The Venus Flytrap Dionaea muscipula Counts Prey-Induced Action Potentials to Induce Sodium Uptake

Abstract

SummaryCarnivorous plants, such as the Venus flytrap (Dionaea muscipula), depend on an animal diet when grown in nutrient-poor soils. When an insect visits the trap and tilts the mechanosensors on the inner surface, action potentials (APs) are fired. After a moving object elicits two APs, the trap snaps shut, encaging the victim. Panicking preys repeatedly touch the trigger hairs over the subsequent hours, leading to a hermetically closed trap, which via the gland-based endocrine system is flooded by a prey-decomposing acidic enzyme cocktail. Here, we asked the question as to how many times trigger hairs have to be stimulated (e.g., now many APs are required) for the flytrap to recognize an encaged object as potential food, thus making it worthwhile activating the glands. By applying a series of trigger-hair stimulations, we found that the touch hormone jasmonic acid (JA) signaling pathway is activated after the second stimulus, while more than three APs are required to trigger an expression of genes encoding prey-degrading hydrolases, and that this expression is proportional to the number of mechanical stimulations. A decomposing animal contains a sodium load, and we have found that these sodium ions enter the capture organ via glands. We identified a flytrap sodium channel DmHKT1 as responsible for this sodium acquisition, with the number of transcripts expressed being dependent on the number of mechano-electric stimulations. Hence, the number of APs a victim triggers while trying to break out of the trap identifies the moving prey as a struggling Na+-rich animal and nutrition for the plant.Video Abstract

Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells

“…Upon haptoelectric trap activation, the surface area of the multicellular gland cell complex increases by 30% and an acidic protein moiety is released into the green stomach formed by the hermetically sealed lobes of the trap (3,(5)(6)(7)13). In search of the membrane reservoir responsible for the surface increase of stimulated glands, we exposed traps to the JA-Ile mimic COR.…”

“…Dionaea secretion is directly coupled to acidification; H + and chloride, Cl − , are released into the digestive fluid of the tightly sealed trap (15). To test whether touch stimulation of the flytrap's trigger hairs is translated into ion fluxes across the gland plasma membrane, we used Ca 2+ -, Cl − -, and H + -sensitive microelectrode ion flux measuring (MIFE) microelectrodes (3,16), which measure fluxes by recording local concentration gradients. After five to 10 consecutive trigger-hair stimulations and a lag time of about 10 min, a rapid shift in the net ion fluxes toward net Ca 2+ uptake into the gland cells was observed ( Fig.…”

“…Growing on mineral-deficient soils, the carnivorous Venus flytrap (Dionaea muscipula) lures, captures, and digests small arthropods (3)(4)(5)(6)(7)(8) to feed on the nutrients extracted from their flesh (9)(10)(11)(12). Closure of the bilobed snap trap is initiated by mechanical stimulation of trigger hairs located at the inner trap surface.…”

“…If a second one fires within 20 s, it triggers rapid trap closure. In case an insect is trapped and struggles to escape, two and more haptoelectric stimuli activate jasmonate (JA) signaling and biosynthesis (3,6,7). From the fifth strike on, glands raise their expression levels of hydrolase and nutrient transporter genes.…”

“…When mechanostimulation is replaced by application of coronatine (COR), a mimic of the biologically active JA hormone JA-Ile, it can substitute for the mechanoelectric stimulation of the flytrap (7). Haptoelectric signaling and touch hormone activation turn the closed trap into a "green stomach," flooding the entrapped prey with an acidic digestive fluid (3,6,13). Although prey capture and consumption of the Venus flytrap has been known since Darwin's time (2), the molecular mechanisms of fluid phase secretion underlying animal consumption have remained unknown (14).…”