Transcriptional profiling of olfactory system development identifies distal antenna as a regulator of subset of neuronal fates

Abstract

Drosophila uses 50 different olfactory receptor neuron (ORN) classes that are clustered within distinct sensilla subtypes to decipher their chemical environment. Each sensilla subtype houses 1–4 ORN identities that arise through asymmetric divisions of a single sensory organ precursor (SOP). Despite a number of mutational studies investigating the regulation of ORN development, a majority of the transcriptional programs that lead to the different ORN classes in the developing olfactory system are unknown. Here we use transcriptional profiling across the time series of antennal development to identify novel transcriptional programs governing the differentiation of ORNs. We surveyed four critical developmental stages of the olfactory system: 3rd instar larval (prepatterning), 8 hours after puparium formation (APF, SOP selection), 40 hrs APF (neurogenesis), and adult antennae. We focused on the expression profiles of olfactory receptor genes and transcription factors—the two main classes of genes that regulate the sensory identity of ORNs. We identify distinct clusters of genes that have overlapping temporal expression profiles suggesting they have a key role during olfactory system development. We show that the expression of the transcription factor distal antenna (dan) is highly similar to other prepatterning factors and is required for the expression of a subset of ORs.

Combinations of DIPs and Dprs control organization of olfactory receptor neuron terminals in Drosophila

“…To identify candidate genes that may be involved in the establishment of 50 class specific glomeruli, we analyzed our previously reported antennal transcriptome data from four stages of development: 3 rd instar larval antennal discs (3L), 8 hrs after puparium formation (APF) antennal discs (p8), 40 hrs APF antennae (p40) and adult antennae (Adult) [ 33 , 34 ]. Axon guidance, glomerular sorting, and ORN-PN matching are inherently temporal processes that occur in a specific developmental order [ 8 ].…”

Patterns of transcriptional parallelism and variation in the developing olfactory system of Drosophila species

“…Nevertheless, recent years have revealed the general logic and some of the molecular and developmental events generating the diversity of ORN fates and OR gene regulation in D. melanogaster 15 – 17 , 20 . Thus, limiting our developmental analysis to TFs that have previously been identified as regulating ORN development 15 – 17 , 20 , 26 , 27 , we looked for differences in flexibility among TFs by comparing transcriptional variation, again using the pairwise interspecies ALFC values, for each TF across the three developmental time points. Similar to our adult analysis, we plotted the results both as a boxplot combining all pairwise comparisons and as a heatmap showing each interspecies comparison separately.…”

“…As for our ap manipulations, we used UAS- ap driven by rn- Gal4 on the same Or22a -mCD8GFP promoter-fusion background 15 . Dan mutant heterozygous flies were characterized in a previous study 27 .…”

Two types of sensory proliferation patterns underlie the formation of spatially tuned olfactory receptive fields in the cockroach Periplaneta americana

“…In Drosophila , distal antenna ( dan ) and distal antenna‐related ( danr ) genes are specifically expressed in the presumptive distal region of the antenna in the imaginal disc, controlling the differentiation of distal antenna structures (Emerald, Curtiss, Mlodzik, & Cohen, ). The expression of dan also regulates the development of a subset of OSN classes, temporally and spatially (Barish, Li, Pan, Soeder, Jones, & Volkan, ). Thus, the development of the antennae and OSNs are well controlled by distal–proximal patterning genes in Drosophila .…”