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 additionally evolved rapid touch-induced movements. These movements can be used to deter herbivory, as is seen with the sensitive plant (Mimosa pudica), or to physically capture and digest mobile animals, as occurs in carnivorous plants (Chehab et al., 2008). 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; indeed, Charles Darwin proclaimed the species "one of the most wonderful [plants] in the world" (Darwin, 1875).

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Several groups have described the events that evoke trap closure in Venus flytrap in detail. The plant leaf consists of an open bilobed trap, to which animal prey are attracted by volatile secretions (Kreuzwieser et al., 2015; Lloyd, 1942). There, the animal comes into contact with one of three to four mechanosensory trigger hairs on each lobe. Bending of any one trigger hair generates an action potential in sensory cells at the base of the trigger hair that propagates through the trap (Benolken and Jacobson, 1970; Burdon-Sanderson, 1873) and is correlated with an increase in cytosolic calcium in leaf trap cells (Suda et al., 2020). Two action potentials (or two touches) in a short period are required to likely further increase cytosolic calcium levels above a necessary threshold to initiate rapid closure of the trap, which ensnares the prey (Brown and Sharp, 1910; Suda et al., 2020). Trap closure occurs in as little as 100 ms, representing one of the fastest movements in the plant kingdom (Forterre et al., 2005). These electromotive properties were first described in the 1870s (Burdon-Sanderson, 1873); however, almost a century and a half later, the molecular underpinnings of these events remain elusive.

Early recordings from Venus flytrap trigger hairs suggest that, based on the time scale of action potential generation, mechanosensitive ion channels may play a role in transducing force into electrical signals (Benolken and Jacobson, 1970; Jacobson, 1965). To identify possible ion channels required for the touch response in Venus flytrap, we sought to find genes that are preferentially expressed in trigger hairs.

The Venus flytrap genome is very large (Palfalvi et al., 2020)—approximately 20× the size of that of the commonly studied model plant Arabidopsis thaliana (Figure 1—source data 1)—and lacks available inbred strains. Therefore, we established a clonal propagation system for the collection of genetically identical material (Figure 1A,B, and Figure 1—figure supplement 1). Using these clones, we generated a de novo transcriptome representing genes expressed in trap tissue from Illumina-based short sequencing reads. The transcriptome of our clonal strain consists of almost 28,000 unique transcripts with open reading frames coding for predicted proteins of at least 100 amino acids. 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 BUSCO analysis (see Materials and Methods). When we compared the transcriptome of trigger hairs with that of only the leaf traps, 495 protein-coding genes were differentially enriched by greater than twofold in the trigger hair, whereas 1844 were similarly enriched in the trap (Supplementary file 1A and 1B). 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).

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Figure 1—source data 1

Size estimates of two Arabidopsis (Col-0) samples compared to our Venus flytrap strain (CP01).

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Figure 1—source data 2

Summary of sequencing reads used to build the de novo transcriptome (NCBI Transcriptome Shotgun Assembly Sequence Database accession # GHJF00000000).

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To find potential mechanosensitive ion channels, we screened our trigger hair-enriched transcriptome for transcripts coding for likely multi-pass transmembrane proteins. Of 45 such transcripts, three coded for possible candidates based on homology to Arabidopsis proteins. Two of these shared homology to MSL family proteins (transcript IDs comp20014_c0_seq1 and comp28902_c0_seq1), and one to the OSCA family (comp16046_c0_seq1) (Haswell and Meyerowitz, 2006; Murthy et al., 2018). We call these genes FLYCATCHER1 and FLYCATCHER2 (FLYC1 and FLYC2) and DmOSCA, respectively. We did not observe enriched expression of homologs to the mechanically activated PIEZO channels. Strikingly, one of these MSL-related transcripts, FLYC1, was expressed 85-fold higher in trigger hairs than in trap tissue (Figure 1C,D), and was the second highest enriched gene (a putative terpene synthase was 176-fold enriched; see Materials and Methods). By contrast, the other two putative ion channels were less than sevenfold differentially expressed.

Using a similar approach, Iosip et al., 2020 recently described 495 genes as trigger hair-specific. These genes were enriched in the trigger hair relative to six other tissue types: root, flower, petiole, trap, rim, and gland tissues. Remarkably, this approach identified FLYC1/DmMSL10 (transcript Dm_00009130-RA) as the most trigger hair-specific of all genes. FLYC2 (transcript Dm_00001246-RA) and DmOSCA (3' end of transcript Dm_00001755-RA) were not identified as trigger hair-specific using this analysis; however, both transcripts were enriched over twofold in trigger hairs when compared to other leaf tissues (trap, petiole, rim, and glands). Expression of these genes in root and/or flower tissue might suggest that they have additional functions in other organs (Iosip et al., 2020). Together, these findings are consistent with our own, and support the possibility that all three genes might play a role in trigger hair touch sensation.

