Cross-family transfer of the Arabidopsis cell-surface immune receptor LORE to tomato confers sensing of 3-hydroxylated fatty acids and enhanced disease resistance

Abstract

Plant pathogens pose a high risk of yield losses and threaten food security. Technological and scientific advances have improved our understanding of the molecular processes underlying host-pathogen interactions, which paves the way for new strategies in crop disease management beyond the limits of conventional breeding. Cross-family transfer of immune receptor genes is one such strategy that takes advantage of common plant immune signaling pathways to improve disease resistance in crops. Sensing of microbe- or host damage-associated molecular patterns (MAMPs/DAMPs) by plasma membrane-resident pattern recognition receptors (PRR) activates pattern-triggered immunity (PTI) and restricts the spread of a broad spectrum of pathogens in the host plant. In the model plant Arabidopsis thaliana, the S-domain receptor-like kinase LIPOOLIGOSACCHARIDE-SPECIFIC REDUCED ELICITATION (AtLORE, SD1-29) functions as PRR, which senses medium chain-length 3-hydroxylated fatty acids (mc-3-OH-FAs), such as 3-OH-C10:0, and 3-hydroxyalkanoates (HAAs) of microbial origin to activate PTI. In this study, we show that ectopic expression of the Brassicaceae-specific PRR AtLORE in the solanaceous crop species Solanum lycopersicum cv. M82 leads to the gain of 3-OH-C10:0 immune sensing without altering plant development. AtLORE-transgenic tomato shows enhanced resistance against Pseudomonas syringae pv. tomato DC3000 and Alternaria solani NL03003. Applying 3-OH-C10:0 to the soil before infection induces resistance against the oomycete pathogen Phytophthora infestans Pi100 and further enhances resistance to A. solani NL03003. Our study proposes a potential application of AtLORE-transgenic crop plants and mc-3-OH-FAs as resistance-inducing bio-stimulants in disease management.