Peripheral coding of taste

Abstract

Five canonical tastes, bitter, sweet, umami (amino acid), salty, and sour (acid), are detected by animals as diverse as fruit flies and humans, consistent with a near-universal drive to consume fundamental nutrients and to avoid toxins or other harmful compounds. Surprisingly, despite this strong conservation of basic taste qualities between vertebrates and invertebrates, the receptors and signaling mechanisms that mediate taste in each are highly divergent. The identification over the last two decades of receptors and other molecules that mediate taste has led to stunning advances in our understanding of the basic mechanisms of transduction and coding of information by the gustatory systems of vertebrates and invertebrates. In this Review, we discuss recent advances in taste research, mainly from the fly and mammalian systems, and we highlight principles that are common across species, despite stark differences in receptor types.

Figure 1

The taste organs in mammals, such as mice and humans, and in flies. (A) The rodent tongue contains taste buds that are located in three distinct regions. Taste buds are also found on the palate (not shown). (B) The taste bud is composed of 50–100 modified epithelial cells that extend a process to the taste pore, where they come into contact with ingested chemicals. At least five types of sensory cells (depicted in different colors) are found in the taste bud, corresponding to the five canonical tastes. (C) Green circles indicate locations of external gustatory organs distributed on an adult Drosophila female. (D) The Drosophila proboscis. Shown are the labellum, and three internal taste organs indicated in blue: the labral sense organs (LSOs), the dorsal cibarial sense organ (DCSO), and the ventral cibarial sense organ (VCSO). (E) Distribution of the L-, I- and S-type sensilla on a fly labellum. (F) An S- or L-type sensilla containing four GRNs. The accessory cells are not shown. (G) A Drosophila larvae. The external chemosensory organs are located at the anterior. (H) Anterior end of a larvae. The locations of the dorsal organ (DO), the terminal organ (TO), and the ventral organ (VO) are indicated.

Figure 2

Taste receptors and transduction in the mouse and fly. (A) Transmembrane topology of bitter, sweet and umami receptors in mouse. All are G-protein coupled-receptors. Bitter receptors (35 total in mice) are Class A GPCRs while sweet and umami receptors (two each) are Class C receptors, characterized by a large N terminal domain that forms a Venus flytrap structure. Sweet and umami receptors bind both ligands (ovals) and allosteric modifiers (circles) that can increase potency of the agonist. (B) Transduction of bitter, sweet and umami in the vertebrate is mediated by a canonical PLC-signaling cascade, that culminates in the opening of the TRPM5 ion channel. This produces a depolarization that may allow CALMH1 channels to open and release ATP, which serves as a neurotransmitter. (C) Drosophila taste receptors that function in bitter, sweet, amino acid (L-canavanine), glycerol and water detection. The minimum number of receptors are indicated.

Figure 3

Sour taste. Sour taste in vertebrates is initiated when protons enter through an apically located proton-selective ion channel. Weak acids may also activate sour cells by penetrating the cell membrane and acidifying the cytosol, leading to closure of resting K⁺ channels and membrane depolarization.

Figure 4

Salt taste. (A) The mouse low salt sensor is a protypical ENaC channel composed of three subunits. The high salt sensor in TRPM5 or PKD2L1-expressing taste cells is not known. (B) The salt sensors in fly larvae. (C) No Na⁺ influx through IR76b when adult flies are not exposed to salt containing food, since the Na⁺ concentration in the endolymph is low. (D) The concentration of Na⁺ concentration in the endolymph rises when adult flies are exposed to salt containing food, leading to an influx of Na⁺ through constitutively open IR76b and activation of the GRN.