Barley stem rust resistance mechanisms: Diversity, gene structure, and function suggest a recently evolved host-pathogen relationship
580Stem rust caused by Puccinia graminis f. sp. tritici was historically one of the most devastating diseases of barley and wheat. The barley resistance gene Rpg1 provided remarkably durable resistance against diverse stem rust races in the United States until P. graminis f. sp. tritici race QCCJF emerged in the US, which was virulent on barley lines containing Rpg1. Of higher concern for cereal production worldwide were the highly virulent race TTKSK (A.K.A. Ug99) and its variants, which are virulent on most of world’s commercial wheat varieties and barley cultivars, including those containing Rpg1. Cloning and characterization of the Rpg1 gene demonstrated that the resistance responses are activated within minutes of avirulent spores landing on the leaf surface, indicative of an early cell surface receptor mediated resistance response, possibly representing early non race specific PAMP triggered immunity. The emergence of P. graminis f. sp. tritici races QCCJF and TTKSK prompted the identification of new wheat stem rust resistance genes in barley effective against these new threats. As a result the barley rpg4/Rpg5 resistance locus was identified on chromosome 5H and cloning efforts showed that the locus harbors three tightly linked genes (Rpg5, HvRga1 and HvAdf3) that function together to provide resistance against a broad spectrum of stem rust races including QCCJF and TTKSK. Rpg5 and HvRga1 are tightly linked nucleotide binding site-leucine rich repeat (NLR) R-genes with head-to-head genome architecture typical of dual NLR R-genes that function together for race specific resistances. Rpg5 and HvRga1 possibly follow the “integrated decoy” model where one NLR with an integrated domain functions as the pathogen “sensor and activator” and the second NLR functions as a “repressor” of resistance signaling. Rpg5 has the typical NLR domains and a C-terminal serine threonine protein kinase domain that is indispensable for resistance function and possibly acts as the pathogen sensory domain. Interestingly, Rpg5 alleles evolved that contain a phosphatase domain instead of kinase domain that compromise stem rust resistance and act as dominant susceptibility factors explaining the recessive nature of the rpg4-mediated wheat stem rust resistance. The requirement of the actin depolymerization factor, HvAdf3, for the rpg4/Rpg5 mediated resistance response is also not surprising as actin cytoskeleton remodeling during pathogen attack is crucial, not only to provide a physical barrier to block pathogen ingress, but also working as an early pathogen sensing mechanism to prepare for later robust Rpg5/HvRga1 mediated hypersensitive responses. Parallels drawn from the model pathosystem Arabidopsis-Pseudomonas syringe are aiding in our understanding of the complex and intertwined 581molecular orchestra involving cytoskeleton dynamics and cellular signaling operating in barley-stem rust pathosystem. Mounting evidence shows that the early immunity responses effective against broad races of wheat stem rust in barley, that are elicited before haustorial development, probably represent non-host resistance mechanisms suggesting that barley may represent a recent host of the wheat stem rust pathogen.