To validate our transcriptome, we verified the FLYC1 transcript sequence from cDNA. In addition, we used Sanger sequencing of PCR products generated from genomic DNA template to assemble the complete gene sequence. Thirty-two single nucleotide polymorphisms (SNPs) were detected between the two FLYC1 alleles of our clonal strain, of which only two were found in the coding region and were both silent (Figure 1—figure supplement 2). To further assess the natural variation that may exist, we sequenced the FLYC1 gene from a morphologically dissimilar cultivar, and found additional SNPs and short sequence variations. Of these, eight SNPs were located in exons, two of which caused amino acid changes (Figure 1—figure supplements 2 and 3). No additional SNPs were found in a coding sequence reported by others (Iosip et al., 2020; Palfalvi et al., 2020). The scarcity of SNPs causing amino acid changes when compared to the abundance of SNPs in introns is likely indicative of selection for the protein product.

FLYC1 and FLYC2 code for predicted proteins of 752 and 897 amino acids, respectively, with homology to Arabidopsis MSL10 and MSL5 (Figure 2A). Ten MSL (MscS-like) proteins have been identified in Arabidopsis based on their similarity to the bacterial mechanosensitive channel of small conductance, MscS (Haswell and Meyerowitz, 2006). In Escherichia coli, MscS opens to allow ion release upon osmotic down-shock and cell swelling, thereby preventing cell rupture (Booth and Blount, 2012; Levina et al., 1999). In Arabidopsis, MSL8 functions in pollen rehydration, whereas the roles of the remaining MSLs in mechanosensory physiological processes is unclear (Hamilton et al., 2015). Notably, MSL10 forms a functional mechanosensitive ion channel with slight preference for chloride when heterologously expressed in Xenopus laevis oocytes (Maksaev and Haswell, 2012). Furthermore, along with other members of the MSL family, MSL10 accounts for stretch-activated currents recorded from root protoplasts (Haswell et al., 2008). Whereas FLYC1 and FLYC2 are 38.8% identical (Figure 2—figure supplement 1), they share 47.5 and 35.5% identity with MSL10, respectively, with most variation in the cytoplasmic N-terminus. Compared to MscS, FLYC1 and FLYC2 have three additional predicted transmembrane helices, six in total, with the C-terminus of the proteins sharing highest homology (Figure 2B,C).

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DmOSCA encodes a predicted 754-amino acid protein with highest homology to Arabidopsis OSCA1.5 (64% identity), which belongs to a 15-member family of OSCA proteins in Arabidopsis (Figure 2D,E). Although initial identification characterized the OSCA family as hyperosmolarity-activated calcium channels, it has been demonstrated that several members of the OSCA family are mechanosensitive ion channels that are non-selective for cations with some chloride permeability (Murthy et al., 2018; Yuan et al., 2014). Fly and mammalian orthologues, Tmem63, also encode mechanosensitive ion channels, suggesting that the molecular function of the OSCA genes is conserved. Furthermore, purification and reconstitution of AtOSCA1.2 in proteoliposomes induce stretch-activated currents, indicating that these proteins are inherently mechanosensitive (Murthy et al., 2018). Notably, mutant OSCA1.1 plants have stunted leaf and root growth when exposed to hyperosmotic stress (Yuan et al., 2014), possibly as a consequence of impaired mechanotransduction in response to changes in cell size. This suggests an ancestral role for these channels as osmosensors, similar to the MSL family.

