The conserved nematode pheromone ascr#18 primes plant immunity

Plants sense a diverse array of small molecules and macromolecules derived from their natural environment, including diverse microbe-associated molecular patterns (MAMPs) that can trigger defense responses. Several MAMPs have been shown to prime plants for enhanced defense, providing extended protection against pathogens with minimal fitness costs. However, the extent to which conserved small molecule signatures of other phyla contribute to priming of plant defenses is unclear. Here, we demonstrate that exposure of seeds or plants to the ascaroside ascr#18, a pheromone secreted by plant-parasitic and free-living soil nematodes, primes immune genes for enhanced expression upon pathogen challenge, thereby increasing resistance to diverse microbial pathogens. We further show that ascr#18-induced priming is associated with the formation of open chromatin in the regulatory regions of defense genes. Defense priming and disease protection by ascr#18 is compromised in Arabidopsis mutants defective in the receptor of ascr#18, the leucine-rich repeat receptor-like kinase NILR1. Defense priming by ascr#18 is retained under field conditions, demonstrating potential of ascaroside treatment as a crop protection strategy to reduce pesticide usage. Our findings provide insight into the molecular basis of defense priming by ascr#18 and demonstrate how evolutionarily conserved small molecule signatures of plant-associated macrobiota modulate immunity.