Nonvisual system-mediated body color change in fish reveals nonvisual function of Opsin 3 in skin

Body-color changes in many poikilothermic animals can occur quickly. This color change is generally initiated by visual system, followed by neuromuscular or neuroendocrine control. We have previously showed that the ventral skin color of the large yellow croaker (Larimichthys crocea) presents golden yellow in dark environment and quickly changes to silvery white in light environment. In the present study, we found that the light-induced whitening of ventral skin color was independent of visual input. Using light-emitting diode sources of different wavelength with same luminance (150 lx) but different absolute irradiance (0.039–0.333 mW/cm2), we further found that the blue light (λmax = 480 nm, 0.107 mW/cm2) is more effectively in induction of whitening of ventral skin color in compare with other light sources. Interestingly, the result of RT-PCR showed opsin 3 transcripts expressed in xanthophores. Recombinant protein of Opsin 3 with 11-cis retinal formed functional blue-sensitive pigment, with an absorption maximum at 468 nm. The HEK293T cells transfected with Opsin 3 showed a blue light-evoked Ca2+ response. Knock-down of Opsin 3 expression blocked the light-induced xanthosomes aggregation in vitro. Moreover, the light-induced xanthosomes aggregation was mediated via Ca2+-PKC and Ca2+-CaMKII pathways, and relied on microtubules and dynein. Decrease of cAMP levels was a prerequisite for xanthosomes aggregation. Our results provide a unique organism model exhibiting light-induced quick body color change, which was independent of visual input but rather rely on non-visual function of Opsin 3 within xanthophore.