Detecting chemical cues can be a matter of life or death for insects, and many employ three families of receptor proteins to detect a broad range of odors. Members of one of these receptor families, the olfactory receptors, form a complex with another protein, the olfactory coreceptor that is essential for both positioning and stabilizing the receptor, as well as the actual function.

Crustaceans share a common ancestor with insects, and since they do not have olfactory receptors it has been proposed that these receptors evolved when prehistoric insects moved from the sea to live on land. According to this idea, olfactory receptors evolved because these ancestors needed to be able to detect odor molecules floating in the air rather than dissolved in water.

Previous research on insect olfactory receptors has focused on insects with wings. Missbach et al. have now used a wide range of techniques to investigate how evolutionarily older wingless insect groups detect scents. As all investigated groups evolved from a common ancestor at different times these experiments allow tracking of the historical development of olfactory receptors.

In the wingless species that is more closely related to the flying insects there was evidence of the presence of multiple coreceptors but not the olfactory receptors themselves. In the most basal insects no evidence for any part of the olfactory receptor-based system was found. This indicates that the main olfactory receptors evolved independently of the coreceptor long after the migration of insects from water to land. Missbach et al. suggest that olfactory receptors instead developed far later, around the time when vascular plants spread and insects developed the ability to fly.

All living organisms, including bacteria, protozoans, fungi, plants, and animals, detect chemicals in their environment. The sensitivity and chemical range of animal olfactory systems is remarkable, enabling animals to detect and discriminate between thousands of different odor molecules. Although there is a striking evolutionary convergence towards a conserved organization of signaling pathways in vertebrate and invertebrate olfactory systems (Hildebrand and Shepherd, 1997), the involved receptor gene families evolved independently. The molecular identity of olfactory receptors was first unraveled in vertebrates (Buck and Axel, 1991). In mammals, as many as 1000 heterotrimeric GTP-binding protein (or G protein)-coupled receptors are considered to be employed in olfactory discrimination (Buck and Axel, 1991). A similar number of chemoreceptors, with about 1300 receptor genes and 400 pseudogenes, have been hypothesized for Caenorhabditis elegans (Robertson and Thomas, 2006).

All data on insect olfactory receptors are based on studies investigating the neopteran insects (overview of insect order relationship is given in Figure 1). The identity of receptors involved in olfaction in the evolutionarily more ancient apterygote insects (Archaeognatha, Zygentoma) and paleopteran insects (Odonata and Ephemeroptera) is thus completely unknown. In neopteran insects (Polyneoptera, Paraneoptera, and Holometabola) most volatile stimuli are recognized by members of the olfactory receptor family (ORs). ORs are multitransmembrane domain proteins unrelated to nematode or vertebrate olfactory receptors (Mombaerts, 1999; Robertson, 2001; Hill et al., 2002), displaying a distinct membrane topology (Benton et al., 2006; Lundin et al., 2007). The number of functional OR genes varies from 10 in the human body louse Pediculus humanus humanus (Kirkness et al., 2010) to about 60 in Drosophila melanogaster (Clyne et al., 1999; Gao and Chess, 1999; Vosshall et al., 1999) and up to 350 OR genes in ants (Zhou et al., 2012). ORs have been suggested to be distantly related to the gustatory receptors of arthropods, with some proteins containing a signature motif in the carboxyl terminus (Scott et al., 2001).

Figure 1

Download asset Open asset

Insect olfactory receptors function as heteromultimers composed of at least one ligand-specific OR and the coreceptor Orco (Vosshall et al., 1999; Elmore et al., 2003; Krieger et al., 2003; Larsson et al., 2004; Sato et al., 2008; Wicher et al., 2008). Interestingly, while Orco (Vosshall and Hansson, 2011) is highly conserved among insects, the sequences of other olfactory receptor genes exhibit very little sequence similarity even within the same insect order (Krieger et al., 2003), complicating their identification. So far, Orco homologues have been identified in Lepidoptera, Diptera, Coleoptera, Hymenoptera, Hemiptera (Krieger et al., 2003; Pitts et al., 2004; Smadja et al., 2009), and Orthoptera (Yang et al., 2012). Neither Orco nor ORs are present in the genome of the crustacean Daphnia pulex, indicating that ORs are insect specific. However, GRs were found in Crustacea, just as in insects (Peñalva-Arana et al., 2009).

A second receptor family, the variant ionotropic glutamate receptors (IRs), is also involved in insect chemosensation (Benton et al., 2009). IRs act in combinations of up to three subunits; individual odor-specific receptors and one or two of the broadly expressed coreceptors IR25a, IR8a, and IR76b (Abuin et al., 2011). IRs are present in olfactory tissues across the Protostomia (Croset et al., 2010), for example two conserved members of this group were described in the Daphnia genome (Croset et al., 2010) and the coreceptor IR25a homologue is expressed in many, if not all mature OSNs of the American lobster Homarus americanus (Hollins et al., 2003) and the spiny lobster Panulirus argus (Tadesse et al., 2011). Since crustaceans are the closest relatives of insects (Friedrich and Tautz, 1995; Boore et al., 1998; Regier et al., 2010), IRs are most likely the ancient type of insect olfactory receptor.

But when and why did insect ORs evolve? Hexapods derived from an aquatic crustacean ancestor, probably in the Early Ordovician, approximately 483 mya (Rota-Stabelli et al., 2013). The transition from sea to land meant that molecules needed to be detected in gas phase instead of aquatic solution. Therefore, the olfactory system of a hexapod ancestor had to adapt to the terrestrial conditions and detection of volatile, air-borne chemicals. One proposed hypothesis has been that Orco and ORs of the insect type are an adaptation to this terrestrial lifestyle (Robertson et al., 2003; Krång et al., 2012). To reconstruct an evolutionary scenario for insect ORs, we investigated species belonging to different ancient insect orders, including Archaeognatha (jumping bristletails) and Zygentoma (silverfishes and firebrats), and a neopteran insect belonging to the Phasmatodea (leaf and stick insects) as so far not analyzed control group using morphological, electrophysiological and molecular techniques.

