Ir56d-dependent fatty acid responses in Drosophila uncovers taste discrimination between different classes of fatty acids

  1. Elizabeth B Brown
  2. Kreesha D Shah
  3. Justin Palermo
  4. Manali Dey
  5. Anupama Dahanukar  Is a corresponding author
  6. Alex C Keene  Is a corresponding author
  1. Florida Atlantic University, United States
  2. University of California, Riverside, United States

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.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all figures.

Article and author information

Author details

  1. Elizabeth B Brown

    Biological Science, Florida Atlantic University, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Kreesha D Shah

    Biological Sciences, Florida Atlantic University, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Justin Palermo

    Biological Sciences, Florida Atlantic University, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Manali Dey

    Molecular, Cell and Systems Biology, University of California, Riverside, Riverside, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Anupama Dahanukar

    Molecular, Cell and Systems Biology, University of California, Riverside, Riverside, United States
    For correspondence
    anupama.dahanukar@ucr.edu
    Competing interests
    The authors declare that no competing interests exist.
  6. Alex C Keene

    Biological Sciences, Florida Atlantic University, Jupiter, United States
    For correspondence
    keenea@fau.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6118-5537

Funding

National Institutes of Health (NIH R01DC017390)

  • Elizabeth B Brown
  • Kreesha D Shah
  • Justin Palermo
  • Manali Dey
  • Anupama Dahanukar

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2021, Brown et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Elizabeth B Brown
  2. Kreesha D Shah
  3. Justin Palermo
  4. Manali Dey
  5. Anupama Dahanukar
  6. Alex C Keene
(2021)
Ir56d-dependent fatty acid responses in Drosophila uncovers taste discrimination between different classes of fatty acids
eLife 10:e67878.
https://doi.org/10.7554/eLife.67878

Share this article

https://doi.org/10.7554/eLife.67878

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