CRISPR/Cas9 Mutation Of A Gonad-Expressed Opsin Prevents Jellyfish Light-Induced Spawning

Across the animal kingdom, environmental light cues are widely involved in regulating gamete release, but the molecular and cellular bases of the photoresponsive mechanisms are poorly understood. In hydrozoan jellyfish, spawning is triggered by dark-light or light-dark transitions acting on the gonad, and is mediated by oocyte maturation-inducing neuropeptide hormones (MIHs) released from the gonad ectoderm. Using the model species Clytia hemisphaerica we determined that blue-cyan light triggers autonomous spawning in isolated gonads. A candidate opsin (Opsin9) identified from gonad transcriptomes was found co-expressed with MIH within specialised ectodermal neural cells. Opsin9 knockout jellyfish generated by CRISPR/Cas9 failed to undergo oocyte maturation and spawning, phenotypes reversible by synthetic MIH. We conclude that gamete maturation and release in Clytia is regulated by gonadal photosensory-neurosecretory cells that secrete MIH in respose to light via Opsin9. Similar photosensitive-neurosecretory cells in ancestral eumetazoans may have allowed tissue-level photo-regulation of diverse behaviours, a feature elaborated in cnidarians in parallel with expansion of the opsin gene family.