Our first step was to analyze the evolutionary ancestry of the insect olfactory system by assessing its complexity in each of three non-holometabolan insects.

To correlate OSN responses with type of sensillum (with pores and grooves) identified in SEM studies of the antennae, we investigated the morphological and physiological characteristics of olfactory sensilla and their olfactory sensory neurons.

Morphology and physiology

On the antennae of L. y-signata the only putative olfactory sensilla were porous olfactory basiconic sensilla (Figure 2B–E). These sensilla were arranged in a pattern that is highly stereotypical between antennal modules composed of 5–12 annuli, with annuli typically containing zero-to-four Sensilla basiconica (Missbach et al., 2011). Responses to all tested chemical classes of odors, including acids, alcohols, aldehydes, esters, and ketones, were recorded from OSNs housed in these sensilla using the single sensillum recoding measurements (SSR) (Figure 3, uppermost heat map). Based on the response profile, spontaneous activity, and colocalization inside the same sensillum, we identified 12 OSN types, present in five functional basiconic sensillum types. Out of the 12 OSN types, only seven responded to odors tested; two exclusively to acids, while five responded with a similar activity rate to acids or amines and to other odors. OSNs belonging to this second class were broadly tuned and exhibited relatively low spiking activity. In general, OSN classes displayed a low baseline activity with about 1 to 7 spikes/s, with Lys-ab2A that had a spontaneous activity of more than 25 spikes/s as the only exception. Only rarely was an increase in spiking rate of more than 60 spikes per second recorded, even for the best identified ligands (Figure 3—source data 1). No responses were obtained for ammonia or pyridine. Coeloconic-like sensilla, s-shaped trichoid sensilla, and chaetic sensilla did not display any morphological features indicating olfactory function and did also not respond to any odor tested (Missbach et al., 2011; data not shown). In conclusion, 7 OSN types that were all housed in basiconic sensilla responded to a wide spectrum of odor molecules.

Figure 2

Download asset Open asset

Figure 3

Download asset Open asset

Figure 3—source data 1

Excel file of mean responses and baseline firing rate of the different OSN classes of L.y-signata, T. domestica, P.siccifolium, and D. melanogaster.

https://doi.org/10.7554/eLife.02115.006

Download elife-02115-fig3-data1-v1.xlsx

The morphology of the zygentoman antenna and its sensilla was similar to that of L. y-signata, with the presence of grooved sensilla as the only exception (Figure 2G; Adel, 1984; Berg and Schmidt, 1997). Five different functional types of olfactory sensilla were present (Figure 3: three porous, two grooved s. basiconica, the latter are indicated by blue caption). In contrast to L. y-signata, a nascent functional and spatial separation of the detection of amines and acids, and ketones and alcohols appeared in T. domestica. The former primarily elicited responses in OSNs of grooved sensilla, while less polar ones were mainly detected by porous sensilla. However, most of the OSNs in porous sensilla exhibited broad tuning and responded to at least one of the tested acids or amines as well.

We then turned to a neopteran insect. Unlike the other analyzed species, the leaf insect P. siccifolium displayed a strong sexual antennal dimorphism, with males having very long antennae covered with trichoid sensilla (Figure 2L), and the females very short antennae without trichoid sensilla (Figure 2K). In comparison to the wingless insects, the response repertoire of the leaf insect was much more diverse, with a total of 23 different functional sensillum types as identified by SSR recordings (Figure 3). No responses were obtained from trichoid sensilla, but since they were only present on the male antennae they could be involved in detection of an unknown volatile pheromone. In all cases, reported detection of volatile pheromones in insects is dependent on very specific ORs. Taken together these data suggest that leaf insects have a much broader response repertoire with a higher number of different OSN types than the more basal species we analyzed; apparently the number of olfactory receptors has increased. It also seems likely that at least the leaf insect makes use of ORs in odorant detection.

No ORs or Orco were found in the transcriptome of L. y-signata

The transcriptome data sets were manually screened for genes encoding proteins putatively involved in insect olfaction, including ORs, Orco, GRs, and IRs (number of identified contigs are given in Table 2).

Table 2

Organism	Orco	ORs	GRs	IRs
Lepismachilis y-signata	–	–	7 (5 above 400 bp)	17 (16 above 400 bp)
Thermobia domestica	6 (1 above 400 bp)	–	9 (3 above 400 bp)	19 (9 above 400 bp)
Phyllium siccifolium	1 (1 above 400 bp)	30 (16 above 400 bp)	6 (2 above 400 bp)	32 (19 above 400 bp)

Neither OR- nor Orco-coding transcripts were identified in the transcriptomes of L. y-signata using BLAST and HMM domain profile searches as described in the ‘Material and methods’ section. Custom HMMR-profiles directed against conserved regions of Orco proteins also failed to identify any Orco-related sequences in the bristletail transcriptome. We discovered five GR candidates. MSA analysis of these together with ORs and GRs of various insect species and the Daphnia GRs always confirmed the position of the L. y-signata GR candidates within the GR and not the OR family (Figure 4A, Figure 4—source data 1, Figure 4—source data 2, Figure 4—source data 3, Figure 4—source data 4, Figure 4—source data 5). Since expression levels of gustatory receptors are very low even in gustatory tissue (Clyne et al., 2000; Scott et al., 2001), we argue that ORs or at least Orco should be represented in the large, sensory tissue-specific transcriptome data set of L. y-signata if they are indeed part of the olfactory system in the species.

