The systemin receptor SYR1 enhances resistance of tomato against herbivorous insects

Abstract

The discovery in tomato of systemin, the first plant peptide hormone, was a fundamental change for the concept of plant hormones. Numerous other peptides have since been shown to play regulatory roles in many aspects of the plant life, including growth, development, fertilization and interactions with symbiotic organisms. Systemin, an 18 amino acid peptide derived from a larger precursor protein , was proposed to act as the spreading signal that triggers systemic defence responses observed in plants after wounding or attack by herbivores. Further work culminated in the identification of a leucine-rich repeat receptor kinase (LRR-RK) as the systemin receptor 160 (SR160). SR160 is a tomato homologue of Brassinosteroid Insensitive 1 (BRI1), which mediates the regulation of growth and development in response to the steroid hormone brassinolide. However, a role of SR160/BRI1 as systemin receptor could not be corroborated by others. Here, we demonstrate that perception of systemin depends on a pair of distinct LRR-RKs termed SYR1 and SYR2. SYR1 acts as a genuine systemin receptor that binds systemin with high affinity and specificity. Further, we show that presence of SYR1, although not decisive for local and systemic wound responses, is important for defence against insect herbivory.

Regulation of plant peptide hormones and growth factors by post‐translational modification

“…Although these LRR‐RLKs appeared to be dispensable for systemic wound responses, their contribution to insect resistance in tomato was confirmed (Wang et al . ).…”

The systemin signaling cascade as derived from phosphorylation time courses under stimulation by systemin and its inactive Thr17Ala (A17) analog

“…The recently identified plasma membrane located LRR-RLK receptors for the systemin peptide (16) were not identified among the 3312 phosphopeptides from this work, while several other receptor kinases, among them also the phytosulfokine receptor PSKR2 (Solyc07g063000) or FERONIA (Solyc09g015830) were quantified in our experiments. There could be several reasons for missing these proteins in the phosphopeptide analysis: Firstly, a shotgun type phosphoproteome analysis was carried out depending on sufficient quantity and quality (peptide length, amino acid composition) of identified (phospho)peptides.…”

“…Consistent with this proposition, binding to the putative receptor was shown to rely on the N-terminus of systemin, while the C-terminus, including Thr17, is required for activation (10). The receptor was recently identified as SYR1, and A17 was confirmed as a competitive systemin antagonist (16). By comparing phosphoproteomic responses triggered by A17 and by systemin, the data set can be filtered for systemin-specific phosphorylation changes.…”

“…The aim of our work was to (i) identify early events induced by systemin and (ii) identify kinases and phosphatases involved in these signaling events. The maturation of the signaling peptide systemin is beginning to be understood (9), and the primary receptor of systemin was recently identified (16). While individual early responses to systemin perception, such as an increase in cytosolic calcium (17), ROS production (16,58), the modulation of the H + -ATPase activity (19), or the activation of MAPkinase signaling (52) have been identified, the proteome-wide effects of systemin treatment were not yet studied.…”

“…Purification and characterization of the binding protein tentatively placed the receptor into the family of leucin-rich repeat receptor-like kinases (LRR-RLKs), but the protein initially declared as the systemin receptor later turned out to be the tomato ortholog of BRI1, the brassinosteroid receptor in Arabidopsis (12)(13)(14)(15). Recent work identified the systemin receptor as SYR1, a LRR-RLK closely related to known pattern recognition receptors (16). The early cellular responses to systemin do in fact resemble those typically triggered by microbe-associated molecular patterns (MAMPs) including an increase in cytosolic calcium, extracellular alkalization, plasma membrane depolarization, an oxidative burst, and ethylene production (17)(18)(19).…”