The photoreceptive and neuroendocrine pineal organ of Atlantic salmon.

Daily and seasonal variations in the periodicity of sunlight are one of the most important cues about the external environment, and nonvisual photoreception is essential for registration and correct timing of many biological processes. Atlantic salmon (Salmo salar) is a species where life history transitions are controlled by seasonal changes in light periodicity. In teleost, the pineal organ is photosensitive and produces melatonin, however, the diversity of photoreceptors, their organization and which opsin is responsible for the photic regulation of melatonin synthesis have got little attention in salmon. Based on RNA sequencing and histological profiling of the Atlantic salmon pineal, this study provides an extensive topographic mapping of several nonvisual opsins of the alevin and parr pineal organ in combination with melatonin synthesizing enzymes arylakylamine N-acetyltransferase (aanat2) and N-acetylserotonin O-methyltransferase (asmt). The results show that exorhodopsin (exorh) expressing cells constitute the vast majority of photoreceptors in the pineal organ. These cell types also contain expression of melatonin synthesizing enzymes and are therefore a main regulator of melatonin synthesis in Atlantic salmon, while parapinopsin b (ppb) most likely has an accessory role in the photic regulation of melatonin synthesis. The majority of the nonvisual photoreceptors are located towards the pineal lumen with their outer segment protruding into this, while ppb is located more centrally in the epithelium. Retinal G-protein coupled receptor (rgr) is expressed in a vast majority of the photoreceptors and is localized together with other opsins like exorh, suggesting a photoisomerase function for this opsin. In addition, for the first time, peropsin is characterized in the ciliated choroid plexus cells, suggesting the presence of photoreceptive activity in this cerebrospinal fluid producing organ. Overall, expression analysis clearly indicates that the pineal organ is multi-photoreceptive and that melatonin synthesis is linked to photoreceptors expressing exorh.