Abstract
Chemosensory systems are critical for evaluating the caloric value and potential toxicity of food prior to ingestion. While animals can discriminate between 1000's of odors, much less is known about the discriminative capabilities of taste systems. Fats and sugars represent calorically potent and innately attractive food sources that contribute to hedonic feeding. Despite the differences in nutritional value between fats and sugars, the ability of the taste system to discriminate between different rewarding tastants is thought to be limited. In Drosophila, sweet taste neurons expressing the Ionotropic Receptor 56d (IR56d) are required for reflexive behavioral responses to the medium-chain fatty acid, hexanoic acid. Further, we have found that flies can discriminate between a fatty acid and a sugar in aversive memory assays, establishing a foundation to investigate the capacity of the Drosophila gustatory system to differentiate between various appetitive tastants. Here, we tested whether flies can discriminate between different classes of fatty acids using an aversive memory assay. Our results indicate that flies are able to discriminate medium-chain fatty acids from both short- and long-chain fatty acids, but not from other medium-chain fatty acids. While IR56d neurons are broadly responsive to short-, medium-, and long-chain fatty acids, genetic deletion of IR56d selectively disrupts response to medium-chain fatty acids. Further, IR56d+GR64f+ neurons are necessary for proboscis extension response (PER) to medium-chain fatty acids, but both IR56d and GR64f neurons are dispensable for PER to short- and long-chain fatty acids, indicating the involvement of one or more other classes of neurons. Together, these findings reveal that IR56d is selectively required for medium-chain fatty acid taste, and discrimination of fatty acids occurs through differential receptor activation in shared populations of neurons. Our study uncovers a capacity for the taste system to encode tastant identity within a taste category.
Highlights
Animals detect food primarily through taste and olfactory systems
We and others have found that deletion of PLC signaling selectively impairs fatty acid response while leaving sweet taste intact, raising the possibility that activation of distinct intracellular signaling pathways could serve as a mechanism for discrimination between sucrose and fatty acid (Masek & Keene, 2013; Ahn et al, 2017; Tauber et al, 2017), while another suggests TRPA1 and GR64e are targets of PLC and are generally required for FA sensing (Kim et al, 2018)
One 357 possibility is that this is due to differences in fatty acid detection, which is dependent on Ionotropic Receptors (IRs), and sweet and bitter tastant detection, which relies on gustatory receptors (GRs) (Chen & Dahanukar, 2020)
Summary
Animals detect food primarily through taste and olfactory systems. Across phyla, there is enormous complexity in olfactory receptors and downstream processing mechanisms that allow for detection and differentiation between odorants (Keller et al, 2017; Nara et al, 2011; Parnas et al, 2013). Quantification of the responses to all tastants confirmed that Ca2+ responses to 6C-8C fatty acids are disrupted in IR56dGAL4 flies, and restored to levels observed in control flies by expression of UAS-IR56d (Figure 5H) Overall, these results demonstrate that at both behavioral and physiological levels, IR56dGAL4 is required for taste responses to medium chain fatty acids. In agreement with our previous findings, these neurons were robustly responsive to hexanoic acid (6C), but not by sucrose (Figure 6D-F; Tauber et al, 2017) These neurons responded to other classes of fatty acids including short- (4C and 5C), medium- (7C and 8C) and long-chain (9C and 10C) (Figure 6D-F). These findings support the notion that medium chain fatty acids are detected through a shared sensory channel, allowing flies to distinguish medium chain from short or long-chain, but not between different medium-chain fatty acids
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