Figure 4

Download asset Open asset

Figure 4—source data 1

Amino acid sequences of putative olfactory and gustatory receptors of L. y-signata, T. domestica, and P. siccifolium.

https://doi.org/10.7554/eLife.02115.010

Download elife-02115-fig4-data1-v1.docx

Figure 4—source data 2

Nucleotide sequences of putative olfactory and gustatory receptors of L. y-signata, T. domestica, and P. siccifolium.

https://doi.org/10.7554/eLife.02115.011

Download elife-02115-fig4-data2-v1.docx

Figure 4—source data 3

MAFFT-alignment of OR and GR candidates of L. y-signata, T. domestica, P. siccifolium and D. melanogaster (Clyne et al., 1999, Gao and Chess, 1999, Vosshall et al., 1999) and Apis mellifera (Robertson and Wanner, 2006) GR and OR proteins, as well as Daphnia pulex GRs done.

https://doi.org/10.7554/eLife.02115.012

Download elife-02115-fig4-data3-v1.fasta

Figure 4—source data 4

FastTree file resulting from the MSA of Figure 4—source data 3 (can be opened with FigTree).

https://doi.org/10.7554/eLife.02115.013

Download elife-02115-fig4-data4-v1.txt

Figure 4—source data 5

Tree file resulting from the MSA of Figure 4—source data 3 containing node support values (can be opened e.g., with Adobe Illustrator).

https://doi.org/10.7554/eLife.02115.014

Download elife-02115-fig4-data5-v1.pdf

The three Orco-paralogues of T. domestica

In contrast to L. y-signata, three different Orco-related sequences were identified in the transcriptome of T. domestica. All candidates were cloned as full-length coding sequences using RACE-PCR. The three sequences displayed different similarities to the Orco sequence of D. melanogaster, one sequence shared 45.8%, one 35.1%, and the third 24.4% sequence similarity at the amino acid level. Orco was the protein most similar to all three Orco candidate sequences (Figures 4B and 5), although some of the key amino acids of the coreceptor are substituted at least in TdomOrco3 (Wicher et al., 2008; Sargsyan et al., 2011; Nakagawa et al., 2012; Kumar et al., 2013; highlighted in alignment Figure 5). Apart from the Orco variants, no OR-related sequences were identified, but 9 contigs for GR candidates were found that were assigned to seven GRs, including three candidates close to full length or full length and four additional fragments (Table 2 and Figure 4A).

Figure 5

Download asset Open asset

Orco expression in T. domestica

Considering that for all other insects analyzed so far one Orco is the norm, the appearance of three Orco candidates in T. domestica is highly unusual. We thus assessed the expression of the three candidates in different tissues using RT-PCR. For all three Orco types expression was limited to the antenna (Figure 6). To further assess the expression, we used in situ hybridization employing an antisense probe of one of the coreceptors. This led to staining of single cells below one or two basiconic sensilla of an antennal subsegment (Figure 7), suggesting that TdomOrco1 might indeed be expressed in OSNs. However, only one neuron per sensillum was stained. No signals were obtained when using a sense probe for TdomOrco1 (Figure 7—figure supplement 1).

Figure 6

Download asset Open asset

Figure 6—source data 1

Primers and their properties used in this study.

https://doi.org/10.7554/eLife.02115.017

Download elife-02115-fig6-data1-v1.xlsx

Figure 7 with 1 supplement see all

Download asset Open asset

Only IRs in L-y-signata

As none of the experiments gave a hint for the existence of any OR or Orco-related sequence in the bristletail transcriptome, we focused on the second olfactory receptor family of insects, the IRs. Although we could not identify any OR sequences in the transcriptome, a high number of putative glutamate receptor coding contigs was identified (Table 2). However, only five candidate iGluRs and 14 candidate IRs appeared to be real unigenes, possessing at least two of the three transmembrane domains. Some candidate sequences were extended in 3’-direction using RACE-PCR with antennal cDNA as template, allowing verification of unigene status and antennal expression. In MSA and phylogenetic analysis, the identified IRs grouped with DmelIRs (Croset et al., 2010). Among the identified putative LsigIRs were orthologues of the D. melanogaster coreceptors IR25a and IR8a, as well as one receptor similar to IR76b (Figure 8A, Figure 8—source data 1, Figure 8—source data 2, Figure 8—source data 3, Figure 8—source data 4, Figure 8—source data 5). As in other IRs (Benton et al., 2009) one or several key amino acids in the predicted glutamate binding domains were absent in the non-coreceptor IR candidates and LsigIR76b (Figure 8B). 7 out of 14 LsigIRs group close to a cluster of D. pulex IRs and the antennal IRs IR21a and IR68a of D. melanogaster, with no clear relationship to one or the other. None of the Lepismachilis IR candidates grouped with the ‘divergent’ Drosophila IRs.

Figure 8

Download asset Open asset

Figure 8—source data 1

Amino acid sequences of putative variant ionotropic glutamate receptors of L. y-signata, T. domestica, and P. siccifolium.

https://doi.org/10.7554/eLife.02115.021

Download elife-02115-fig8-data1-v1.docx

Figure 8—source data 2

Nucleotide sequences of putative variant ionotropic glutamate receptors of L. y-signata, T. domestica, and P. siccifolium.

https://doi.org/10.7554/eLife.02115.022

Download elife-02115-fig8-data2-v1.docx

Figure 8—source data 3

MAFFT amino acid alignment of iGluR and IR candidates of L. y-signata, T. domestica, P. siccifolium, D. melanogaster, and D. pulex (D. melanogaster and D. pulex sequences were sequences taken from Croset et al., 2010).

https://doi.org/10.7554/eLife.02115.023

Download elife-02115-fig8-data3-v1.fasta

Figure 8—source data 4

FastTree file resulting from the MSA of Figure 4—source data 3 (can be opened with FigTree).

https://doi.org/10.7554/eLife.02115.024

Download elife-02115-fig8-data4-v1.txt

Figure 8—source data 5

Tree file resulting from the MSA of Figure 8—source data 3 containing node support values.

https://doi.org/10.7554/eLife.02115.025

Download elife-02115-fig8-data5-v1.pdf

We then performed fluorescent in situ hybridization with RNA probes directed against the IR coreceptor candidates (Figure 9). Antisense probes of IR25a and IR8a led to labeling of one to three OSNs underneath basiconic sensilla (Figure 9—figure supplement 1). In control experiments with sense probes, or without any probe, no staining was obtained (Figure 9—figure supplement 2). The pattern of expression of IR coreceptors in OSNs of L. y-signata indicates that most OSNs are covered by this gene family.

Figure 9 with 2 supplements see all

Download asset Open asset

All experiments thus indicate that the olfactory system of this species employs other receptors like IRs or GRs, with no ORs or Orco present.

