Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicon) plant-to-plant communication

Tomato plants respond to herbivory by emitting volatile organic compounds (VOCs), which are released into the surrounding atmosphere. We analyzed the tomato herbivore-induced VOCs and tested the ability of tomato receiver plants to detect tomato donor volatiles by analyzing early responses, including plasma membrane potential (Vm) variations and cytosolic calcium ([Ca2+]cyt) fluxes. Receiver tomato plants responded within seconds to herbivore-induced VOCs with a strong Vm depolarization, which was only partly recovered by fluxing receiver plants with clean air. Among emitted volatiles, we identified by GC–MS some green leaf volatiles (GLVs) such as (E)-2-hexenal, (Z)-3-hexenal, (Z)-3-hexenyl acetate, the monoterpene α-pinene, and the sesquiterpene β-caryophyllene. GLVs were found to exert the stronger Vm depolarization, when compared to α-pinene and β-caryophyllene. Furthermore, Vm depolarization was found to increase with increasing GLVs concentration. GLVs were also found to induce a strong [Ca2+]cyt increase, particularly when (Z)-3-hexenyl acetate was tested both in solution and with a gas. On the other hand, α-pinene and β-caryophyllene, which also induced a significant Vm depolarization with respect to controls, did not exert any significant effect on [Ca2+]cyt homeostasis. Our results show for the first time that plant perception of volatile cues (especially GLVs) from the surrounding environment is mediated by early events, occurring within seconds and involving the alteration of the plasma membrane potential and the [Ca2+]cyt flux.

Graphical abstractHerbivore-induced volatiles from donor tomato plants are perceived by receiving tomato plants through plasma membrane depolarization and increasing cytosolic calcium fluxes. Green leaf volatiles exert higher inducing activity than mono- and sesquiterpenes.Figure optionsDownload full-size imageDownload as PowerPoint slideHighlights► Herbivore-wounded tomato plants emit volatile organic compounds (VOCs). ► Receiver tomato plants react to donor VOCs by plasma membrane (Vm) depolarization. ► Vm depolarization is associated with Ca2+ signaling. ► Green leaf volatiles induce more Vm depolarization and Ca2+ signaling than terpenoids. ► Tomato plant-to-plant communication occurs through VOCs perception.