We sought to find which cells in the trigger hair express FLYC1, FLYC2, and DmOSCA. The trigger hair can be divided into two main regions: a cutinized lever and a podium on which the lever sits (Figure 1B). An indentation zone at the top of the podium separates the two regions (Figure 3A,C), and is where most flexure of the trigger hair occurs (Lloyd, 1942). Electrophysiological recordings have demonstrated that mechanical stimulation of the trigger hair generates action potentials from a single layer of sensory cells at this indentation zone, and not from other cells of the podium or lever (Benolken and Jacobson, 1970). Remarkably, by fluorescent in situ hybridization, we detected FLYC1 transcript specifically in indentation zone sensory cells (Figure 3B,D). No transcript was observed in cells of the lever or lower podium (Figure 3B,E). In contrast, EF1α transcript, a housekeeping gene, was detected throughout the trigger hair and trap (Figure 3—figure supplement 1). FLYC1-sense probes produced no signal above background (Figure 3B). Using similar in situ hybridization methods, we were unable to detect FLYC2 transcripts, whereas DmOSCA was found at high levels within trigger hair sensory cells, but also low levels in other cell types (Figure 3—figure supplement 2). These results are consistent with our RNA-seq findings from whole trigger hairs, where FLYC2 and DmOSCA were less enriched over background trap tissue compared to FLYC1, and in the case of FLYC2 only weakly expressed (Figure 1D). Regardless, the expression profile of FLYC1 and DmOSCA is consistent with them being at the site of touch-induced initiation of action potentials.

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To test whether FLYC1, FLYC2, and DmOSCA were indeed mechanically activated ion channels and could confer mechanosensitivity to naïve cells, we expressed human codon-optimized sequences of these genes in mechanically insensitive HEK-P1KO cells (Dubin et al., 2017). Robust stretch-activated currents were recorded from FLYC1-expressing cells when negative pressure was applied to the recording pipette in the cell-attached patch configuration (Figure 4, A), but not from FLYC2-, or DmOSCA-expressing cells (Figure 4—figure supplement 1). Notably, overexpression of human codon-optimized MSL10 and of OSCA1.5 subcloned from A. thaliana also failed to produce stretch-activated currents in our system (Figure 4—figure supplement 1). However, previous studies have shown that expression of MSL10 in oocytes does elicit stretch-activated currents, suggesting that trafficking of these plant proteins is largely compromised in mammalian cells (Maksaev and Haswell, 2012). Given the high transcript enrichment, localization in sensory cells, and mechanosensitivity, we focused on FLYC1 as a likely functional mechanosensor in Venus flytrap sensory hairs.

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Further characterization of the FLYC1 channel in cell-attached patch clamp mode indicated that the pressure required for half-maximal activation (P₅₀) of FLYC1 was 77.3 ± 4.0 mmHg (N = 9) (Figure 4B and Figure 4—figure supplement 2A). The channel has a conductance of 164 ± 9 pS (N = 6) in physiological recording solution (Figure 4C), and upon removal of the stretch stimulus, the currents decay with a time constant of 167 ± 34 ms (N = 5). In land plants and green algae, chloride-permeable channel opening is associated with membrane depolarization, due to the efflux of chloride ions down their electrochemical gradient (Beilby, 2007; Hedrich, 2012). Therefore, we tested whether FLYC1 is permeable to chloride by recording stretch-activated FLYC1 currents from inside-out excised patches in symmetrical versus asymmetrical NaCl solution. In symmetrical 150 mM NaCl, FLYC1 stretch-activated single-channel currents reversed at +2.9 ± 1.0 mV (N = 8), whereas in intracellular 30 mM NaCl and extracellular 150 mM NaCl asymmetrical solutions, FLYC1 currents reversed at −30 ± 1.5 mV (N = 7). This reversal potential is closer to the theoretical reversal potential of −37.8 mV for chloride ion than of +37.8 mV for sodium ion, derived from the Nernst equation under our experimental conditions. Therefore, FLYC1 exhibited a preference for chloride over sodium with a P_Cl/P_Na ratio of 9.8 ± 1.8 (N = 7), as measured using the Goldman–Hodgkin–Katz equation (Figure 4D). These results are further supported by the lack of inward chloride currents at positive potential when stretch-activated currents were recorded in calcium-gluconate containing extracellular solution in the cell-attached patch clamp mode (Figure 4—figure supplement 2B). Finally, from our excised inside-out patches in symmetrical 150 mM NaCl the single-channel conductance of FLYC1 was 276 ± 10 pS (N = 9), calculated as the slope of the I–V curve between −80 and 0 mV (Figure 4D).