Insects provide us with an excellent opportunity to study groups of animals that have retained ancestral characteristics and understand how the specific building blocks in olfaction have evolved in both insects and other animals. Consequently, we selected insects at crucial positions of the phylogenetic tree with a functional olfactory system adapted to terrestrial conditions and detection of volatile chemicals. This species collection provides an excellent model to study the early evolution of the insect olfactory system.

To address which receptors are involved in odor detection in these insects and in basal insects in general, we applied several different approaches. Based on our transcriptome data sets, we suggest a stepwise evolution of the Orco/OR complex with Orco having evolved in the lineage of Dicondylia (Zygentoma + Pterygota) and the functional complex of Orco and ORs emerging within the pterygote insects (this study, Clyne et al., 1999; Gao and Chess, 1999; Smadja et al., 2009; Vosshall et al., 1999; Robertson and Wanner, 2006; Kirkness et al., 2010). Although it is impossible to completely rule out the presence of ORs, none of our extensive experiments led to the identification of either ORs or Orco in the bristletail L. y-signata. The well-established conservation of the Orco coding gene through evolution suggests that it is highly unlikely that we missed it. We did, however, identify a number of IRs, including the IR coreceptors IR25a, IR8a, and IR76b in the L. y-signata antennal transcriptome. FISH allowed us to visualize expression of the IR co-receptors in a large number of OSNs associated with basiconic sensilla. Based on these results we propose that the olfactory system of L. y-signata is not based on ORs.

In insects, different sensillum types house OSNs typically responding to different sets of odors. In D. melanogaster IRs are the functional receptor type of OSNs in double-walled coeloconic sensilla, and ORs are predominantly expressed in OSNs housed in single-walled basiconic and trichoid sensilla (Hallem et al., 2004; Silbering et al., 2011). It follows that this organization cannot exist with just one sensillum type present, as is the case in Archaeognatha (Berg and Schmidt, 1997; Missbach et al., 2011) and older hexapod taxa as the Collembola (Altner and Prillinger, 1980). The oldest insect taxon where double-walled sensilla were investigated is Zygentoma, which have both single-walled basiconic sensilla with pores and double-walled sensilla with spoke channels (Berg and Schmidt, 1997). Coeloconic sensilla differ dramatically from the single-walled trichoid and basiconic types in both wall structure and in internal environment. The coeloconic structure has been thought to be a prerequisite for IR function (Benton et al., 2009; Guo et al., 2014). However, in the Archaeognatha we find that IRs are most likely located in OSNs of Sensilla basiconica. IRs might thus have evolved in a single-walled sensillum and did not find their modern, coeloconic environment until neopteran insects evolved.

In the bristletail L. y-signata, we found that many of the OSNs are very broadly tuned, responding to volatiles with several different functional groups at higher doses. However, broadly tuned receptors might not have high affinities. By counting and integrating molecules over longer times, OSNs could include even low-probability binding events in generating their response (Firestein, 2001). This might also mean that the system does not have a high temporal resolution, which seems to be a fair trade-off for a walking insect that lives in its substrate.

The response spectrum of Drosophila IRs is much narrower than the responses we find in the bristletail. If IRs are the only olfactory receptor type in basal insects they should exhibit a broader spectrum of possible ligands, including acids, aldehydes, alcohols, but also esters and ketones, as revealed in our physiological measurements. One additional observation in the bristletail is that many of those neurons have a broad overlap in their response spectra. One hypothesis to explain an IR-based olfactory system in L. y-signata would be very broad tuning of single receptors, another that the selectivity of OSNs could be regulated by combinations of different IRs.

In D. melanogaster, one conserved IR (IR64a) is expressed in different subpopulations of sensilla in the third chamber of the sacculus (Silbering et al., 2011). Corresponding OSNs are activated either by free protons or organic acids and many other odors, including esters, alcohols, and ketones (Ai et al., 2010). Expression of this IR together with IR8a is both necessary and sufficient for sensitivity towards organic acids and other odors, but probably requires a different, until now unknown cofactor to mediate the specific response of OSNs to inorganic acids and CO₂ (Ai et al., 2010).

Alternatively, GR candidates could account for part of the non-neopteran olfactory setup, especially since it has been shown that GRs can add to the olfactory repertoire (Tauxe et al., 2013). Putative contact chemosensory sensilla are highly abundant on the antennae of L. y-signata (Missbach et al., 2011) and T. domestica (Adel, 1984). Both detection of sugars/amino acids (shown for T. domestica: Hansen-Delkeskamp, 2001) and a proposed contact-pheromone (Fröhlich and Lu, 2013) likely involve GRs, indicating that involvement of the limited set of GRs beyond this scope is unlikely.

However, these data do not explain the presence of three different Orco variants in the firebrat. So far only one Orco orthologue has been identified in each studied insect species (e.g., Krieger et al., 2003; Pitts et al., 2004; Smadja et al., 2009; Yang et al., 2012). All T. domestica variants were found to be expressed in antennae, suggesting their involvement in chemosensation. TdomOrco3 even has an amino acid exchange of a functional important residue from asparagine to glutamic acid at position 466. This residue was demonstrated as critical for the ion channel function in D. melanogaster, where substitution of D466 with amino acids other than glutamic acid resulted in a substantial reduction in channel activity, but substitution to glutamic acid leads to an increase in sensitivity of the heteromeric receptor complex (Kumar et al., 2013). Additionally, this residue is highly conserved across insects (Kumar et al., 2013) including two of the three T. domestica Orcos (this study).

While the antennal expression argues for a potential involvement in chemosensation, the existence of three Orco types remains mysterious. It will be part of future studies to investigate if the Orco candidates form heterodimers with other receptors like GRs or with each other to build functional receptors or if they fulfill a channel function in other processes than olfaction.

