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Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells

Scherzer, Sönke; Shabala, Lana; Hedrich, Benjamin; Fromm, Jörg; Bauer, Hubert; Munz, Eberhard; Jakob, Peter; Al-Rascheid, Khaled A. S.; Kreuzer, Ines; Becker, Dirk; Eiblmeier, Monika; Rennenberg, Heinz; Shabala, Sergey; Bennett, Malcolm J.; Neher, Erwin; Hedrich, Rainer

Authors

Sönke Scherzer

Lana Shabala

Benjamin Hedrich

Jörg Fromm

Hubert Bauer

Eberhard Munz

Peter Jakob

Khaled A. S. Al-Rascheid

Ines Kreuzer

Dirk Becker

Monika Eiblmeier

Heinz Rennenberg

Sergey Shabala

Erwin Neher

Rainer Hedrich



Abstract

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.

Journal Article Type Article
Journal Proceedings of the National Academy of Sciences
Electronic ISSN 1091-6490
Publisher National Academy of Sciences
Peer Reviewed Peer Reviewed
Volume 114
Issue 18
APA6 Citation Scherzer, S., Shabala, L., Hedrich, B., Fromm, J., Bauer, H., Munz, E., …Hedrich, R. (in press). Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells. Proceedings of the National Academy of Sciences, 114(18), doi:10.1073/pnas.1701860114
DOI https://doi.org/10.1073/pnas.1701860114
Keywords Amperometry, Exocytosis, Dionaea muscipula, Secretion, Plant digestion
Publisher URL http://www.pnas.org/content/114/18/4822
Copyright Statement Copyright information regarding this work can be found at the following address: http://eprints.nottingh.../end_user_agreement.pdf

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Copyright Statement
Copyright information regarding this work can be found at the following address: http://eprints.nottingham.ac.uk/end_user_agreement.pdf


Research Report scherzer 2017 Suppl information.pdf (421 Kb)
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Copyright Statement
Copyright information regarding this work can be found at the following address: http://eprints.nottingham.ac.uk/end_user_agreement.pdf





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