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This study maps the expression patterns of Beat and Side cell-surface protein families in Drosophila olfactory neurons and their synaptic partners, revealing that each neuron class expresses a unique combination of these genes. While disrupting specific Beat-Side interactions between partner neurons did not affect their ability to find correct targets, the researchers found that Side proteins are important for synapse development. The expression patterns of these genes are conserved across different insect species including ants and mosquitoes, suggesting an evolutionary preserved role in olfactory circuit organization.
Why it matters
Understanding how complex neural circuits wire themselves correctly has implications for developmental neurobiology and could inform strategies for neural repair or addressing neurodevelopmental disorders. The evolutionary conservation across insect species suggests these molecular recognition systems may represent fundamental principles of brain organization.
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by Qichen Duan, Sumie Okuwa, Rachel Estrella, Chun Yeung, Yu-Chieh David Chen, Laura Quintana Rio, Chengcheng Du, Khanh M. Vien, Pelin Cayirlioglu Volkan
Over the past decades, many molecular players have been uncovered to control distinct steps of olfactory circuit assembly in Drosophila. Among these, multi-member gene families encoding cell-surface proteins are of interest as they can act as neuron-specific recognition tags in combinations and contribute to circuit assembly in complex brains. Recently, a multi-protein interactome has been described between Beat and Side families of IgSF proteins. Here, we use newly generated gene trap transgenic driver lines to probe the spatial expression pattern of beat/side genes in olfactory receptor neurons (ORNs) and their synaptic target projection neurons (PNs). Our results revealed that each ORN/PN class expresses a specific combination of beat/side genes, hierarchically regulated by lineage-specific genetic programs. To explore whether the class-specific expression of beats/sides defines ORN-PN matching specificity, we perturbed presynaptic beat-IIa and postsynaptic side-IV in two ORN-PN partners. However, disruption of Beat-IIa-Side-IV interaction did not produce any significant mistargeting in these two examined glomeruli. Our expression mapping revealed that the Beat/Side interactome between ORNs and PNs appears to be error-tolerant, supporting the robust trans-synaptic recognition. Though without affecting general glomerular targeting, knockdown of side in ORNs leads to the reduction of synaptic development. Interestingly, we found conserved expression patterns of beat/side orthologs across ORNs in ants and mosquitoes, indicating the shared regulatory strategies specifying the expression of these duplicated paralogs in insect evolution. This also implies the biological significance of beats/sides in ORN circuit development or function, which is preserved under selective pressure across divergent insect lineages. Overall, this comprehensive analysis of expression patterns lays a foundation for in-depth functional investigations into how Beat/Side combinatorial expression contributes to the olfactory circuit assembly.