Evolution, diversity, and function of the disease susceptibility gene Snn1 in wheat

Authors: SENEVIRATNE, SUDESHI - North Dakota State University; SHI, GONGJUN - North Dakota State University; SZABO-HEVER, AGNES - North Dakota State University; Zhang, Zengcui; Peters Haugrud, Amanda; RUNNING, KATHERINE - North Dakota State University; SINGH, GURMINDER - North Dakota State University; Nandety, Raja Sekhar; Fiedler, Jason; MCCLEAN, PHILIP - North Dakota State University; Xu, Steven; Friesen, Timothy; Faris, Justin

Submitted to: The Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/30/2024
Publication Date: 6/23/2024
Citation: Seneviratne, S., Shi, G., Szabo-Hever, A., Zhang, Z., Peters Haugrud, A.R., Running, K., Singh, G., Nandety, R.S., Fiedler, J.D., Mcclean, P., Xu, S.S., Friesen, T.L., Faris, J.D. 2024. Evolution, diversity, and function of the disease susceptibility gene Snn1 in wheat. The Plant Journal. 119(4):1720-1736. https://doi.org/10.1111/tpj.16879.
DOI: https://doi.org/10.1111/tpj.16879

Interpretive Summary: The disease known as Septoria nodorum blotch, or SNB, is caused by a fungal pathogen that infects wheat plants and can cause substantial losses in grain yield. When a specific protein known as Tox1 is produced by the fungus and it is recognized by the wheat gene named Snn1, there is a compatible interaction that leads to disease in the wheat plant. Here, researchers conducted genetic, genomic, and bioinformatic analyses to determine how the Snn1 gene evolved, characterize the level of genetic diversity among wheat lines that carry the Snn1 gene, determine how the Snn1 gene functions to recognize the fungal SnTox1 protein, and to develop molecular markers that can be used by wheat breeders to track the Snn1 gene. The researchers found that some wheat lines carry two copies of Snn1, and the second copy resulted from a relatively recent genetic duplication of the first copy. Specific features in the DNA of the Snn1 genes were identified that dictate whether Snn1 can recognize SnTox1 thereby making the wheat plant either resistant or susceptible to SNB. These features were targeted for the development of several molecular markers that can be used in efficient DNA assays to determine if the Snn1 gene is present, and therefore if a given wheat plant will be resistant or susceptible to SNB. These marker assays will serve as useful tools to wheat breeders for the efficient development of SNB-resistant wheat varieties.

Technical Abstract: Septoria nodorum blotch (SNB), caused by Parastagonospora nodorum, is a disease of durum and common wheat initiated by the recognition of pathogen-produced necrotrophic effectors (NEs) by specific wheat genes. The wheat gene Snn1 encodes a wall-associated kinase that directly interacts with the NE SnTox1 leading to the development of SNB. Here, sequence analysis of Snn1 from 114 accessions including diploid, tetraploid, and hexaploid wheat species revealed that some wheat lines possess two copies of Snn1 (designated Snn1-B1 and Snn1-B2) approximately 120 kb apart. Snn1-B2 evolved relatively recently as a paralog of Snn1-B1, and both genes have undergone diversifying selection. Three point mutations associated with the formation of the first SnTox1-sensitive Snn1-B1 allele from a primitive wild wheat were identified. Four subsequent and independent SNPs, three in Snn1-B1 and one in Snn1-B2, that converted the sensitive alleles to insensitive forms were also identified. These four mutations were predicted to disrupt the compatible Snn1-SnTox1 interaction either through destabilization of the Snn1 protein or direct disruption of the protein-protein interaction. High-throughput markers were developed for the causal mutations and evaluated on panels of durum and common wheat. The markers were able to correctly identify 96.9 % of SnTox1-sensitive durum wheat accessions, and a marker for the null allele was 100% accurate at predicting SnTox1-insensitive lines in both durum and spring wheat. Results of this study increase our understanding of the evolution, diversity, and function of Snn1-B1 and Snn1-B2 genes and will be useful for marker-assisted elimination of these genes for better host resistance.