Altogether our data suggests that ORs evolved in insects after the emergence of Archaeognatha and Zygentoma, and therefore long after insects transitioned to a terrestrial lifestyle. At the time when flying insects occurred, the vegetation on earth was rapidly spreading and diversifying. ORs might not only increase the diversity of detected chemicals, but also allow the olfactory system to rapidly assess airborne odors. This is especially important for insects for which stimulus contact is very short and a fast response time is critical (Getahun et al., 2012). The oldest flying insect orders Odonta (dragonflies and damselflies) and Ephemeroptera (mayflies) were traditionally considered to be anosmic, lacking both a glomerular antennal lobe and mushroom body calyces (Strausfeld et al., 1998; Farris, 2005). Recent studies have shown that at least dragonflies have an aerial sense of smell (Rebora et al., 2012). However the small antennae and the low number of olfactory sensilla will make it even more challenging to identify putative ORs and Orco in antennal transcriptomes. ORs were definitely present in the last common ancestor of ‘hemi’- and holometabolan insects at least 318–300 million years ago, with Orco present in both groups (this study, Krieger et al., 2003; Pitts et al., 2004; Smadja et al., 2009; Yang et al. 2012). The increasing dispersion of vascular plants together with the development of wings and a secondary wing articulation opened new and wider ranges of habitats and ecological niches for insects and the receptors to find them.

1. 1. Missbach C
   2. Dweck HKM
   3. Vogel H
   4. Vilcinskas A
   5. Stensmyr MC
   6. Hansson BS
   7. Grosse-Wilde E

   (2014) Evolution of insect olfactory receptors - RNAseq

   ID PRJEB5093. Publicly available at the European Nucleotide Archive (http://www.ebi.ac.uk/ena/).

   http://www.ebi.ac.uk/ena/data/view/PRJEB5093

1. 1. Adel T

   (1984)

   Sensilla and sensilla pattern on the antenna of Thermobia domestica and Lepisma saccharina (Insecta: Zygentoma)

   Braunschweiger Naturkundliche Schriften 2:191–218.

   • Google Scholar
2. 1. Ai M
   2. Min S
   3. Grosjean Y
   4. Leblanc C
   5. Bell R
   6. Benton R
   7. Suh GS

   (2010) Acid sensing by the Drosophila olfactory system

   Nature 468:691–695.

   https://doi.org/10.1038/nature09537

   • Google Scholar
3. 1. Abuin L
   2. Bargeton B
   3. Ulbrich MH
   4. Isacoff EY
   5. Kellenberger S
   6. Benton R

   (2011) Functional architecture of olfactory ionotropic glutamate receptors

   Neuron 69:44–60.

   https://doi.org/10.1016/j.neuron.2010.11.042

   • Google Scholar
4. 1. Altner H
   2. Prillinger L

   (1980) Ultrastructure of invertebrate chemo-, thermo- and hygroreceptors and its functional significance

   International Review of Cytology 67:69–139.

   https://doi.org/10.1016/S0074-7696

   • Google Scholar
5. Book

   1. Angerer LM
   2. Angerer RC

   (1992)

   In situ hybridization to cellular RNA with radiolabeled RNA probes

   In: Wilkinson DG, editors. In Situ Hybridization. A practical approach. Oxford: IRL Press. pp. 15–32.

   • Google Scholar
6. 1. Benton R
   2. Vannice KS
   3. Gomez-Diaz C
   4. Vosshall LB

   (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila

   Cell 136:149–162.

   https://doi.org/10.1016/j.cell.2008.12.001

   • Google Scholar
7. 1. Benton R
   2. Sachse S
   3. Michnick SW
   4. Vosshall LB

   (2006) A typical membrane topology and heteromeric function of Drosophila odorant receptors in vivo

   PLOS Biology 4:e20.

   https://doi.org/10.1371/journal.pbio.0040020

   • Google Scholar
8. 1. Berg J
   2. Schmidt K

   (1997) Comparative morphology and moulting of Sensilla basiconica of Lepisma saccharina Linnaeus (Zygentoma: Lepismatidae) and Machilis sp. (Archaeognatha: Machilidae)

   International Journal of Insect Morphology & Embryology 26:161–172.

   https://doi.org/10.1016/S0020-7322(97)00018-4

   • Google Scholar
9. 1. Bockhorst KG

   (1988)

   Patterns of sensilla on the antennae of some Machilidae (Insecta, Archaeognatha)

   Braunschweiger Naturkundliche Schriften 3:137–170.

   • Google Scholar
10. 1. Boore JL
    2. Lavrov DV
    3. Brown WM

    (1998) Gene translocation links insects and crustaceans

    Nature 392:667–668.

    https://doi.org/10.1038/33577

    • Google Scholar
11. 1. Buck L
    2. Axel R

    (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition

    Cell 65:175–187.

    https://doi.org/10.1016/0092-8674(91)90418-X

    • Google Scholar
12. 1. Clyne PJ
    2. Warr CG
    3. Freeman MR
    4. Lessing D
    5. Kim J
    6. Carlson JR

    (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila

    Neuron 22:327–338.

    https://doi.org/10.1016/S0896-6273(00)81093-4

    • Google Scholar
13. 1. Clyne PJ
    2. Warr CG
    3. Carlson JR

    (2000) Candidate taste receptors in Drosophila

    Science 287:1830–1834.

    https://doi.org/10.1126/science.287.5459.1830

    • Google Scholar
14. 1. Conesa A
    2. Götz S
    3. García-Gómez JM
    4. Terol J
    5. Talón M
    6. Robles M

    (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research

    Bioinformatics 21:3674–3676.

    https://doi.org/10.1093/bioinformatics/bti610

    • Google Scholar
15. 1. Croset V
    2. Rytz R
    3. Cummins SF
    4. Budd A
    5. Brawand D
    6. Kaessmann H
    7. Gibson TJ
    8. Benton R

    (2010) Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction

    PLOS Genetics 6:e1001064.

    https://doi.org/10.1371/journal.pgen.1001064

    • Google Scholar
16. 1. Eddy SR

    (2011) Accelerated profile HMM searches

    PLOS Computational Biology 7:e1002195.

    https://doi.org/10.1371/journal.pcbi.1002195

    • Google Scholar
17. 1. Elmore T
    2. Ignell R
    3. Carlson JR
    4. Smith DP

    (2003)

    Targeted mutation of a Drosophila odor receptor defines receptor requirement in a novel class of sensillum

    Journal of Neuroscience 23:9906–9912.

