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

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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

(2021) Sequencing of methylated GATC DNA fragments (Targeted DamID) from seven olfactory neuron populations in Drosophila melanogaster
ArrayExpress, E-MTAB-8935.

https://www.ebi.ac.uk/arrayexpress/experiments/E-MTAB-8935/

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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.
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.
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.
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.
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.
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.

"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.

Copyright

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.