unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens

• Published in: Proceedings of the National Academy of Sciences - PNAS 2010-07, Vol.107 (30), p.13544-13549
• Main Authors: Faris, Justin D, Zhang, Zengcui, Lu, Huangjun, Lu, Shunwen, Reddy, Leela, Cloutier, Sylvie, Fellers, John P, Meinhardt, Steven W, Rasmussen, Jack B, Xu, Steven S, Oliver, Richard P, Simons, Kristin J, Friesen, Timothy L
• Format: Article
• Language: English
• Subjects: Alleles; Amino Acid Sequence; Ascomycota - metabolism; Ascomycota - physiology; Binding sites; Biological Sciences; Chromosome Mapping; Chromosomes; Chromosomes, Plant - genetics; Cloning; Cloning, Molecular; disease resistance; DNA, Plant - chemistry; DNA, Plant - genetics; fungal diseases of plants; Fungi; Gene expression; Gene Expression Regulation, Plant; Genes; Genes, Plant - genetics; Genomes; Genomics; Genotype & phenotype; Host-Pathogen Interactions; host-pathogen relationships; Immunity, Innate - genetics; Kinases; Leptosphaeria nodorum; molecular cloning; Molecular Sequence Data; Mutation; Mycotoxins - genetics; Mycotoxins - metabolism; nucleotide sequences; Pathogens; Phylogeny; Plant diseases; Plant Diseases - genetics; Plant Diseases - microbiology; Plant Proteins - classification; Plant Proteins - genetics; Plant Proteins - metabolism; Plants; polypeptides; Protein Binding; Proteins; Pyrenophora tritici-repentis; Reverse Transcriptase Polymerase Chain Reaction; Rice; Sequence Analysis, DNA; Sequence Homology, Amino Acid; Triticum; Triticum - classification; Triticum - genetics; Triticum - microbiology; Triticum aestivum; Tsn1 gene; Two-Hybrid System Techniques; Wheat
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1004090107

Plant disease resistance is often conferred by genes with nucleotide binding site (NBS) and leucine-rich repeat (LRR) or serine/threonine protein kinase (S/TPK) domains. Much less is known about mechanisms of susceptibility, particularly to necrotrophic fungal pathogens. The pathogens that cause the diseases tan spot and Stagonospora nodorum blotch on wheat produce effectors (host-selective toxins) that induce susceptibility in wheat lines harboring corresponding toxin sensitivity genes. The effector ToxA is produced by both pathogens, and sensitivity to ToxA is governed by the Tsn1 gene on wheat chromosome arm 5BL. Here, we report the cloning of Tsn1, which was found to have disease resistance gene-like features, including S/TPK and NBS-LRR domains. Mutagenesis revealed that all three domains are required for ToxA sensitivity, and hence disease susceptibility. Tsn1 is unique to ToxA-sensitive genotypes, and insensitive genotypes are null. Sequencing and phylogenetic analysis indicated that Tsn1 arose in the B-genome diploid progenitor of polyploid wheat through a gene-fusion event that gave rise to its unique structure. Although Tsn1 is necessary to mediate ToxA recognition, yeast two-hybrid experiments suggested that the Tsn1 protein does not interact directly with ToxA. Tsn1 transcription is tightly regulated by the circadian clock and light, providing further evidence that Tsn1-ToxA interactions are associated with photosynthesis pathways. This work suggests that these necrotrophic pathogens may thrive by subverting the resistance mechanisms acquired by plants to combat other pathogens.