Innervation directs receptor synthesis and localization in Drosophila embryo synaptogenesis

Abstract

In the Drosophila embryo, motor neurons form stereotyped synapses (neuromuscular junctions) on identified muscles. We have used a mutant (prospero) that removes or delays innervation to assay the role of the presynaptic motor neuron in the development of the receptive field of the postsynaptic muscle. prospero (pros) is not expressed in the muscles or their precursors. Here we find that the muscle defines the correct synaptic zone in the absence of the motor neuron by restricting putative guidance molecules to this specialized membrane region. Furthermore, the muscle expresses functional transmitter receptors at the correct developmental time without innervation. On the other hand, the muscle does not localize receptors to the synapse without instruction from the motor neuron, nor does a second, much larger, synthesis of receptors occur in muscles deprived of innervation. In muscles receiving delayed innervation, or muscles innervated at aberrant synaptic sites, both receptor clustering and receptor synthesis are delayed or redirected, consistent with the new pattern of innervation. We conclude that the muscle autonomously defines the synaptic site, whereas the motor neuron directs the development of the muscle's receptive field by stimulating the synthesis and localization of transmitter receptors.