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

Erik Procko,Adam Coombs,Swetha Murthy,Seyed Ali Reza Mousavi,Joanne Chory,William T Keenan,Carl Procko,Lisa Baird,Ardem Patapoutian,Tsegaye Dabi

doi:10.7554/elife.64250

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.

Highlights

How organisms evolve new forms and functions is a question of major interest
This is larger than the approximately 21,000 genes previously predicted by genome sequencing (Palfalvi et al, 2020), reflecting the presence of multiple isoforms in our transcriptome, possible heterozygosity and strain differences, and/or differences in genome/transcriptome completeness, indicated by Benchmarking Universal Single-Copy Orthologs (BUSCO) analysis
Based on homology to Arabidopsis, many genes preferentially expressed in leaf traps were associated with photosynthetic function, whereas those more highly expressed in the trigger hairs included transcription factors and genes that may affect cellular and organ structure (Supplementary file 1C and 1D)

Summary

Introduction

How organisms evolve new forms and functions is a question of major interest. For example, whereas most plants respond slowly to mechanical stimuli—such as touch, gravity, or changes in turgor pressure—by altering growth, some plants have evolved rapid touch-induced movements. The best known carnivorous plant, Dionaea muscipula (Venus flytrap) of the Droseraceae family, is one such plant that has evolved a remarkable and rapid touch response to facilitate prey capture (Video 1). How this predator evolved its complex leaf form and function for this purpose has long puzzled scientists; Charles Darwin proclaimed the species "one of the most wonderful [plants] in the world" (Darwin, 1875).

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