Recognition of environmental cues is essential for the survival of all organisms. Precise transcriptional changes occur to enable the generation and function of the neural circuits underlying sensory perception. To gain insight into these changes, we generated single-cell transcriptomes of Drosophila olfactory receptor neurons (ORNs), thermosensory and hygrosensory neurons from the third antennal segment at an early developmental and adult stage. We discovered that ORNs maintain expression of the same olfactory receptors across development. Using these receptors and computational approaches, we matched transcriptomic clusters corresponding to anatomically and physiologically defined neuronal types across multiple developmental stages. Cell-type-specific transcriptomes, in part, reflected axon trajectory choices in early development and sensory modality in adults. Our analysis also uncovered type-specific and broadly expressed genes that could modulate adult sensory responses. Collectively, our data reveal important transcriptomic features of sensory neuron biology and provides a resource for future studies of their development and physiology.

https://www.biorxiv.org/content/biorxiv/early/2020/10/09/2020.10.08.332130.full.pdf

Single-cell transcriptomes of developing and adult olfactory receptor neurons in Drosophila

The regulatory mechanisms by which neurons coordinate their physiology and connectivity are not well understood The Drosophila olfactory receptor neurons (ORNs) provide an excellent system to investigate this question Each ORN type expresses a unique olfactory receptor or a combination thereof, and sends their axons to a stereotyped glomerulus Using single-cell RNA-sequencing, we identified 33 transcriptomic clusters for ORNs and mapped 20 to their glomerular types, demonstrating that transcriptomic clusters correspond well with anatomically and physiologically defined ORN types Each ORN type expresses hundreds of transcription factors Transcriptome-instructed genetic analyses revealed that 1) one broadly expressed transcription factor (Acj6) only regulates olfactory receptor expression in one ORN type and only wiring specificity in another type; 2) one type-restricted transcription factor (Forkhead) only regulates receptor expression; and 3) another type-restricted transcription factor (Unplugged) regulates both events Thus, ORNs utilize diverse strategies and complex regulatory networks to coordinate their physiology and connectivity

Single-Cell Transcriptomes Reveal Diverse Regulatory Strategies for Olfactory Receptor Expression and Axon Targeting

Neurons undergo substantial morphological and functional changes during development to form precise synaptic connections and acquire specific physiological features. What are the underlying transcriptomic bases? Here, we obtained the single-cell transcriptomes of Drosophila olfactory projection neurons (PNs) at four developmental stages. We decoded the identity of 21 transcriptomic clusters corresponding to 20 PN types and developed methods to match transcriptomic clusters representing the same PN type across development. We discovered that PN transcriptomes reflect unique biological processes unfolding at each stage—neurite growth and pruning during metamorphosis at an early pupal stage; peaked transcriptomic diversity during olfactory circuit assembly at mid-pupal stages; and neuronal signaling in adults. At early developmental stages, PN types with adjacent birth order share similar transcriptomes. Together, our work reveals principles of cellular diversity during brain development and provides a resource for future studies of neural development in PNs and other neuronal types.

Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons

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Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons