Proprioceptive Opsin Functions in Drosophila Larval Locomotion

Highlights

• Drosophila larval locomotion requires the visual opsins NINAE and Rh6

• NINAE and Rh6 occur in ciliated proprioceptor dendrites along the larval body

• Loss of NINAE or Rh6 impairs proprioceptor function and TRP channel localization

• NINAE and Rh6, though rhabdomeric, contribute to cilium integrity

Summary

Animals rely on mechanosensory feedback from proprioceptors to control locomotory body movements. Unexpectedly, we found that this movement control requires visual opsins. Disrupting the Drosophila opsins NINAE or Rh6 impaired larval locomotion and body contractions, independently of light and vision. Opsins were detected in chordotonal proprioceptors along the larval body, localizing to their ciliated dendrites. Loss of opsins impaired mechanically evoked proprioceptor spiking and cilium ultrastructure. Without NINAE or Rh6, NOMPC mechanotransduction channels leaked from proprioceptor cilia and ciliary Inactive (Iav) channels partly disappeared. Locomotion is shown to require opsins in proprioceptors, and the receptors are found to express the opsin gene Rh7, in addition to ninaE and Rh6. Besides implicating opsins in movement control, this documents roles of non-ciliary, rhabdomeric opsins in cilium organization, providing a model for a key transition in opsin evolution and suggesting that structural roles of rhabdomeric opsins preceded their use for light detection.