Tomato Receptors of the Bacterial Cold Shock Protein and the Plant Peptide Signal Systemin

Abstract

Plants have large families of plasma membrane localized receptors that can sense extracellular signals and initiate appropriate cytoplasmic responses. The csp22 peptide derived from bacterial cold shock protein (CSP) has been known as an immune elicitor for more than a decade, but the corresponding receptor has not been identified. Discovered more than a quarter-century ago as the first plant peptide hormone, systemin was shown to be critical for systemic wound response and anti-herbivore defense in tomato. The receptor for this peptide hormone also remains elusive, since the previously proposed receptor SR160 is a tomato homolog of the brassinosteroid receptor BRI1 and its role as systemin receptor could not be corroborated in later work. Our work started with the observation that the wild tomato Solanum pennellii, in contrast to the cultivated tomato Solanum lycopersicum, lacks responsiveness to csp22 and systemin, indicating natural variation in perception of both peptides. By making use of well-defined introgression lines of these two species, we mapped the genes responsible for csp22 and systemin sensing to a common genomic region on chromosome 3. This region contains around two dozen genes encoding potential cell surface receptors. Functional analysis of these individual receptor candidate genes expressed in leaves of young N. benthamiana plants revealed one leucine-rich repeat-receptor kinase (LRR-RK) that strongly enhanced responsiveness to csp22, which we named cold shock protein receptor (CORE), and two other closely related LRR-RKs that conferred sensitivity to systemin, which we named systemin receptor 1 and 2 (SYR1, SYR2). CORE and SYR1 showed high affinity and specificity for their respective ligands in receptor binding assays. They also proved functional when heterologously expressed in Arabidopsis cells. Furthermore, ectopic expression of CORE can confer Arabidopsis increased resistance to the bacterial pathogen Pseudomonas syringae pv. tomato DC3000. Presence of SYR1, while not decisive for local and systemic wound responses as previously reported, is important for defense against insect herbivory in tomato plants.