title: A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens.
abstract: 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.
authors.affiliation: Cereal Crops Research Unit, Northern Crop Science Laboratory, US Department of Agriculture-Agricultural Research Service, Fargo, ND 58102, USA. justin.faris@ars.usda.gov
authors.forename: Justin D
authors.initials: JD
authors.lastname: Faris
authors.forename: Zengcui
authors.initials: Z
authors.lastname: Zhang
authors.forename: Huangjun
authors.initials: H
authors.lastname: Lu
authors.forename: Shunwen
authors.initials: S
authors.lastname: Lu
authors.forename: Leela
authors.initials: L
authors.lastname: Reddy
authors.forename: Sylvie
authors.initials: S
authors.lastname: Cloutier
authors.forename: John P
authors.initials: JP
authors.lastname: Fellers
authors.forename: Steven W
authors.initials: SW
authors.lastname: Meinhardt
authors.forename: Jack B
authors.initials: JB
authors.lastname: Rasmussen
authors.forename: Steven S
authors.initials: SS
authors.lastname: Xu
authors.forename: Richard P
authors.initials: RP
authors.lastname: Oliver
authors.forename: Kristin J
authors.initials: KJ
authors.lastname: Simons
authors.forename: Timothy L
authors.initials: TL
authors.lastname: Friesen
mesh_terms: D000595:Amino Acid Sequence; D001203:Ascomycota / Q000378:metabolism / Q000502:physiology*; D002874:Chromosome Mapping; D032461:Chromosomes, Plant / Q000235:genetics; D003001:Cloning, Molecular; D018744:DNA, Plant / Q000737:chemistry / Q000235:genetics; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant / Q000235:genetics*; D054884:Host-Pathogen Interactions; D007113:Immunity, Innate / Q000235:genetics; D008969:Molecular Sequence Data; D009154:Mutation; D009183:Mycotoxins / Q000235:genetics / Q000378:metabolism; D010802:Phylogeny; D010935:Plant Diseases / Q000235:genetics / Q000382:microbiology; D010940:Plant Proteins / Q000145:classification / Q000235:genetics* / Q000378:metabolism; D011485:Protein Binding; D020133:Reverse Transcriptase Polymerase Chain Reaction; D017422:Sequence Analysis, DNA; D017386:Sequence Homology, Amino Acid; D014908:Triticum / Q000145:classification / Q000235:genetics* / Q000382:microbiology*; D020798:Two-Hybrid System Techniques
chemical_list: D018744:DNA, Plant; D009183:Mycotoxins; D010940:Plant Proteins