Contributed by Erwin Neher, March 17, 2017 (sent for review February 2, 2017; reviewed by R. Mark Wightman and Viktor Zarsky)
The Venus flytrap has been in the focus of scientists since Darwin’s time. Carnivorous plants, with their specialized lifestyle, including insect capture, as well as digestion and absorption of prey, developed unique tools to gain scarce nutrients. In this study, we describe mechanistic insights into the cascade of events following the capture of insect prey. Action potentials evoked by the struggling prey are translated into touch-inducible hormone signals that promote the formation of secretory vesicles. Different varieties of digestive compounds are released sequentially into the flytrap’s “green stomach” and break down the captured animal. Amperometry provides insight into the kinetics and chemistry of the stimulus-coupled glandular secretion process.
The Venus flytrap Dionaea muscipula captures insects and consumes their flesh. Prey contacting touch-sensitive hairs trigger traveling electrical waves. These action potentials (APs) cause rapid closure of the trap and activate secretory functions of glands, which cover its inner surface. Such prey-induced haptoelectric stimulation activates the touch hormone jasmonate (JA) signaling pathway, which initiates secretion of an acidic hydrolase mixture to decompose the victim and acquire the animal nutrients. Although postulated since Darwin’s pioneering studies, these secretory events have not been recorded so far. Using advanced analytical and imaging techniques, such as vibrating ion-selective electrodes, carbon fiber amperometry, and magnetic resonance imaging, we monitored stimulus-coupled glandular secretion into the flytrap. Trigger-hair bending or direct application of JA caused a quantal release of oxidizable material from gland cells monitored as distinct amperometric spikes. Spikes reminiscent of exocytotic events in secretory animal cells progressively increased in frequency, reaching steady state 1 d after stimulation. Our data indicate that trigger-hair mechanical stimulation evokes APs. Gland cells translate APs into touch-inducible JA signaling that promotes the formation of secretory vesicles. Early vesicles loaded with H+ and Cl− fuse with the plasma membrane, hyperacidifying the “green stomach”-like digestive organ, whereas subsequent ones carry hydrolases and nutrient transporters, together with a glutathione redox moiety, which is likely to act as the major detected compound in amperometry. Hence, when glands perceive the haptoelectrical stimulation, secretory vesicles are tailored to be released in a sequence that optimizes digestion of the captured animal.
↵1Present address: Medical University of Graz, 8010 Graz, Austria.
Author contributions: S. Scherzer, P.J., K.A.S.A.-R., I.K., D.B., H.R., S. Shabala, M.B., E.N., and R.H. designed research; S. Scherzer, L.S., B.H., J.F., H.B., E.M., I.K., M.E., and S. Shabala performed research; S. Scherzer, P.J., K.A.S.A.-R., I.K., D.B., H.R., M.B., E.N., and R.H. contributed new reagents/analytic tools; S. Scherzer, L.S., E.M., P.J., I.K., D.B., H.R., S. Shabala, and E.N. analyzed data; and S. Scherzer, K.A.S.A.-R., I.K., D.B., S. Shabala, M.B., E.N., and R.H. wrote the paper.
Reviewers: R.M.W., University of North Carolina at Chapel Hill; and V.Z., Charles University and Czech Academy of Sciences.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1701860114/-/DCSupplemental.
