Adaptation of pineal expressed teleost exo-rod opsin to non-image forming photoreception through enhanced Meta II decay

• Published in: Cellular and molecular life sciences : CMLS 2011-11, Vol.68 (22), p.3713-3723
• Main Authors: Tarttelin, Emma E., Fransen, Maikel P., Edwards, Patricia C., Hankins, Mark W., Schertler, Gebhard F. X., Vogel, Reiner, Lucas, Robert J., Bellingham, James
• Format: Article
• Language: English
• Subjects: Actinopterygii; Adaptation; Adaptation, Physiological; Animals; Biochemistry; Biological Evolution; Biomedical and Life Sciences; Biomedicine; Brackish; Cell Biology; Circadian rhythm; Danio rerio; Fish; Fugu; GTP-Binding Proteins - metabolism; Life Sciences; Marine; Molecular biology; Opsins - chemistry; Opsins - genetics; Opsins - metabolism; Photic Stimulation; Photoreception; Photoreceptor Cells, Vertebrate - cytology; Photoreceptor Cells, Vertebrate - physiology; Pigments; Pineal Gland - chemistry; Research Article; Species diversity; Spectroscopy, Fourier Transform Infrared; Takifugu - anatomy & histology; Takifugu - metabolism; Takifugu rubripes; Teleostei; Vision, Ocular - physiology; Zebrafish - anatomy & histology; Zebrafish - metabolism
• ISSN: 1420-682X; 1420-9071
• DOI: 10.1007/s00018-011-0665-y

Photoreception by vertebrates enables both image-forming vision and non-image-forming responses such as circadian photoentrainment. Over the recent years, distinct non-rod non-cone photopigments have been found to support circadian photoreception in diverse species. By allowing specialization to this sensory task a selective advantage is implied, but the nature of that specialization remains elusive. We have used the presence of distinct rod opsin genes specialized to either image-forming (retinal rod opsin) or non-image-forming (pineal exo-rod opsin) photoreception in ray-finned fish ( Actinopterygii ) to gain a unique insight into this problem. A comparison of biochemical features for these paralogous opsins in two model teleosts, Fugu pufferfish ( Takifugu rubripes ) and zebrafish ( Danio rerio ), reveals striking differences. While spectral sensitivity is largely unaltered by specialization to the pineal environment, in other aspects exo-rod opsins exhibit a behavior that is quite distinct from the cardinal features of the rod opsin family. While they display a similar thermal stability, they show a greater than tenfold reduction in the lifetime of the signaling active Meta II photoproduct. We show that these features reflect structural changes in retinal association domains of helices 3 and 5 but, interestingly, not at either of the two residues known to define these characteristics in cone opsins. Our findings suggest that the requirements of non-image-forming photoreception have lead exo-rod opsin to adopt a characteristic that seemingly favors efficient bleach recovery but not at the expense of absolute sensitivity.