Investigation of Drosophila fruitless neurons that express Dpr/DIP cell adhesion molecules

  1. Savannah G Brovero
  2. Julia C Fortier
  3. Hongru Hu
  4. Pamela C Lovejoy
  5. Nicole R Newell
  6. Colleen M Palmateer
  7. Ruei-Ying Tzeng
  8. Pei-Tseng Lee
  9. Kai Zinn
  10. Michelle N Arbeitman  Is a corresponding author
  1. Florida State University, United States
  2. Baylor College of Medicine, United States
  3. California Institute of Technology, United States

Abstract

Drosophila reproductive behaviors are directed by fruitless neurons. A reanalysis of genomic studies shows that genes encoding dpr and DIP Immunoglobulin superfamily (IgSF) members are expressed in fru P1 neurons. We find that each fru P1 and dpr/DIP (fru P1dpr/DIP) overlapping expression pattern is similar in both sexes, but there are dimorphisms in neuronal morphology and cell number. Behavioral studies of fru P1dpr/DIP perturbation genotypes indicates that the mushroom body functions together with the lateral protocerebral complex to direct courtship behavior. A single-cell RNA-seq analysis of fru P1 neurons shows that many DIPs have high expression in a small set of neurons, whereas the dprs are often expressed in a larger set of neurons at intermediate levels, with a myriad of dpr/DIP expression combinations. Functionally, we find that perturbations of sex hierarchy genes and of DIP-ε change the sex-specific morphologies of fru P1DIP-α neurons.

Data availability

All raw data are provided in the supplementary materials. The sequencing data has been deposited in GEO under accession number GSE162098

The following data sets were generated

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Author details

  1. Savannah G Brovero

    Biomedical Sciences, Florida State University, Tallahassee, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Julia C Fortier

    Biomedical Sciences, Florida State University, Tallahassee, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Hongru Hu

    Biomedical Sciences, Florida State University, Tallahassee, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Pamela C Lovejoy

    Biomedical Sciences, Florida State University, Tallahassee, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Nicole R Newell

    Biomedical Sciences, Florida State University, Tallahassee, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Colleen M Palmateer

    Biomedical Sciences, Florida State University, Tallahassee, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Ruei-Ying Tzeng

    Biomedical Sciences, Florida State University, Tallahassee, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Pei-Tseng Lee

    Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Kai Zinn

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6706-5605
  10. Michelle N Arbeitman

    Biomedical Sciences, Florida State University, Tallahassee, United States
    For correspondence
    michelle.arbeitman@med.fsu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2437-4352

Funding

National Institutes of Health (R01 grant number R01GM073039)

  • Savannah G Brovero
  • Julia C Fortier
  • Hongru Hu
  • Pamela C Lovejoy
  • Nicole R Newell
  • Colleen M Palmateer
  • Ruei-Ying Tzeng
  • Michelle N Arbeitman

National Institutes of Health (R03 grant number R03NS090184)

  • Ruei-Ying Tzeng

National Institutes of Health (R01 grant number R01GM073039)

  • Michelle N Arbeitman

Florida State University (R01 grant number Biomedical Sciences)

  • Hongru Hu
  • Pamela C Lovejoy
  • Nicole R Newell
  • Colleen M Palmateer

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

Reviewing Editor

  1. Michael B Eisen, University of California, Berkeley, United States

Version history

  1. Received: September 17, 2020
  2. Accepted: February 22, 2021
  3. Accepted Manuscript published: February 22, 2021 (version 1)
  4. Version of Record published: March 18, 2021 (version 2)

Copyright

© 2021, Brovero 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. Savannah G Brovero
  2. Julia C Fortier
  3. Hongru Hu
  4. Pamela C Lovejoy
  5. Nicole R Newell
  6. Colleen M Palmateer
  7. Ruei-Ying Tzeng
  8. Pei-Tseng Lee
  9. Kai Zinn
  10. Michelle N Arbeitman
(2021)
Investigation of Drosophila fruitless neurons that express Dpr/DIP cell adhesion molecules
eLife 10:e63101.
https://doi.org/10.7554/eLife.63101

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