Drosophila Bitter Taste(s)

Abstract

Most animals possess taste receptors neurons detecting potentially noxious compounds. In humans, the ligands which activate these neurons define a sensory space called “bitter”. By extension, this term has been used in animals and insects to define molecules which induce aversive responses. In this review, based on our observations carried out in Drosophila, we examine how bitter compounds are detected and if bitter-sensitive neurons respond only to molecules bitter to humans. Like most animals, flies detect bitter chemicals through a specific population of taste neurons, distinct from those responding to sugars or to other modalities. Activating bitter-sensitive taste neurons induces aversive reactions and inhibits feeding. Bitter molecules also contribute to the suppression of sugar-neuron responses and can lead to a complete inhibition of the responses to sugar at the periphery. Since some bitter molecules activate bitter-sensitive neurons and some inhibit sugar detection, bitter molecules are represented by two sensory spaces which are only partially congruent. In addition to molecules which impact feeding, we recently discovered that the activation of bitter-sensitive neurons also induces grooming. Bitter-sensitive neurons of the wings and of the legs can sense chemicals from the gram negative bacteria, Escherichia coli, thus adding another biological function to these receptors. Bitter-sensitive neurons of the proboscis also respond to the inhibitory pheromone, 7-tricosene. Activating these neurons by bitter molecules in the context of sexual encounter inhibits courting and sexual reproduction, while activating these neurons with 7-tricosene in a feeding context will inhibit feeding. The picture that emerges from these observations is that the taste system is composed of detectors which monitor different “categories” of ligands, which facilitate or inhibit behaviors depending on the context (feeding, sexual reproduction, hygienic behavior), thus considerably extending the initial definition of “bitter” tasting.

Immediate perception of a reward is distinct from the reward’s long-term salience

“…Tip-recording was performed as previously described (French et al, 2015). Briefly, adult flies (3- to 4-day old) were anesthetized on ice and immobilized on a putty platform (UHU stick), using thin stripes of tape.…”

Evolutionary Insights into Taste Perception of the Invasive PestDrosophila suzukii

“…Unlike ORs, some GRs are characterized by exhibiting functional plasticity beyond gustatory perception: for example, GR28bD is involved in thermosensation (Ni et al 2013), while GR21a and GR63a are expressed in specific antennal sensilla and are associated with CO 2 detection (Jones et al 2007; Kwon et al 2007). Such functional diversification is also revealed by the observation that, in D. melanogaster , GRs are expressed not only in GRNs, but also in other neurons scattered in different tissues (French et al 2015). …”

“…Initially discovered in 1999 (Clyne et al 2000), GRs are the first and most extensively studied family of chemoreceptors to be found to be expressed in GRNs in insects. Efforts to elucidate the molecular details of their function have been steadily increasing in the past few years, but to date only a limited number of GRs have been deorphanized in a few insect species (Sato et al 2011; Erdelyan et al 2012; Freeman and Dahanukar 2015; French et al 2015; Joseph and Carlson 2015). In D. melanogaster , the GR family includes 60 genes encoding 68 receptor proteins (Robertson et al 2003; Gardiner et al 2008; Almeida et al 2014).…”

Morphological and electrophysiological analysis of tarsal sensilla in the medfly Ceratitis capitata (Wiedemann, 1824) (Diptera: Tephritidae)

“…Bitter chemoreception has a noteworthy relevance in insects in relation to feeding behaviour or to avoidance of toxic substances (French et al 2015). Apis mellifera massively extends the proboscis (PER value was around 80%) in response to 1 M sucrose, while salicin or quinine do not cause retraction of the proboscis when applied to the contralateral antenna (De Brito Sanchez et al 2005).…”

“…Transmission electron microscopy showed four GRNs and one mechanoreceptor in each tarsal sensillum (Nayak & Singh 1983). These four GRNs were activated by sugars, low concentration of salt, water and bitter compounds (Meunier et al 2000(Meunier et al , 2009French et al 2015).…”