Schadenfreude: Tomatoes (Solanum lycopersicum) eavesdrop on the misfortune of neighbors to prepare for herbivore attack

Recent efforts in biological control have explored using the attractive qualities of herbivore-induced plant volatiles (HIPVs) to draw natural enemies to protect crops throughout the field. These HIPVs also function in interplant communication whereby plants ‘eavesdrop’ on volatiles released by their herbivore-infested neighbors and exploit this cue as an early warning system to induce defenses in anticipation of attack.  It is thought this may occur by inducing defenses directly, or by priming plant defense such that the plant responds much more strongly and quickly to subsequent damage.  To further understand the mechanisms underlying HIPV-mediated plant communication, we studied the defenses of tomatoes (Solanum lycopersicum) exposed to the HIPV methyl salicylate (MeSA).  We predicted that MeSA-primed S. lycopersicum would induce stronger and faster defenses to herbivores upon attack compared with naïve plants.  To test this hypothesis, we assessed the interactive effects of HIPV exposure and Manduca sexta herbivory in the following treatments: (1) naïve control; (2) MeSA exposure; (3) M. sexta damage; and (4) MeSA exposure and subsequent M. sexta damage.  We measured the plants’ responses to these treatments by measuring increases in polyphenol oxidase and proteinase inhibitor levels, released volatile organic compounds, mRNA expression of key defense genes, and M. sexta performance.  When damaged, tomatoes released higher levels of the volatiles β-phellandrene, caryophyllene, and MeSA.  Defense levels were found to be higher in plants exposed to HIPVs before attack.