    • Google Scholar
18. 1. Farris SM

    (2005) Evolution of insect mushroom bodies: old clues, new insights

    Arthropod Structure & Development 34:211–234.

    https://doi.org/10.1016/j.asd.2005.01.008

    • Google Scholar
19. 1. Firestein S

    (2001) How the olfactory system makes sense of scents

    Nature 413:211–218.

    https://doi.org/10.1038/35093026

    • Google Scholar
20. 1. Friedrich M
    2. Tautz D

    (1995) Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods

    Nature 376:165–167.

    https://doi.org/10.1038/376165a0

    • Google Scholar
21. 1. Fröhlich A
    2. Lu Z

    (2013) The “rosette-like“ structures in the cuticle of Petrobius brevistylis are the openings of epidermal glands

    Arthropod Structure & Development 42:89–94.

    https://doi.org/10.1016/j.asd.2012.10.001

    • Google Scholar
22. 1. Gao Q
    2. Chess A

    (1999) Identification of candidate Drosophila olfactory receptors from genomic DNA sequence

    Genomics 60:31–39.

    https://doi.org/10.1006/geno.1999.5894

    • Google Scholar
23. 1. Getahun MN
    2. Wicher D
    3. Hansson BS
    4. Olsson SB

    (2012) Temporal response dynamics of Drosophila olfactory sensory neurons depends on receptor type and response polarity

    Frontiers in Cellular Neuroscience 6:1–11.

    https://doi.org/10.3389/fncel.2012.00054

    • Google Scholar
24. 1. Guo M
    2. Krieger J
    3. Grosse-Wilde E
    4. Mißbach C
    5. Zhang L
    6. Breer H

    (2014) Variant ionotropic receptors are expressed in olfactory sensory neurons of coeloconic sensilla on the antenna of the desert locust (Schistocerca gregaria)

    International Journal of Biological Sciences 10:1–14.

    https://doi.org/10.7150/ijbs.7624

    • Google Scholar
25. 1. Hallem EA
    2. Ho MG
    3. Carlson JR

    (2004) The molecular basis of odor coding in the Drosophila antenna

    Cell 117:965–979.

    https://doi.org/10.1016/j.cell.2004.05.012

    • Google Scholar
26. 1. Hansen-Delkeskamp E

    (2001) Responsiveness of antennal taste hairs of the apterygotan insect, Thermobia domestica (Zygentoma); an electrophysiological investigation

    Journal of Insect Physiology 47:689–697.

    https://doi.org/10.1016/S0022-1910(00)00159-1

    • Google Scholar
27. 1. Hildebrand JG
    2. Shepherd GM

    (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla

    Annual Review of Neuroscience 20:595–631.

    https://doi.org/10.1146/annurev.neuro.20.1.595

    • Google Scholar
28. 1. Hill CA
    2. Fox AN
    3. Pitts RJ
    4. Kent LB
    5. Tan PL
    6. Chrystal MA
    7. Cravchik A
    8. Collins FH
    9. Robertson HM
    10. Zwiebel LJ

    (2002) G protein coupled receptors in Anopheles gambiae

    Science 298:176–178.

    https://doi.org/10.1126/science.1076196

    • Google Scholar
29. 1. Hollins B
    2. Hardin D
    3. Gimelbrant AA
    4. McClintock TS

    (2003) Olfactory-enriched transcripts are cell-specific markers in the lobster olfactory organ

    The Journal of Comparative Neurology 455:125–138.

    https://doi.org/10.1002/cne.10489

    • Google Scholar
30. 1. Katoh K
    2. Kuma K
    3. Toh H
    4. Miyata T

    (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment

    Nucleic Acids Research 33:511–518.

    https://doi.org/10.1093/nar/gki198

    • Google Scholar
31. 1. Kirkness EF
    2. Haas BJ
    3. Sun W
    4. Braig HR
    5. Perotti MA
    6. Clark JM
    7. Lee SH
    8. Robertson HM
    9. Kennedy RC
    10. Elhaik E
    11. Gerlach D
    12. Kriventseva EV
    13. Elsik CG
    14. Graur D
    15. Hill CA
    16. Veenstra JA
    17. Walenz B
    18. Tubío JM
    19. Ribeiro JM
    20. Rozas J
    21. Johnston JS
    22. Reese JT
    23. Popadic A
    24. Tojo M
    25. Raoult D
    26. Reed DL
    27. Tomoyasu Y
    28. Kraus E
    29. Mittapalli O
    30. Margam VM
    31. Li HM
    32. Meyer JM
    33. Johnson RM
    34. Romero-Severson J
    35. Vanzee JP
    36. Alvarez-Ponce D
    37. Vieira FG
    38. Aguadé M
    39. Guirao-Rico S
    40. Anzola JM
    41. Yoon KS
    42. Strycharz JP
    43. Unger MF
    44. Christley S
    45. Lobo NF
    46. Seufferheld MJ
    47. Wang N
    48. Dasch GA
    49. Struchiner CJ
    50. Madey G
    51. Hannick LI
    52. Bidwell S
    53. Joardar V
    54. Caler E
    55. Shao R
    56. Barker SC
    57. Cameron S
    58. Bruggner RV
    59. Regier A
    60. Johnson J
    61. Viswanathan L
    62. Utterback TR
    63. Sutton GG
    64. Lawson D
    65. Waterhouse RM
    66. Venter JC
    67. Strausberg RL
    68. Berenbaum MR
    69. Collins FH
    70. Zdobnov EM
    71. Pittendrigh BR

    (2010) Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle

    Proceedings of the National Academy of Sciences of the United States of America 107:12168–12173.

    https://doi.org/10.1073/pnas.1003379107

    • Google Scholar
32. 1. Krång A-S
    2. Knaden M
    3. Steck K
    4. Hansson BS

    (2012) Transition from sea to land: olfactory function and constraints in the terrestrial hermit crab Coenobita clypeatus

    Proceedings Biological Sciences/The Royal Society 279:3510–3519.

