Body coloration in many poikilothermic animals is plastic and occurs over multiple timescales (e.g., cuttlefish can change quickly in seconds, certain Arctic animals change over months) [[1], [2], [3]]. The relative quick color change refers to synchronous bidirectional translocation of pigment organelles within chromatophores in the skin (e.g., black melanophores containing melanin, yellow xanthophores containing pteridine, red erythrophores containing carotenoids) [[4], [5], [6]]. In general, quick color change is under visual system-dependent neuromuscular (cephalopods) [7] or neuroendocrine control (most other taxa) [8]. However, an additional recent consideration is that color change may be guided in some species by photoreceptors that are found outside of the eyes [3]. It has been shown that some geckos can change color to match the background when their eyes are covered, but not when their flanks were covered, which seemingly contain opsins [9]. Indeed, several types of opsins have been identified in chromoatophore [10,11], but their functions remain to be illuminated.

Most opsin-based pigments consist of an opsin protein belonging to G protein-coupled receptors (GPCRs), and a light-sensitive retinal chromophore [[12], [13], [14]]. Rhodopsin, the founding member of the opsin family, has long been known to be important for visual function in the eye [15]. The first non-visual opsin was pinopsin, which served as a photoreception in the pineal organs of birds [16]. Since then, several non-visual opsins, e.g. Parapinopsin [17], Vertebrate ancient’ opsin [18], Encephalopsin [19], Melanopsin (Opsin 4) [20], and Neuropsin [21], were identified in animals. The skin is the largest organ exposed to environmental conditions, such as light. The earliest evidence of opsin in the skin is the discovery of melanopsin in Xenopus dermal melanophores [20]. So far, a wide array of opsins had been identified in the skin of human, murine, fish, and cephalopod [[22], [23], [24], [25], [26], [27]]. The function of opsins in chromatophores has gained the most scientific attention. Recent studies in human demonstrated that Opsin 3 and Opsin 5 were involved in the regulation of melanin levels in epidermal melanocytes [26,[28], [29], [30]]. Comprehensive studies in from Castrucci's lab showed that opsins are involved in light radiation-induced several physiological and cellular processes response, such as melanin production, cell death induction, growth and molecular clock modulation [[31], [32], [33], [34], [35], [36]]. Conversely, only a few studies explore the function and mechanism of opsin in regulation of movement of pigment organelles within chromatophores, which remains to be further investigated [11,35,37,38].

The large yellow croaker (Larimichthys crocea) is a common commercial fish in East Asia, ranking at the top of the mariculture fishes in China [39]. As the meaning of its common name, the skin (especial ventral area) of this fish exhibits golden yellow color. However, the ventral skin color of the croaker quickly changes to silvery white in white light environment (in a range of 10–6000 lx, 0.003–1.595 mW/cm2) [40]. Our previous study showed that the yellowness of L. crocea skin was mainly due to dispersion of pigment granules (xanthosomes) in xanthophores [41]. The dispersion of xanthosomes was regulated by melanocyte-stimulating hormone (MSH) that is released both from the pituitary through the endocrine pathway and from the xanthophores through an autocrine pathway. Subsequently, cyclic adenosine monophosphate-protein kinase A (cAMP-PKA) signaling pathway mediated the action of MSH on xanthosomes dispersion. Intriguingly, when the xanthophores were exposed to light in vitro, xanthosomes aggregated [41]. Therefore, we hypothesize that the photosensitive of xanthophores was mediated via opsin-based pigments. In the present study, we defined the wavelengths of the responses well as the signal pathways and cytoskeleton system involved in light-induced xanthosomes aggregation. Based on the transcriptome data of skin, and RT-PCR detection of opsin genes in xanthophore, we further identified and examined the molecular properties of recombinant Opsin 3. Lines of evidence from the present study identified a unique function of Opsin 3 in light-induced body color change in L. crocea.