Functional Characterization of Teleost Intrinsic Photosensitive Dermal Chromatophores

Abstract

Mammalians process their photoreceptions through lateral eyes; however, non-mammalian vertebrates and invertebrates possess additional extraretinal photoreceptors over their bodies to detect light stimuli. Chromatophores, i.e. dermal specialized pigment cells, play important roles in the regulation of body patterns. Since chromatophores derive from neural crest, they share the common embryonic origin with retina. Recent evidence shows that they are light-sensitive due to opsin expression. In the present study, the expression of seven cone opsins was detected in tilapia caudal fin tissues. Moreover, distinct photoresponses were found in two chromatophore types. Regardless of stimulating wavelengths, melanophores tend to disperse and maintain cell shape at dispersion stage by shuttling pigment granules. Conversely, erythrophores respond to light in a wavelength-dependent manner. The opsin expression profiles of melanophores and erythrophores imply SWS1 and RH2 group genes may play important roles in chromatophore photoresponses. Through measuring photosensitivity, I suggest the two opsins play opposite roles in light-induced translocations of pigment granules within erythrophores: SWS1 for aggregations at UV and short wavelength regions and RH2b for dispersion in middle/long wavelengths. An antagonistic interaction occurs in the overlapping of the absorbance spectra of the two opsins. I also found that the photoresponses take place along with the occurrence of the change of cell membrane potential. In addition, the effect of different light backgrounds (broad spectrum, short wavelength-rich, and red-shifted light conditions) on the photosensitivity of tilapia erythrophores was investigated. I found that the major opsin classes (SWS1 and RH2b) responsible for photoresponses remain constant in three groups of erythrophores. Together, I postulate that melanophores may serve as a light filter in integumentary tissues, and the chromatically antagonistic mechanism enables tilapia erythrophores to sense the subtle change of environmental photic condition and to fine-tune pigmentation. I also investigated the ontogenetic change of photoresponses of rainbow trout melanophores. Distinct photoresponses were found in parrs and smolts. Furthermore, smolt melanophores responded to light in a wavelength-dependent manner. Since the change of coloration and visual system during smoltification of salmonids is regulated by thyroid hormone (TH), I suggest that the development of melanophore photosensitivity is associated to TH as well.