    https://doi.org/10.1098/rspb.2012.0596

    • Google Scholar
33. 1. Krieger J
    2. Klink O
    3. Mohl C
    4. Raming K
    5. Breer H

    (2003) A candidate olfactory receptor subtype highly conserved across different insect orders

    Journal of Comparative Physiology A, Neuroethology, Sensory, Neural, and Behavioral Physiology 189:519–526.

    https://doi.org/10.1007/s00359-003-0427-x

    • Google Scholar
34. 1. Kumar BN
    2. Taylor RW
    3. Pask GM
    4. Zwiebel LJ
    5. Newcomb RD
    6. Christie DL

    (2013) A conserved aspartic acid is important for agonist (VUAA1) and odorant/tuning receptor-dependent activation of the insect odorant co-receptor (Orco)

    PLOS ONE 8:e70218.

    https://doi.org/10.1371/journal.pone.0070218

    • Google Scholar
35. 1. Larsson MC
    2. Domingos AI
    3. Jones WD
    4. Chiappe ME
    5. Amrein H
    6. Vosshall LB

    (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction

    Neuron 43:703–714.

    https://doi.org/10.1016/j.neuron.2004.08.019

    • Google Scholar
36. 1. Liu K
    2. Linder CR
    3. Warnow T

    (2011) RAxML and FastTree: comparing two methods for large-scale maximum likelihood phylogeny estimation

    PLOS ONE 6:e27731.

    https://doi.org/10.1371/journal.pone.0027731

    • Google Scholar
37. 1. Lundin C
    2. Käll L
    3. Kreher SA
    4. Kapp K
    5. Sonnhammer EL
    6. Carlson JR
    7. Heijne Gv
    8. Nilsson I

    (2007) Membrane topology of the Drosophila OR83b odorant receptor

    FEBS Letters 581:5601–5604.

    https://doi.org/10.1016/j.febslet.2007.11.007

    • Google Scholar
38. 1. Missbach C
    2. Harzsch S
    3. Hansson BS

    (2011) New insights into an ancient insect nose: the olfactory pathway of Lepismachilis y-signata (Archaeognatha: Machilidae)

    Arthropod Structure & Development 40:317–333.

    https://doi.org/10.1016/j.asd.2011.03.004

    • Google Scholar
39. 1. Mombaerts P

    (1999) Seven-transmembrane proteins as odorant and chemosensory receptors

    Science 286:707–711.

    https://doi.org/10.1126/science.286.5440.707

    • Google Scholar
40. 1. Nakagawa T
    2. Pellegrino M
    3. Sato K
    4. Vosshall LB
    5. Touhara K

    (2012) Amino acid residues contributing to function of the heteromeric insect olfactory receptor complex

    PLOS ONE 7:e32372.

    https://doi.org/10.1371/journal.pone.0032372

    • Google Scholar
41. 1. Peñalva-Arana DC
    2. Lynch M
    3. Robertson HM

    (2009) The chemoreceptor genes of the waterflea Daphnia pulex: many Grs but no Ors

    Bmc Evolutionary Biology 9:79.

    https://doi.org/10.1186/1471-2148-9-79

    • Google Scholar
42. 1. Pitts RJ
    2. Fox AN
    3. Zwiebel LJ

    (2004) A highly conserved candidate chemoreceptor expressed in both olfactory and gustatory tissues in the malaria vector Anopheles gambiae

    Proceedings of the National Academy of Sciences of the United States of America 101:5058–5063.

    https://doi.org/10.1073/pnas.0308146101

    • Google Scholar
43. 1. Price MN
    2. Dehal PS
    3. Arkin AP

    (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix

    Molecular Biology and Evolution 26:1641–1650.

    https://doi.org/10.1093/molbev/msp077

    • Google Scholar
44. 1. Rebora M
    2. Salerno G
    3. Piersanti S
    4. Dell’Otto A
    5. Gaino E

    (2012) Olfaction in dragonflies: electrophysiological evidence

    Journal of Insect Physiology 58:270–277.

    https://doi.org/10.1016/j.jinsphys.2011.11.018

    • Google Scholar
45. 1. Regier JC
    2. Shultz JW
    3. Zwick A
    4. Hussey A
    5. Ball B
    6. Wetzer R
    7. Martin JW
    8. Cunningham CW

    (2010) Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences

    Nature 463:1079–1083.

    https://doi.org/10.1038/nature08742

    • Google Scholar
46. 1. Robertson HM

    (2001) Taste: independent origins of chemoreception coding systems?

    Current Biology 11:560–562.

    https://doi.org/10.1016/S0960-9822(01)00343-8

    • Google Scholar
47. 1. Robertson HM
    2. Warr CG
    3. Carlson JR

    (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster

    Proceedings of the National Academy of Sciences of the United States of America 100:14537–14542.

    https://doi.org/10.1073/pnas.2335847100

    • Google Scholar
48. 1. Robertson HM
    2. Thomas JH

    (2006) The putative chemoreceptor families of C. elegans

    (January 06, 2006). In: The C. elegans Research Community, editor. WormBook, 10.1895/wormbook.1.66.1, http://www.wormbook.org.

    http://www.wormbook.org

    • Google Scholar
49. 1. Robertson HM
    2. Wanner KW

    (2006) The chemoreceptor superfamily in the honey bee Apis mellifera: expansions of the odorant, but not gustatory, receptor families

    Genome Research 16:1395–1403.

    https://doi.org/10.1101/gr.5057506

    • Google Scholar
50. 1. Rota-Stabelli O
    2. Daley AC
    3. Pisani D

    (2013) Molecular timetrees reveal a Cambrian colonization of land and a new scenario for ecdysozoan evolution

    Current Biology 23:392–398.

    https://doi.org/10.1016/j.cub.2013.01.026

    • Google Scholar
51. 1. Sargsyan V
    2. Getahun MN
    3. Lavista Llanos S
    4. Olsson SB
    5. Hansson BS
    6. Wicher D

    (2011) Phosphorylation via PKC regulates the function of the Drosophila odorant co-receptor

    Frontiers in Cellular Neuroscience 5:5.

