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Title: Concerted action of two avirulent spore effectors activates Reaction to Puccinia graminis 1 (Rpg1)-mediated cereal stem rust resistance

item NIRMALA, J - Washington State University
item DRADER, T. - Washington State University
item LAWRENCE, P. - Washington State University
item YIN, C. - Washington State University
item HULBERT, SCOT - Washington State University
item Steber, Camille
item STEFFENSON, B. - Washington State University
item Szabo, Les
item VON WETTSTEIN, D. - Washington State University
item KLEINHOFS, A. - Washington State University

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/30/2011
Publication Date: 8/30/2011
Citation: Nirmala, J., Drader, T., Lawrence, P.K., Yin, C., Hulbert, S., Steber, C.M., Steffenson, B.J., Szabo, L.J., Von Wettstein, D., Kleinhofs, A. 2011. Concerted action of two avirulent spore effectors activates Reaction to Puccinia graminis 1 (Rpg1)-mediated cereal stem rust resistance. Proceedings of the National Academy of Sciences. 108(35):14676-81.

Interpretive Summary: The Rpg1 (Reaction to Puccinia graminis 1) gene provides barley with resistance to the pathogen that causes stem rust, a disease that can drastically reduce yield. Over time pathogens overcome the ability of plant disease resistance genes to block infection. When new virulent races, such as Ug99, overcome crop disease resistance they can have devastating consequences. The Rpg1 gene is unique in that it provided durable resistance, controlling the disease for a very long time. In developing new strategies for plant disease resistance it is important to understand what mechanisms make durable resistance genes successful. This study identified that proteins from the pathogen that are recognized by the Rpg1 resistance gene, and elucidates the initial signaling events triggering resistance.

Technical Abstract: The barley stem rust resistance gene Reaction to Puccinia graminis 1 (Rpg1), encoding a receptor-like kinase, confers durable resistance to the stem rust pathogen Puccinia graminis f. sp. tritici. The fungal urediniospores form adhesion structures with the leaf epidermal cells within 1 h of inoculation, followed by hyphae and haustorium formation. The RPG1 protein is constitutively expressed and not phosphorylated. On inoculation with avirulent urediniospores, it is phosphorylated in vivo within 5 min and subsequently degraded. Application of arginine-glycine-aspartic acid peptide loops prevented the formation of adhesion structures for spore attachment, the phosphorylation of RPG1, and germination of the viable spores. Arginine-glycine-aspartic acid affinity chromatography of proteins from the ungerminated avirulent rust spores led to the purification and identification of a protein with fibronectin type III and breast cancer type 1 susceptibility protein domains and a vacuolar protein sorting-associated protein 9 with a coupling of ubiquitin to endoplasmic reticulum degradation domain. Both proteins are required to induce in vivo phosphorylation and degradation of RPG1. Combined application of both proteins caused hypersensitive reaction on the stem rust-resistant cultivar Morex but not on the susceptible cultivar Steptoe. Expression studies indicated that mRNA of both genes are present in ungerminated urediniospores and are constitutively transcribed in sporelings, infected leaves, and haustoria in the investigated avirulent races. Evidence is presented that RPG1, in yeast, interacts with the two protein effectors from the urediniospores that activate cooperatively the stem rust resistance protein RPG1 long before haustoria formation.