NLR with Janus Faced Integrated Sensory Domains

The barley NBS-LRR (NLR) genes, Rpg5 and HvRga1, are required together for resistance to Puccinia graminis f. sp. Tritici(Pgt) the wheat stem rust pathogen. The “integrated decoy hypothesis” outlines the role of dual NLR genes and why one typically contains a fused mimic of a protein that was originally a host protein targeted by a pathogen virulence effector to facilitate disease. Yet, once fused to a NLR immunity receptor acts as an integrated sensory domains (ISD) to trap the pathogen and initiate defense. Alleles of Rpg5 contain two diverse C-terminal ISDs, the Rpg5 resistance allele has a serine threonine protein kinase (PK) ISD whereas the major class of rpg5 susceptible alleles contain a protein phosphatase 2C (PP2C) ISD. Genetic and functional analysis shows that in the heterozygous state the Rpg5-PK and Rpg5-PP2C alleles functions antagonistically resulting in recessive segregation. Thus, the rpg5-PP2C allele acts as a dominant susceptibility factor suppressing Rpg5-PK mediated Pgt resistance. Interestingly, the Rpg5-PK ISD progenitor, HvAPK1b, is the Arabidopsis AtAPK1b orthologue, which is involved in stomatal aperture opening in response to light. We hypothesize that the pathogen effector, Avr-45, manipulates HvApk1b during the infection process, which evolved to occur in the dark, allowing pathogen entry through otherwise closed stomata. Counter evolution during the molecular arms race, directed by duplication and translocation of the HvAPK1b target protein, resulted in the Rpg5 NLR-HvApk1b integrated decoy immunity receptor. Thus, the pathogen’s attempt at incognito entry betrays itself resulting in activation of defense.