Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells
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-...
| Main Authors: | , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Published: |
National Academy of Sciences
2017
|
| Subjects: | |
| Online Access: | https://eprints.nottingham.ac.uk/43757/ |
| _version_ | 1848796761643024384 |
|---|---|
| author | 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 |
| author_facet | 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 |
| author_sort | Scherzer, Sönke |
| building | Nottingham Research Data Repository |
| collection | Online Access |
| description | 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. |
| first_indexed | 2025-11-14T19:53:07Z |
| format | Article |
| id | nottingham-43757 |
| institution | University of Nottingham Malaysia Campus |
| institution_category | Local University |
| last_indexed | 2025-11-14T19:53:07Z |
| publishDate | 2017 |
| publisher | National Academy of Sciences |
| recordtype | eprints |
| repository_type | Digital Repository |
| spelling | nottingham-437572020-05-04T18:43:53Z https://eprints.nottingham.ac.uk/43757/ 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 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. National Academy of Sciences 2017-05-02 Article PeerReviewed 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 and Hedrich, Rainer (2017) Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells. Proceedings of the National Academy of Sciences, 114 (18). pp. 4822-4827. ISSN 1091-6490 Amperometry Exocytosis Dionaea muscipula Secretion Plant digestion http://www.pnas.org/content/114/18/4822 doi:10.1073/pnas.1701860114 doi:10.1073/pnas.1701860114 |
| spellingShingle | Amperometry Exocytosis Dionaea muscipula Secretion Plant digestion 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 Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells |
| title | Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells |
| title_full | Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells |
| title_fullStr | Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells |
| title_full_unstemmed | Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells |
| title_short | Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells |
| title_sort | insect haptoelectrical stimulation of venus flytrap triggers exocytosis in gland cells |
| topic | Amperometry Exocytosis Dionaea muscipula Secretion Plant digestion |
| url | https://eprints.nottingham.ac.uk/43757/ https://eprints.nottingham.ac.uk/43757/ https://eprints.nottingham.ac.uk/43757/ |