Targeted molecular profiling of rare olfactory sensory neurons identifies fate, wiring and functional determinants

  1. J Roman Arguello
  2. Liliane Abuin
  3. Jan Armida
  4. Kaan Mika
  5. Phing Chian Chai
  6. Richard Benton  Is a corresponding author
  1. University of Lausanne, Switzerland

Abstract

Determining the molecular properties of neurons is essential to understand their development, function and evolution. Using Targeted DamID (TaDa), we characterize RNA polymerase II occupancy and chromatin accessibility in selected Ionotropic receptor (Ir)-expressing olfactory sensory neurons in Drosophila. Although individual populations represent a minute fraction of cells, TaDa is sufficiently sensitive and specific to identify the expected receptor genes. Unique Ir expression is not consistently associated with differences in chromatin accessibility, but rather to distinct transcription factor profiles. Genes that are heterogeneously-expressed across populations are enriched for neurodevelopmental factors, and we identify functions for the POU-domain protein Pdm3 as a genetic switch of Ir neuron fate, and the atypical cadherin Flamingo in segregation of neurons into discrete glomeruli. Together this study reveals the effectiveness of TaDa in profiling rare neural populations, identifies new roles for a transcription factor and a neuronal guidance molecule, and provides valuable datasets for future exploration.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files, or in data repositories as specified in the corresponding methods section.

The following data sets were generated

Article and author information

Author details

  1. J Roman Arguello

    Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. 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.
  3. Jan Armida

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

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

    Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  6. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4305-8301

Funding

Novartis Institutes for BioMedical Research (12A14)

  • J Roman Arguello

FP7 Ideas: European Research Council (615094)

  • Richard Benton

H2020 European Research Council (833548)

  • Richard Benton

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (310030B 185377)

  • Richard Benton

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: September 11, 2020
  2. Accepted: March 4, 2021
  3. Accepted Manuscript published: March 5, 2021 (version 1)
  4. Version of Record published: March 25, 2021 (version 2)

Copyright

© 2021, Arguello 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. J Roman Arguello
  2. Liliane Abuin
  3. Jan Armida
  4. Kaan Mika
  5. Phing Chian Chai
  6. Richard Benton
(2021)
Targeted molecular profiling of rare olfactory sensory neurons identifies fate, wiring and functional determinants
eLife 10:e63036.
https://doi.org/10.7554/eLife.63036
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