Bacterial MscS are bona fide mechanically activated ion channels, with in-depth structural and molecular understanding of how they are gated by membrane tension (Booth and Blount, 2012). Much less is known about the structure and function of plant MSLs. Although homology modeling of MSL10 with MscS has hinted at certain residues that alter channel conductance, molecular determinants of selectivity and gating in MSL10 remain largely unknown (Maksaev and Haswell, 2013; Maksaev et al., 2018). Intrigued by the high sequence similarity in the C-terminus of MscS, MSL10, and FLYC1 proteins (Figure 4—figure supplement 3A), we asked to what extent the molecular architecture of the putative pore-lining helix is shared among these channels. Homology-modeling of FLYC1 with the known MscS structure (Bass et al., 2002) suggested that certain features of the pore-forming transmembrane domain (TM6) are indeed conserved. These include hydrophobic residues within the part of the helix that lines the pore (TM6a), and a glycine kink at G575 followed by an amphipathic helix (TM6b) that lies parallel to the inner plasma membrane surface (Figure 4—figure supplement 3B,C). Based on our result that FLYC1 has a higher preference to chloride, we tested whether the positively charged lysines on either side of the putative pore (K558 and K579) may confer pore properties. We substituted lysines at position 558 and 579 with glutamate and measured P_Cl/P_Na. Whereas selectivity for chloride in both mutants remained unchanged, the K579E mutant exhibited smaller single-channel currents at positive membrane potentials (Figure 4—figure supplement 3D), suggesting that K579 is indeed in the vicinity of the pore. This analysis confirms that the predicted TM6 of FLYC1 is part of the pore-lining region of the channel, consistent with mutagenesis results in MSL10 (Maksaev et al., 2018). These observations are further supported by the cryo-electron microscopy structure of AtMSL1, which indicates a similar architecture of the last TM of the channel (Deng et al., 2020). Future structural studies on FLYC1 will better resolve how selectivity is determined in these channels.

If FLYC1 is indeed important for touch-induced prey recognition, we reasoned that its expression and function in mechanosensory structures is likely to be conserved across carnivorous Droseraceae plants. To test this, we investigated the largest genus in the family, Drosera, which includes ~200 species of sundew (Poppinga et al., 2013). Sundews are characterized by touch-sensitive projections on their leaf surface called tentacles (Figure 5A; Darwin, 1875; Lloyd, 1942; Poppinga et al., 2013; Williams, 1976). These tentacles typically secrete a glob of sticky mucilage from their head, which acts as a trapping adhesive when contacted by insect prey. Movement by the adhered insect results in action potentials along the tentacle (Williams and Pickard, 1972), often accompanied by radial movement of the tentacle towards the leaf center (Darwin, 1875). This traps the struggling insect against even more mucilage-secreting tentacles, allowing for digestion to occur (Figure 5B and Video 2).

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We identified the expression of two FLYC1 homologs in Cape sundew (Drosera capensis) by quantitative reverse transcriptase (qRT)-PCR (Butts et al., 2016). Consistent with our findings from Venus flytrap, these two transcripts had 30- to 40-fold higher expression in tentacles compared to tentacle-less leaf tissue (Figure 5C). The cloned cDNAs of these two genes—which we call DcFLYC1.1 and DcFLYC1.2—code for almost identical predicted protein products with 96.4% identity. They share 66.2 and 65.6% identity to Venus flytrap FLYC1, respectively (Figure 2A).

Cape sundew tentacles display variation in length depending on their position on the leaf (Figure 5—figure supplement 1), but share a similar mechanosensory head structure, with two outer layers of secretory cells (Figure 5D; Lloyd, 1942; Williams and Pickard, 1972, Williams and Pickard, 1974). The outermost secretory cells have previously been hypothesized to also be the site of touch sensation (Lloyd, 1942). Not only are these cells directly exposed to the mucilage environment on which the insect prey adheres and pulls, but they display a unique morphology of outer cell wall buttresses and plasma membrane crenellations (Figure 5—figure supplement 2; Lloyd, 1942). In addition, cellulose fibrils extend from the outer cell wall into the cuticle in much the same way as they do in the Venus flytrap indentation zone (Sievers, 1968; Williams and Pickard, 1974). Strikingly, smFISH probes against DcFLYC1.1 and DcFLYC1.2 transcripts localized to the outer secretory cells, whereas no transcripts were observed in the leaf at the base of the tentacles (Figure 5E).

Heterologous expression of human codon-optimized DcFLYC1.1 and DcFLYC1.2 cDNA, independently or together in HEK-P1KO cells, did not result in stretch-activated currents (Figure 5—figure supplement 3). Similar to our findings with DmFLYC2 and DmOSCA, we speculate that the lack of activity could be due to incorrect folding and trafficking of these proteins. Nonetheless, our expression data is consistent with a conserved role for FLYC1 in two divergent species in carnivorous Droseraceae plants.

