Coexpression of three opsins in cone photoreceptors of the salamander Ambystoma tigrinum

• Published in: Journal of comparative neurology (1911) 2014-07, Vol.522 (10), p.2249-2265
• Main Authors: Isayama, Tomoki, Chen, Ying, Kono, Masahiro, Fabre, Eduard, Slavsky, Michael, DeGrip, Willem J., Ma, Jian-Xing, Crouch, Rosalie K., Makino, Clint L.
• Format: Article
• Language: English
• Subjects: Ambystoma - anatomy & histology; Ambystoma - growth & development; Ambystoma - physiology; Ambystoma tigrinum; Animals; Caudata; electrophysiology; immunocytochemistry; Immunohistochemistry; Microelectrodes; Opsins - metabolism; Photic Stimulation; phototransduction; retina; Retinal Cone Photoreceptor Cells - cytology; Retinal Cone Photoreceptor Cells - physiology; Retinal Pigments; Retinal Rod Photoreceptor Cells - cytology; Retinal Rod Photoreceptor Cells - physiology; Ultraviolet Rays; Vision, Ocular - physiology; visual pigment
• ISSN: 0021-9967; 1096-9861
• DOI: 10.1002/cne.23531

ABSTRACT Although more than one type of visual opsin is present in the retina of most vertebrates, it was thought that each type of photoreceptor expresses only one opsin. However, evidence has accumulated that some photoreceptors contain more than one opsin, in many cases as a result of a developmental transition from the expression of one opsin to another. The salamander UV‐sensitive (UV) cone is particularly notable because it contains three opsins (Makino and Dodd [1996] J Gen Physiol 108:27–34). Two opsin types are expressed at levels more than 100 times lower than the level of the primary opsin. Here, immunohistochemical experiments identified the primary component as a UV cone opsin and the two minor components as the short wavelength‐sensitive (S) and long wavelength‐sensitive (L) cone opsins. Based on single‐cell recordings of 156 photoreceptors, the presence of three components in UV cones of hatchlings and terrestrial adults ruled out a developmental transition. There was no evidence for multiple opsin types within rods or S cones, but immunohistochemistry and partial bleaching in conjunction with single‐cell recording revealed that both single and double L cones contained low levels of short wavelength‐sensitive pigments in addition to the main L visual pigment. These results raise the possibility that coexpression of multiple opsins in other vertebrates was overlooked because a minor component absorbing at short wavelengths was masked by the main visual pigment or because the expression level of a component absorbing at long wavelengths was exceedingly low. J. Comp. Neurol. 522:2249–2265, 2014. © 2013 Wiley Periodicals, Inc. Single‐cell recording and immunohistochemistry reveal that some cones from the tiger salamander contain three different opsins. UV‐sensitive cones express three opsins early after hatching, through mature aquatic life, and after metamorphosis to the adult terrestrial form, suggesting an as yet undiscovered function for such a unique pattern of expression.