Interplay between axonal Wnt5-Vang and dendritic Wnt5-Drl/Ryk signaling controls glomerular patterning in the Drosophila antennal lobe

Abstract

<jats:p>Despite the importance of dendritic targeting in neural circuit assembly, the mechanisms by which it is controlled still remain incompletely understood. We previously showed that in the developing Drosophila antennal lobe, the Wnt5 protein forms a gradient that directs the ~45° rotation of a cluster of projection neuron (PN) dendrites, including the adjacent DA1 and VA1d dendrites. We report here that the Van Gogh (Vang) transmembrane planar cell polarity (PCP) protein is required for the rotation of the DA1/VA1d dendritic pair. Cell type-specific rescue and mosaic analyses showed that Vang functions in the olfactory receptor neurons (ORNs), suggesting a codependence of ORN axonal and PN dendritic targeting. Loss of Vang suppressed the repulsion of the VA1d dendrites by Wnt5, indicating that Wnt5 signals through Vang to direct the rotation of the DA1 and VA1d glomeruli. We observed that the Derailed (Drl)/Ryk atypical receptor tyrosine kinase is also required for the rotation of the DA1/VA1d dendritic pair. Antibody staining showed that Drl/Ryk is much more highly expressed by the DA1 dendrites than the adjacent VA1d dendrites. Mosaic and epistatic analyses showed that Drl/Ryk specifically functions in the DA1 dendrites in which it antagonizes the Wnt5-Vang repulsion and mediates the migration of the DA1 glomerulus towards Wnt5. Thus, the nascent DA1 and VA1d glomeruli appear to exhibit Drl/Ryk-dependent biphasic responses to Wnt5. Our work shows that the final patterning of the fly olfactory map is the result of an interplay between ORN axons and PN dendrites, wherein converging pre- and postsynaptic processes contribute key Wnt5 signaling components, allowing Wnt5 to orient the rotation of nascent synapses through a PCP mechanism.</jats:p>

The effect ofDrosophila attP40background on the glomerular organization of Or47b olfactory receptor neurons

“…One of the most peculiar observations from our study is that Or47b ORNs seem to be particularly sensitive to changes in genetic background. In fact, VA1v glomerular disruptions are not only restricted to the attP40 background, but can be seen in many other mutants with effects on ORN axon and synapse organization in the antennal lobes (ANG et al 2003;YAO et al 2007;HONG et al 2012;LI et al 2013;HUESTON et al 2016;WU et al 2017;XIE et al 2019;HING et al 2020). In addition to the variability of VA1v glomerular architecture to genetic background effects, pheromone sensing Or47b ORNs and the trichoid at4 sensillum that houses Or47b, Or88a, and Or65a/b/c ORNs are developmentally special.…”