Dietary Macronutrient Imbalances Lead to Compensatory Changes in Peripheral Taste via Independent Signaling Pathways

• Published in: The Journal of neuroscience 2021-12, Vol.41 (50), p.10222-10246
• Main Authors: Ganguly, Anindya, Dey, Manali, Scott, Christi, Duong, Vi-Khoi, Arun Dahanukar, Anupama
• Format: Article
• Language: English
• Subjects: Amino acids; Animals; Deprivation; Diet; Drosophila melanogaster - physiology; Drosophila Proteins - metabolism; Enrichment; Feeding Behavior - physiology; Female; Flies; Food; Food preferences; Food Preferences - physiology; Food sources; Foraging behavior; Insulins - metabolism; Male; Molecular modelling; Nutrients; Nutritional requirements; Plastic properties; Plasticity; Preferences; Receptors, Dopamine D1 - metabolism; Reduction; Sensitivity; Signal Transduction - physiology; Signaling; Sugar; Sweet taste; Taste; Taste thresholds; Transcriptomes
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.2154-20.2021

Food choice, in animals, has been known to change with internal nutritional state and also with variable dietary conditions. To better characterize mechanisms of diet-induced plasticity of food preference in , we synthesized diets with macronutrient imbalances and examined how food choice and taste sensitivity were modified in flies that fed on these diets. We found that dietary macronutrient imbalances caused compensatory behavioral shifts in both sexes to increase preference for the macronutrient that was scant in the food source, and simultaneously reduce preference for the macronutrient that was enriched. Further analysis with females revealed analogous changes in sweet taste responses in labellar neurons, with increased sensitivity on sugar-reduced diet and decreased sensitivity on sugar-enriched diet. Interestingly, we found differences in the onset of changes in taste sensitivity and behavior, which occur over 1-4 d, in response to dietary sugar reduction or enrichment. To investigate molecular mechanisms responsible for diet-induced taste modulation, we used candidate gene and transcriptome analyses. Our results indicate that signaling via is involved in increasing cellular and behavioral sensitivity to sugar as well as in decreasing behavioral sensitivity to amino acids on dietary sugar reduction. On the other hand, cellular and behavioral sensitivity to sugar relies on and a decrease in sugar preference following dietary sugar abundance was correlated with downregulation of Together, our results suggest that feeding preference for sugar and amino acid can be modulated independently to facilitate food choice that accounts for prior dietary experience. Animals adjust their feeding preferences based on prior dietary experiences. Here, we find that upon dietary macronutrient deprivation, flies undergo compensatory changes in food preference. The altered preference correlates with changes in peripheral taste sensitivity. While mediates changes following dietary sugar reduction, downregulation of is associated with changes caused by a sugar-enriched diet. This study contributes to a better understanding of neurophysiological plasticity of the taste system in flies, and its role in facilitating adjustment of foraging behavior based on nutritional requirements.