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.
Highlights
Nervous systems are composed of vast numbers of neuron classes with specific structural and functional characteristics
To test the feasibility of Targeted DamID (TaDa) for profiling Drosophila olfactory sensory neurons (OSNs), we first focused on the Ir64a population, which comprises ~16 neurons that are housed in sensilla in the sacculus, where they detect acidic odors (Ai et al, 2010)
Our study was initially motivated by the desire to test the TaDa method for targeted, genome-wide molecular profiling of very small populations of neurons that are tightly embedded within a highly heterogeneous tissue
Summary
Nervous systems are composed of vast numbers of neuron classes with specific structural and functional characteristics. The Drosophila nose (antenna) contains ~50 classes of olfactory sensory neurons (OSNs), which develop from sensory organ precursor cells specified in the larval antennal imaginal disc (Barish and Volkan, 2015; Jefferis and Hummel, 2006; Yan et al, 2020). Each OSN is characterized by the expression of a unique olfactory receptor (or, occasionally, receptors), of the Odorant Receptor (OR) or Ionotropic Receptor (IR) families These proteins function – together with broadly expressed, family-specific co-receptors – to define neuronal odor-response properties (Benton, 2015; Gomez-Diaz et al, 2018; Robertson, 2019; Rytz et al, 2013).
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