An expression atlas of chemosensory ionotropic glutamate receptors identifies a molecular basis of carbonation detection

Abstract

Taste perception is thought to involve the encoding of appetitive and aversive chemical cues in food through a limited number of sensory pathways. Through expression analysis of the complete repertoire of Drosophila Ionotropic Receptors (IRs), a sensory subfamily of ionotropic glutamate receptors, we reveal that the majority of IRs is expressed in diverse peripheral neuron populations across gustatory organs in both larvae and adults, implying numerous roles in taste-evoked behaviours. We characterise Ir56d, which labels two anatomically-distinct classes of neurons in the proboscis: one represents a subset of sugar-and fatty acid-sensing neurons, while the other responds to carbonated solutions and fatty acids. Mutational analysis shows that IR56d, together with the broadly-expressed co-receptors IR25a and IR76b, is essential for physiological activation by carbonation and fatty acids, but not sucrose. We further demonstrate that carbonation is behaviourally attractive to flies (in an IR56d-dependent manner), but in a distinct way to other appetitive stimuli. Our work provides a valuable toolkit for investigating the taste functions of IRs, defines a molecular basis of carbonation sensing, and illustrates how the gustatory system uses combinatorial expression of sensory receptors in distinct neuron types to coordinate behaviour.Classic models of gustatory perception in mammals highlight the existence of a small number of taste classes signalling nutritive content (e.g., sugars and amino acids) or toxicity (e.g., bitter) that determine -through activation of hard-wired neural circuits -behavioural acceptance or rejection of food 1, 2 . Different classes of tastants are recognised by discrete sensory channels that express distinct, and relatively small, receptor families. For example, detection of all sugars depends upon a single heterodimeric GPCR complex (T1R2/T1R3), while "bitter" cells -which detect an enormous diversity of noxious compounds -co-express a few dozen GPCRs of the T2R family 1, 2 . Such models have been pervasive in interpreting how gustatory perception occurs in other animals, including insects, where analogous segregated sensory pathways for sweet and bitter compounds have been defined [3][4][5][6] . However, in contrast to mammals, where taste -mediated by lingual taste buds -informs only feeding decisions, insect gustation occurs in multiple sensory appendages, including the proboscis, legs, wings and sexual organs, and controls diverse behaviours, such as foraging, feeding, sexual/social recognition and oviposition [3][4][5][6] . In addition to stereotyped appetitive and aversive feeding responses to sweet and bitter compounds respectively, insects display behavioural reactions to many other types of chemicals, including salt 7 , water 8 , carbonation (i.e., aqueous CO 2 ) 9 , organic and inorganic acids 10,11 , and pheromonal cuticular hydrocarbons 12 . The wide-ranging roles of the insect gustatory system are concordantly reflected in the underlying molecular receptors that mediate...

Current Status on the Functional Characterization of Chemosensory Receptors of Cydia pomonella (Lepidoptera: Tortricidae)

“…With the aim to complement these studies, using Illumina-based RNA-sequencing, assembly of a transcriptome from male, female and larval olfactory tissues of the codling moth, a more complete list of chemosensory receptors of C. pomonella was updated to 21 IRs, 20 GRs and 58 putative ORs, among which, 11 represented members of the PR-clade (Walker et al, 2016 ; Table 1 ). Identification of IRs and GRs in antennal transcriptomes of the codling moth was in accordance with the reported findings of their functional importance in insect chemosensation (Clyne et al, 2000 ; Robertson et al, 2003 ; Benton et al, 2009 ; Montell, 2009 ; Ai et al, 2010 ; Silbering et al, 2011 ; Rytz et al, 2013 ; Missbach et al, 2014 ; Sanchez-Alcaniz et al, 2018 ). Despite their importance, most of the efforts to functionally characterize chemosensory receptors of the codling moth targeted ORs, with particular focus on members of the PR-subfamily.…”

Multimodal and multisensory coding in theDrosophilalarval peripheral gustatory center

“…Fig.1). Our approach complements previous strategies based on labeling of few single neurons or subpopulations (6,29,35,39,48), allowing for an overview of activation patterns within the organ. Strengthening our previous observations on the multimodal character of larval taste neurons (48), we identified single GSNs activated by different taste categories as well as single GSNs activated by tastants with opposite associated valence.…”

“…In Drosophila taste sensing has been described in accordance with a labeled-line model, as sweet, bitter and water perception localize in separate populations of peripheral GSNs (18)(19)(20)(21)(22). However, additional tastes such as salt, fatty acid, carbonation, polyamines or amino acids partially overlap onto sweet or bitter sensing GSNs by means of specific added-on receptor expression (23)(24)(25)(26)(27)(28)(29)(30)), suggesting a model of taste sensing with both narrowly and more broadly tuned cells, similar to mammals. The peripheral gustatory system in the Drosophila larva presents many similarities with the adult fly, such as the sensillar organization of dendrites, presence of both internal and external chemosensory organs (31), as well as cue detection through the same chemoreceptor gene families -GRs (Gustatory Receptors), IR (Ionotropic Receptors), PPKs (pickpocket) or TRPs (Transient Receptor Potential) (29,(32)(33)(34)(35)(36)(37)(38).…”

“…However, additional tastes such as salt, fatty acid, carbonation, polyamines or amino acids partially overlap onto sweet or bitter sensing GSNs by means of specific added-on receptor expression (23)(24)(25)(26)(27)(28)(29)(30)), suggesting a model of taste sensing with both narrowly and more broadly tuned cells, similar to mammals. The peripheral gustatory system in the Drosophila larva presents many similarities with the adult fly, such as the sensillar organization of dendrites, presence of both internal and external chemosensory organs (31), as well as cue detection through the same chemoreceptor gene families -GRs (Gustatory Receptors), IR (Ionotropic Receptors), PPKs (pickpocket) or TRPs (Transient Receptor Potential) (29,(32)(33)(34)(35)(36)(37)(38). On the other hand, larval taste processing presents developmental stage particularities, considering that the number of GSNs is much lower than in adult flies and many receptors are larva-specific (39,40).…”

The Two Main Olfactory Receptor Families in Drosophila, ORs and IRs: A Comparative Approach

“…The IRs are formed by an extracellular N-terminus, a highly variable ligand-binding domain with two lobes separated by an ion channel domain, and a short cytoplasmic C-terminus (Benton et al, 2009 ). Sixteen IRs out of the 66 discovered are expressed in antennal neurons, while the rest, named “divergent IRs”, are expressed in other locations in the body (Benton et al, 2009 ; Sánchez-Alcañiz et al, 2018 ).…”