1. Neuroscience
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Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila

  1. Zachary A Knecht
  2. Ana F Silbering
  3. Lina Ni
  4. Mason Klein
  5. Gonzalo Budelli
  6. Rati Bell
  7. Liliane Abuin
  8. Anggie J Ferrer
  9. Aravinthan DT Samuel  Is a corresponding author
  10. Richard Benton  Is a corresponding author
  11. Paul A Garrity  Is a corresponding author
  1. Brandeis University, United States
  2. University of Lausanne, Switzerland
  3. Harvard University, United States
  4. University of Miami, United States
Research Article
  • Cited 72
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Cite this article as: eLife 2016;5:e17879 doi: 10.7554/eLife.17879

Abstract

Ionotropic Receptors (IRs) are a large subfamily of variant ionotropic glutamate receptors present across Protostomia. While these receptors are most extensively studied for their roles in chemosensory detection, recent work has implicated two family members, IR21a and IR25a, in thermosensation in Drosophila. Here we characterize one of the most evolutionarily deeply conserved receptors, IR93a, and show that it is co-expressed and functions with IR21a and IR25a to mediate physiological and behavioral responses to cool temperatures. IR93a is also co-expressed with IR25a and a distinct receptor, IR40a, in a discrete population of sensory neurons in the sacculus, a multi-chambered pocket within the antenna. We demonstrate that this combination of receptors is required for neuronal responses to dry air and behavioral discrimination of humidity differences. Our results identify IR93a as a common component of molecularly and cellularly distinct IR pathways important for thermosensation and hygrosensation in insects.

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Author details

  1. Zachary A Knecht

    Department of Biology, National Center for Behavioral Genomics and Volen Center for Complex Systems, Brandeis University, Waltham, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Ana F Silbering

    Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.

  3. Lina Ni

    Department of Biology, National Center for Behavioral Genomics and Volen Center for Complex Systems, Brandeis University, Waltham, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Mason Klein

    Department of Physics and Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Gonzalo Budelli

    Department of Biology, National Center for Behavioral Genomics and Volen Center for Complex Systems, Brandeis University, Waltham, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Rati Bell

    Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.

  7. Liliane Abuin

    Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.

  8. Anggie J Ferrer

    Department of Physics, University of Miami, Coral Gables, United States
    Competing interests
    The authors declare that no competing interests exist.

  9. Aravinthan DT Samuel

    Department of Physics and Center for Brain Science, Harvard University, Cambridge, United States
    For correspondence
    aravisamuel@me.com
    Competing interests
    The authors declare that no competing interests exist.

  10. Richard Benton

    Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland
    For correspondence
    Richard.Benton@unil.ch
    Competing interests
    The authors declare that no competing interests exist.

  11. Paul A Garrity

    National Center for Behavioral Genomics and Volen Center for Complex Systems, Department of Biology, Brandeis University, Waltham, United States
    For correspondence
    pgarrity@brandeis.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8274-6564

Funding

National Institutes of Health (F31 DC015155 01A1)

  • Zachary A Knecht

National Institutes of Health (F32 NS077835)

  • Mason Klein

Boehringer Ingelheim Fonds (PhD Fellowship)

  • Rati Bell

European Research Council (Starting Independent Researcher Grant 205202)

  • Richard Benton

European Research Council (Consolidator Grant 915094)

  • Richard Benton

National Institutes of Health (F32 GM113318)

  • Gonzalo Budelli

National Institutes of Health (P01 GM103770)

  • Aravinthan DT Samuel
  • Paul A Garrity

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

Reviewing Editor

  1. Mani Ramaswami, Trinity College Dublin, Ireland

Publication history

  1. Received: May 17, 2016
  2. Accepted: September 21, 2016
  3. Accepted Manuscript published: September 22, 2016 (version 1)
  4. Accepted Manuscript updated: September 23, 2016 (version 2)
  5. Version of Record published: October 5, 2016 (version 3)

Copyright

© 2016, Knecht 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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    Ionotropic Receptor-dependent moist and dry cells control hygrosensation in Drosophila

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    Insects use hygrosensation (humidity sensing) to avoid desiccation and, in vectors such as mosquitoes, to locate vertebrate hosts. Sensory neurons activated by either dry or moist air (‘dry cells’ and ‘moist cells’) have been described in many insects, but their behavioral roles and the molecular basis of their hygrosensitivity remain unclear. We recently reported that Drosophila hygrosensation relies on three Ionotropic Receptors (IRs) required for dry cell function: IR25a, IR93a and IR40a (Knecht et al., 2016). Here, we discover Drosophila moist cells and show that they require IR25a and IR93a together with IR68a, a conserved, but orphan IR. Both IR68a- and IR40a-dependent pathways drive hygrosensory behavior: each is important for dry-seeking by hydrated flies and together they underlie moist-seeking by dehydrated flies. These studies reveal that humidity sensing in Drosophila, and likely other insects, involves the combined activity of two molecularly related but neuronally distinct hygrosensing systems.

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