Stretch-activated ion channels identified in the touch-sensitive structures of carnivorous Droseraceae plants

Abstract

In response to touch, some carnivorous plants such as the Venus flytrap have evolved spectacular movements to capture animals for nutrient acquisition. However, the molecules that confer this sensitivity remain unknown. We used comparative transcriptomics to show that expression of three genes encoding homologs of the MscS-Like (MSL) and OSCA/TMEM63 family of mechanosensitive ion channels are localized to touch-sensitive trigger hairs of Venus flytrap. We focus here on the candidate with the most enriched expression in trigger hairs, the MSL homolog FLYCATCHER1 (FLYC1). We show that FLYC1 transcripts are localized to mechanosensory cells within the trigger hair, transfecting FLYC1 induces chloride-permeable stretch-activated currents in naïve cells, and transcripts coding for FLYC1 homologs are expressed in touch-sensing cells of Cape sundew, a related carnivorous plant of the Droseraceae family. Our data suggest that the mechanism of prey recognition in carnivorous Droseraceae evolved by co-opting ancestral mechanosensitive ion channels to sense touch.

Structural Insights into the Venus flytrap Mechanosensitive Ion Channel Flycatcher1

“…During MD simulation we also observed Na + ions (one in each ~100 ns simulation) entering the cytoplasmic cage via the central pore, but a complete exit through the side portals were not observed at this timescale. The ratio of Clto Na + crossing events is broadly consistent with our previous reported PCl/PNa value of 9.8 ± 1.8 calculated on the basis of reversal potential in asymmetrical NaCl solution 9 .…”

“…However, the molecular basis is most likely different; introduction of V320 in AtMSL1 is expected to disturb packing of the pore helix (TM5) 27 , whereas R334E in FLYC1 disrupts a conformation-specific interaction between cytoplasmic domains. The R334E mutation does not alter inactivation kinetics and remains a non-inactivating channel like WT FLYC1 9 (Fig. 4d).…”

“…Our MD simulations support the idea of passage of chloride in an 'all-up' state. However, electrophysiology recordings suggest that although FLYC1 favors chloride flux, it is also permeable to sodium ions 9 , which, when fully hydrated, are larger than hydrated chloride 43 . We did not observe any complete Na + permeation events in our simulations at this timescale, suggesting that our structure of FLYC1 does not represent a fully open conformation.…”

“…Deflection of sensory trigger hairs in the trap results in an action potential [5][6][7] , and two action potentials within a short period of time is sufficient for trap closure 8 . Recently, two independent studies have proposed that the gene Flycatcher1 (FLYC1) is one of the candidates involved in Venus flytrap touch sensation, based on 85-fold enrichment of the transcript in sensory trigger hairs relative to trap tissue 9,10 . FLYC1 selectively localizes to mechanosensory cells in trigger hairs, and overexpression of FLYC1 in mechanically insensitive HEK cells results in robust stretch activated chloride permeable currents, suggesting that FLYC1 encodes a MS ion channel 9 .…”

“…FLYC1 selectively localizes to mechanosensory cells in trigger hairs, and overexpression of FLYC1 in mechanically insensitive HEK cells results in robust stretch activated chloride permeable currents, suggesting that FLYC1 encodes a MS ion channel 9 . Furthermore, two FLYC1 homologs have highly enriched transcripts in the sensory tentacle of a different carnivorous plant within the Droseraceae family, Drosera capensis (Cape sundew) 9 . Therefore, FLYC1 channel homologs may have a general role in touch-induced prey recognition in carnivorous plants.…”