    https://doi.org/10.3389/fncel.2011.00005

    • Google Scholar
52. 1. Sato K
    2. Pellegrino M
    3. Nakagawa T
    4. Nakagawa T
    5. Vosshall LB
    6. Touhara K

    (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels

    Nature 452:1002–1006.

    https://doi.org/10.1038/nature06850

    • Google Scholar
53. 1. Scott K
    2. Brady R Jnr
    3. Cravchik A
    4. Morozov P
    5. Rzhetsky A
    6. Zuker C
    7. Axel R

    (2001) A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila

    Cell 104:661–673.

    https://doi.org/10.1016/S0092-8674(01)00263-X

    • Google Scholar
54. 1. Silbering AF
    2. Rytz R
    3. Grosjean Y
    4. Abuin L
    5. Ramdya P
    6. Jefferis GS
    7. Benton R

    (2011) Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems

    Journal of Neuroscience 31:13357–13375.

    https://doi.org/10.1523/jneurosci.2360-11.2011

    • Google Scholar
55. 1. Smadja C
    2. Shi P
    3. Butlin RK
    4. Robertson HM

    (2009) Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum

    Molecular Biology and Evolution 26:2073–2086.

    https://doi.org/10.1093/molbev/msp116

    • Google Scholar
56. 1. Strausfeld NJ
    2. Hansen L
    3. Ll Y
    4. Gomez RS
    5. Ito K

    (1998) Evolution, discovery, and interpretations of arthropod mushroom bodies

    Learning & Memory 5:11–37.

    https://doi.org/10.1101/lm.5.1.11

    • Google Scholar
57. 1. Tadesse T
    2. Schmidt M
    3. Walthall WW
    4. Tai PC
    5. Derby CD

    (2011) Distribution and function of splash, an achaete-scute homolog in the adult olfactory organ of the Caribbean spiny lobster Panulirus argus

    Developmental Neurobiology 71:316–335.

    https://doi.org/10.1002/dneu.20862

    • Google Scholar
58. 1. Tauxe GM
    2. MacWilliam D
    3. Boyle SM
    4. Guda T
    5. Ray A

    (2013) Targeting a dual detector of skin and CO2 to modify mosquito host seeking

    Cell 155:1365–1379.

    https://doi.org/10.1016/j.cell.2013.11.013

    • Google Scholar
59. 1. Trautwein MD
    2. Wiegmann BM
    3. Beutel R
    4. Kjer KM
    5. Yeates D

    (2012) Advances in insect phylogeny at the dawn of the postgenomic era

    Annual Review of Entomology 57:499–468.

    https://doi.org/10.1146/annurev-ento-120710-100538

    • Google Scholar
60. 1. Vosshall LB
    2. Amrein H
    3. Morozov PS
    4. Rzhetsky A
    5. Axel R

    (1999) A spatial map of olfactory receptor expression in the Drosophila antenna

    Cell 96:725–736.

    https://doi.org/10.1016/s0092-8674(00)80582-6

    • Google Scholar
61. 1. Vosshall LB
    2. Hansson BS

    (2011) A unified nomenclature system for the insect olfactory coreceptor

    Chemical Senses 36:497–498.

    https://doi.org/10.1093/chemse/bjr022

    • Google Scholar
62. 1. Wicher D
    2. Schäfer R
    3. Bauernfeind R
    4. Stensmyr MC
    5. Heller R
    6. Heinemann SH
    7. Hansson BS

    (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels

    Nature 452:1007–1011.

    https://doi.org/10.1038/nature06861

    • Google Scholar
63. 1. Wiegmann BM
    2. Trautwein MD
    3. Kim JW
    4. Cassel BK
    5. Bertone MA
    6. Winterton SL
    7. Yeates DK

    (2009) Single-copy nuclear genes resolve the phylogeny of holometabolous insects

    BMC Biology 7:1–16.

    https://doi.org/10.1186/1741-7007-7-34

    • Google Scholar
64. 1. Yang Y
    2. Krieger J
    3. Zhang L
    4. Breer H

    (2012) The olfactory co-receptor Orco from the migratory locust (Locusta migratoria) and the desert locust (Schistocerca gregaria): identification and expression pattern

    International Journal of Biological Sciences 8:159–170.

    https://doi.org/10.7150/ijbs.8.159

    • Google Scholar
65. 1. Zhou X
    2. Slone JD
    3. Rokas A
    4. Berger SL
    5. Liebig J
    6. Ray A
    7. Reinberg D
    8. Zwiebel LJ

    (2012) Phylogenetic and transcriptomic analysis of chemosensory receptors in a pair of divergent ant species reveals sex-specific signatures of odor coding

    PLOS Genetics 8:e1002930.

    https://doi.org/10.1371/journal.pgen.1002930

    • Google Scholar

Author details

1. Christine Missbach

   Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   CM, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   For correspondence

   cmissbach@ice.mpg.de

   Competing interests

   The authors declare that no competing interests exist.

2. Hany KM Dweck

   Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   HKMD, Conception and design, Acquisition of data, Analysis and interpretation of data

   Competing interests

   The authors declare that no competing interests exist.

3. Heiko Vogel

   Department of Entomology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   HV, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

4. Andreas Vilcinskas

   Institute of Phytopathology and Applied Zoology, Justus-Liebig-Universität Gießen, Gießen, Germany

   Contribution

   AV, Drafting or revising the article, Contributed unpublished essential data or reagents

   Competing interests

   The authors declare that no competing interests exist.

5. Marcus C Stensmyr

   Department of Biology, Lund University, Lund, Sweden

   Contribution

   MCS, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

6. Bill S Hansson

   Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   BSH, Conception and design, Drafting or revising the article

   Contributed equally with

   Ewald Grosse-Wilde

   Competing interests

   The authors declare that no competing interests exist.

7. Ewald Grosse-Wilde

   Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   EG-W, Conception and design, Analysis and interpretation of data, Drafting or revising the article

   Contributed equally with

   Bill S Hansson

   For correspondence

   Grosse-Wilde@ice.mpg.de

   Competing interests

   The authors declare that no competing interests exist.

• 8,875

  views

• 1,596

  downloads

• 238

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.