Here, we identify members of the FLYC and OSCA families of ion channels as candidate mechanosensors in rapid touch sensation in carnivorous plants. First, members of both families have enriched mRNA transcript expression in the sensory trigger hairs of Venus flytrap. Among these, FLYC1 is a prime candidate as its mRNA is massively enriched in the putative mechanosensory cells that initiate transduction of the touch-induced signal. Second, FLYC1 forms a mechanically activated ion channel with properties that would facilitate generation of action potentials in sensory cells. Third, expression of FLYC genes is remarkably conserved in two morphologically disparate touch-sensitive structures from different genera in the Droseraceae family. In addition to the three candidates presented here, our results do not exclude the possibility that other mechanosensitive proteins could also contribute to the events that enable touch-induced prey capture. In the future, knockout experiments will be critical to determine which candidate mechanosensor(s) identified here, if any, are absolutely necessary for functional prey detection and trap closure.

Using a mammalian cell-expression system, we detected robust macroscopic as well as single-channel stretch-activated currents in FLYC1-expressing cells and identified residues important for channel properties, which strongly suggests that FLYC1 form mechanosensitive ion channels. However, we were unable to detect currents from the other channels tested, including Arabidopsis MSL10, which has previously been shown to induce currents only in oocytes but not in mammalian cells. We hypothesize that these channels fail to fold and traffic correctly to the mammalian cell membrane, or, alternatively, that the activation threshold for these channels might be higher than that of DmFLYC1 (Venus flytrap), technically precluding us from recording reliable stretch-activated currents. Future functional studies on these genes in different non-mammalian expression systems and purification and reconstitution of proteins in lipid vesicles will conclusively determine whether these genes encode inherently mechanosensitive ion channels.

It is interesting to compare FLYC1 channel properties to its homologs, MSL10 and MscS. FLYC1 single-channel conductance is 164 ± 9 pS (in physiological pipette solution) in cell-attached patches and 276 ± 10 pS (in 150 mM NaCl) in excised inside-out patches from HEK-P1KO cells, whereas MSL10 and MscS channel conductance from oocytes is 103 ± 3 pS and 218 ± 2 pS, respectively (Maksaev and Haswell, 2011). FLYC1 and MSL10 stretch-activated currents have slow opening and closing kinetics with lack of inactivation in the presence of sustained pressure, unlike MscS (Maksaev and Haswell, 2011). The half-maximal activation (P₅₀77.3 ± 4.0 mmHg) for FLYC1 is two-fold lower than its bacterial orthologs MscS (P₅₀188 ± 31 mmHg; Akitake et al., 2005) and MscL (P₅₀147.3 ± 4.3 mmHg; Doerner et al., 2012). However, we observed that similar to MSL10 recordings in oocytes (Maksaev and Haswell, 2012), the cell membrane in our recordings often ruptured before current saturation (saturated open probability (Po) was measured in only 3/9 cells) resulting in our measurement of FLYC1 P₅₀ likely being an underestimation. Finally, P_Cl/P_Na ratio of FLYC1 (P_Cl/P_Na = 9.8) is higher than ratios obtained for MSL10 (P_Cl/P_Na = 5.9) and MscS (P_Cl/P_K = 1.2–3.0) (Cox et al., 2014; Maksaev and Haswell, 2012). In-depth functional and structural characterization of these channels (FLYC1, MSL10, and MscS) under similar expression systems and recording conditions will further determine absolute differences in their properties and the underlying molecular architecture that govern these properties.

Our characterization of FLYC1 as a chloride-permeable mechanically activated ion channel suggests a possible mechanism to elicit rapid touch-induced movements in Venus flytrap. Due to the high electronegativity of sensory cells (Benolken and Jacobson, 1970; Hodick and Sievers, 1988), combined with a concentration gradient that likely favors efflux (Higinbotham et al., 1967), a chloride-permeable channel like FLYC1 could contribute to membrane depolarization. This is consistent with the finding that increasing concentrations of extracellular chloride ions reduced or abolished the electrical response of Venus flytrap sensory cells to a mechanical stimulus (Jacobson, 1974). FLYC1-mediated depolarization, likely in combination with FLYC2 and OSCA, would then initiate action potentials that propagate into the leaf through plasmodesmata clustered on the basal side of the sensory cells (Williams and Mozingo, 1971), eliciting trap closure (Figure 6A). The role of a mechanosensitive calcium permeable ion channel, OSCA, is noteworthy here. Indeed, it has been described that trigger hair movement causes a rise in cytosolic calcium and that this signal propagates through the trap preceding its closure (Suda et al., 2020); however, the propagation signal most likely involves a mechanism independent of mechanotransduction. A similar chain of events would occur in the sundew tentacle: prey contact with the tentacle results in DcFLYC-induced action potentials, possibly in combination with OSCA or other mechanosensory proteins not identified here, that may propagate through plasmodesmata along the outer cell layers of the tentacle mechanosensory head and stalk, evoking tentacle bending (Figure 6B).

