Protein Kinase-Major Sperm Protein (PK-MSP) Genes Mediate Recognition of the Fungal Necrotrophic Effector SnTox3 to Cause Septoria nodorum Blotch in Wheat.

Abstract

The wheat-Parastagonospora nodorum pathosystem has emerged as a model system for plant-necrotrophic fungal pathogen interactions. In this system, fungal necrotrophic effectors are recognized by specific host genes in an inverse gene-for-gene manner to induce programmed cell death and other host responses, which leads to disease. We previously cloned a wheat gene (Snn3-D1) encoding protein kinase and major sperm protein domains that recognizes the P. nodorum necrotrophic effector SnTox3. Here, we identified an Snn3-D1 homoeolog (Snn3-B1) and a paralog (Snn3-B2) that also recognize SnTox3, leading to susceptibility. DNA sequence divergence of Snn3-B1 and Snn3-B2 and differences in transcriptional expression patterns and three-dimensional protein conformation were associated with a more severe programmed cell death response conferred by Snn3-B2 compared with Snn3-B1. Both Snn3 proteins were localized to the nucleus and cytoplasm in wheat protoplasts, suggesting that they may have acquired novel functions compared with previously characterized major sperm protein domain-containing proteins in other species. Snn3-B2 was previously shown to govern osmotic stress and salt tolerance, indicating that protein kinase-major sperm protein 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. [Formula: see text] The author(s) have dedicated the work to the public domain under the Creative Commons CC0 "No Rights Reserved" license by waiving all of his or her rights to the work worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law, 2025.