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Abstract
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 ectoderm. We determined in Clytia hemisphaerica that blue-cyan light triggers spawning in isolated gonads. A candidate opsin (Opsin9) was found co-expressed with MIH within specialised ectodermal cells. Opsin9 knockout jellyfish generated by CRISPR/Cas9 failed to undergo oocyte maturation and spawning, a phenotype reversible by synthetic MIH. Gamete maturation and release in Clytia is thus regulated by gonadal photosensory-neurosecretory cells that secrete MIH in response to light via Opsin9. Similar 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.
Highlights
Integration of environmental light information contributes to tight coordination of gamete release in a wide range of animal species
maturation-inducing neuropeptide hormones (MIHs) release in Clytia gonads is triggered by a light cue after a minimum dark period of 1–2 hr, with mature eggs being released two hours later (Amiel et al, 2010)
Comparison of neuropeptide involvement in hydrozoan, starfish, fish and frog reproduction suggested an evolutionary scenario in which gamete maturation and release in ancient metazoans was triggered by gonad neurosecretory cells (Takeda et al, 2018)
Summary
Integration of environmental light information contributes to tight coordination of gamete release in a wide range of animal species. Members of Hydrozoa, a subgroup of Cnidaria which can have medusae or polyps as the sexual form, commonly display light-regulated sexual reproduction (Leclere et al, 2016; Siebert and Juliano, 2017). They have simple gonads in which the germ cells are sandwiched between ectoderm and endoderm, and unlike many other animals they lack additional layers of somatic follicle cells surrounding oocytes in the female (Deguchi et al, 2011).
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