The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis

Abstract

The carnivorous sundew plant (Drosera capensis) captures prey using sticky tentacles. We investigated the tentacle and trap reactions in response to the electrical and jasmonate signalling evoked by different stimuli to reveal how carnivorous sundews recognize digestible captured prey in their traps. We measured the electrical signals, phytohormone concentration, enzyme activities and Chla fluorescence in response to mechanical stimulation, wounding or insect feeding in local and systemic traps. Seven new proteins in the digestive fluid were identified using mass spectrometry. Mechanical stimuli and live prey induced a fast, localized tentacle-bending reaction and enzyme secretion at the place of application. By contrast, repeated wounding induced a nonlocalized convulsive tentacle movement and enzyme secretion in local but also in distant systemic traps. These differences can be explained in terms of the electrical signal propagation and jasmonate accumulation, which also had a significant impact on the photosynthesis in the traps. The electrical signals generated in response to wounding could partially mimic a mechanical stimulation of struggling prey and might trigger a false alarm, confirming that the botanical carnivory and plant defence mechanisms are related. To trigger the full enzyme activity, the traps must detect chemical stimuli from the captured prey.

Triggering a false alarm: wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula)

“…(), who demonstrated a crucial role of electrical signalling in the initiation of defence responses at remote sites. In this and our previous study (Krausko et al ., ), we found a particularly close correlation between electrical signal propagation, jasmonate accumulation and enzyme secretion in carnivorous plants, confirming a general assumption of the importance of long‐distance electrical signalling in the systemic response of plants (Mousavi et al ., ). Based on the results from the sundew plant and the Venus flytrap, we can conclude that carnivory is always a local response, which seems reasonable; it would be quite expensive to produce digestive enzymes in all the traps on a plant that had not captured any prey.…”

“…The elevated concentration of cis ‐OPDA may provide a reservoir for JA synthesis (Koo et al ., ), but the signalling role of cis ‐OPDA in this phase of digestion cannot be excluded. The increased concentrations of JA and JA‐Ile during the first hours after prey capture also has been documented in carnivorous sundew plants (Mithöfer et al ., ; Krausko et al ., ).…”

“…In the Venus flytrap, wounding activates rapid trap closure, hermetic trap sealing and the secretion of digestive fluid containing enzymes; together these comprise a typical carnivorous response (Figs c,d, , ; Video S2). Recently, we found the same reaction in the Cape sundew ( Drosera capensis ) but also observed some differences (Krausko et al ., ). In response to wounding, sundew plants generate different electrical signals than those generated in response to mechanical stimulation.…”

“…(), there is good evidence that the APs of higher plants are a nonspecific bioelectric signal independent of stimulus origin, so they do not carry any stimulus‐specific information but signal the onset of adverse conditions in some region of the plant to resting tissues and organs. From the qualitative perspective, our results are consistent with this opinion, and even electrical signalling in the sundew plant, which generates different electrical signals in response to wounding and touch, triggers the same response of tentacle bending and enzyme secretion (Krausko et al ., ). However, from the quantitative perspective, the number of APs is important for regulating the strength of the response in carnivorous plants.…”

“…() and Krausko et al . (), who found the accumulation of jasmonates spatially restricted to the bending segment of the sundew trap with captured prey and that only this segment generates electrical signals and digestive enzymes. Our results agree with those of Mousavi et al .…”