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A method for transformation of Venus flytrap has been recently reported (Suda et al., 2020). By generating targeted knockouts using this method, future studies may be able to address which or if all of these channels are required redundantly for touch responses in the plant. Nonetheless, our findings are consistent with FLYC1 being one of the bona fide sensors of touch in Darwin's ‘most wonderful’ plants, and shed new light on how carnivorous plants evolved to sense touch by co-opting ancestral, osmosensing mechanosensitive channels.

Raw and processed data for the Venus flytrap transcriptome assembly and its analysis are available at the NCBI Sequencing Read Archive and Gene Expression Omnibus under accession numbers PRJNA530242 and GSE131340, and the Transcriptome Shotgun Assembly at DDBJ/ENA/GenBank under the accession GHJF00000000. The transcriptome assembly described in this paper is the first version, GHJF01000000. Cloned cDNA sequences for FLYC genes are deposited at GenBank. All other data are available in the main text or supplementary materials.

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Author details

1. Carl Procko

   Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States

   Contribution

   Conceptualization, Formal analysis, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing, Performed gene expression analysis, cloned and generated FLYC cDNAs

   Contributed equally with

   Swetha Murthy and William T Keenan

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4374-4283

2. Swetha Murthy

   1. Department of Neuroscience, Dorris Neuroscience Center, Scripps Research, San Diego, United States
   2. Howard Hughes Medical Institute, Chevy Chase, United States

   Present address

   Vollum Institute, Oregon Health & Science University, Portland, United States

   Contribution

   Conceptualization, Formal analysis, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing, Recorded and analyzed electrophysiology data

   Contributed equally with

   Carl Procko and William T Keenan

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-9580-3380

3. William T Keenan

   1. Department of Neuroscience, Dorris Neuroscience Center, Scripps Research, San Diego, United States
   2. Howard Hughes Medical Institute, Chevy Chase, United States

   Contribution

   Conceptualization, Formal analysis, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing, Performed and analyzed in situ expression

   Contributed equally with

   Carl Procko and Swetha Murthy

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3381-744X

4. Seyed Ali Reza Mousavi

   1. Department of Neuroscience, Dorris Neuroscience Center, Scripps Research, San Diego, United States
   2. Howard Hughes Medical Institute, Chevy Chase, United States

   Contribution

   Conceptualization, Formal analysis, Visualization, Methodology, Writing - review and editing, Cloned and generated FLYC cDNAs

   Competing interests

   No competing interests declared

5. Tsegaye Dabi

   Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States

   Contribution

   Formal analysis, Investigation, Methodology

   Competing interests

   No competing interests declared

6. Adam Coombs

   1. Department of Neuroscience, Dorris Neuroscience Center, Scripps Research, San Diego, United States
   2. Howard Hughes Medical Institute, Chevy Chase, United States

   Contribution

   Formal analysis, Investigation, Methodology, Cloned and generated FLYC cDNAs and FLYC1 mutants

   Competing interests

   No competing interests declared

7. Erik Procko

   Department of Biochemistry, University of Illinois at Urbana-Champaign, Urbana, United States

   Contribution

   Conceptualization, Formal analysis, Investigation, Methodology, Writing - review and editing, Performed FLYC1 homology modeling

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-0028-490X

8. Lisa Baird

   Department of Biology, University of San Diego, San Diego, United States

   Contribution

   Formal analysis, Investigation, Methodology, Writing - review and editing, Performed toluidine blue staining and microscopy

   Competing interests

   No competing interests declared

9. Ardem Patapoutian

   1. Department of Neuroscience, Dorris Neuroscience Center, Scripps Research, San Diego, United States
   2. Howard Hughes Medical Institute, Chevy Chase, United States

   Contribution

   Conceptualization, Resources, Formal analysis, Supervision, Funding acquisition, Investigation, Visualization, Writing - original draft, Project administration, Writing - review and editing

   For correspondence

   ardem@scripps.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0726-7034

10. Joanne Chory

    Plant Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States

    Contribution

    Conceptualization, Resources, Formal analysis, Supervision, Funding acquisition, Investigation, Visualization, Writing - original draft, Project administration, Writing - review and editing

    For correspondence

    chory@salk.edu

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0002-3664-8525

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