PUBLICATION

Color opponency with a single kind of bistable opsin in the zebrafish pineal organ

Authors
Wada, S., Shen, B., Kawano-Yamashita, E., Nagata, T., Hibi, M., Tamotsu, S., Koyanagi, M., Terakita, A.
ID
ZDB-PUB-181017-3
Date
2018
Source
Proceedings of the National Academy of Sciences of the United States of America   115(44): 11310-11315 (Journal)
Registered Authors
Hibi, Masahiko
Keywords
UV-sensitive opsin, bistable opsin, color opponency, molecular evolution, pineal organ
MeSH Terms
  • Animals
  • Color
  • Color Vision/physiology*
  • Fish Proteins/metabolism
  • Light
  • Pineal Gland/metabolism
  • Pineal Gland/physiology*
  • Retinal Cone Photoreceptor Cells/metabolism
  • Retinal Cone Photoreceptor Cells/physiology
  • Rod Opsins/metabolism
  • Rod Opsins/physiology*
  • Ultraviolet Rays
  • Zebrafish/metabolism
  • Zebrafish/physiology*
PubMed
30322939 Full text @ Proc. Natl. Acad. Sci. USA
Abstract
Lower vertebrate pineal organs discriminate UV and visible light. Such color discrimination is typically considered to arise from antagonism between two or more spectrally distinct opsins, as, e.g., human cone-based color vision relies on antagonistic relationships between signals produced by red-, green-, and blue-cone opsins. Photosensitive pineal organs contain a bistable opsin (parapinopsin) that forms a signaling-active photoproduct upon UV exposure that may itself be returned to the signaling-inactive "dark" state by longer-wavelength light. Here we show the spectrally distinct parapinopsin states (with antagonistic impacts on signaling) allow this opsin alone to provide the color sensitivity of this organ. By using calcium imaging, we show that single zebrafish pineal photoreceptors held under a background light show responses of opposite signs to UV and visible light. Both such responses are deficient in zebrafish lacking parapinopsin. Expressing a UV-sensitive cone opsin in place of parapinopsin recovers UV responses but not color opponency. Changes in the spectral composition of white light toward enhanced UV or visible wavelengths respectively increased vs. decreased calcium signal in parapinopsin-sufficient but not parapinopsin-deficient photoreceptors. These data reveal color opponency from a single kind of bistable opsin establishing an equilibrium-like mixture of the two states with different signaling abilities whose fractional concentrations are defined by the spectral composition of incident light. As vertebrate visual color opsins evolved from a bistable opsin, these findings suggest that color opponency involving a single kind of bistable opsin might have been a prototype of vertebrate color opponency.
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