURMINDER - North Dakota State University; HOLUSOVA, KATERINA - Institute Of Experimental Botany; MOLNAR, ISTVAN - Institute Of Experimental Botany; DOLEZEL, JAROSLAV - Institute Of Experimental Botany; Friesen, Timothy; Faris, Justin

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/28/2025
Publication Date: 4/16/2025
Citation: Zhang, Z., Running, K., Seneviratne, S., Peters Haugrud, A.R., Szabo-Hever, A., Singh, G., Holusova, K., Molnar, I., Dolezel, J., Friesen, T.L., Faris, J.D. 2025. Protein kinase-major sperm protein (PK-MSP) genes mediate recognition of the fungal necrotrophic effector SnTox3 to cause septoria nodorum blotch in wheat. Molecular Plant-Microbe Interactions. 38(2):315-327. https://doi.org/10.1094/MPMI-10-24-0125-FI.
DOI: https://doi.org/10.1094/MPMI-10-24-0125-FI

Interpretive Summary: Septoria nodorum blotch (SNB) is a disease of wheat that causes significant yield losses in many wheat-growing regions of the world. Some wheat plants contain genes that recognize the fungal pathogen that causes SNB, and when recognition occurs, disease ensues. In this study, researchers identified two wheat genes responsible for pathogen recognition, and they conducted experiments to understand how the genes work. They found some wheat lines that lack both genes and are resistant to SNB. Molecular markers were developed that can be used to track the genes and help develop new disease-resistant wheat varieties through conventional cross-hybridization means.

Technical Abstract: The wheat-Parastagonospora nodorum pathosystem has emerged as a model system for plant-necrotrophic fungal pathogen interactions. In this system, fungal necrotrophic effectors (NEs) are recognized by specific host genes in an inverse gene-for-gene manner to induce programmed cell death (PCD) and other host responses, which leads to disease. We previously cloned a wheat gene (Snn3-D1) encoding protein kinase (PK) and major sperm protein (MSP) domains that recognizes the P. nodorum NE SnTox3. Here, we identified an Snn3-D1 homoeolog (Snn3-B1) and a paralog (Snn3-B2) that also recognize SnTox3 leading to susceptibility. Divergence of Snn3-B1 and Snn3-B2 at the DNA and amino acid sequence levels, and differences in transcriptional expression patterns, cellular protein localization, and 3D protein confirmation are associated with more severe PCD response conferred by Snn3-B2 compared to Snn3-B1. Localization of the Snn3 proteins to the nucleus and cytoplasm suggests neofunctionalization of integrated PK-MSP genes because MSP domain proteins are typically localized to the endoplasmic reticulum and plasma membrane. We also found that Snn3-B2 was previously shown to govern osmotic stress and salt tolerance indicating that PK-MSP genes can act in plant defense responses to both biotic and abiotic stresses. Evaluation of a large collection of wheat lines showed that several alleles of each gene, including absent alleles, exist within the germplasm. Diagnostic markers were developed for the absent alleles of both genes, which will prove useful for marker-assisted selection in wheat to eliminate SnTox3 sensitivity and achieve better disease resistance.