Parietal-eye phototransduction components and their potential evolutionary implications

Johns Hopkins University, Baltimore, Maryland, United States
Science (Impact Factor: 33.61). 04/2006; 311(5767):1617-21. DOI: 10.1126/science.1123802
Source: PubMed


The parietal-eye photoreceptor is unique because it has two antagonistic light signaling pathways in the same cell-a hyperpolarizing pathway maximally sensitive to blue light and a depolarizing pathway maximally sensitive to green light. Here, we report the molecular components of these two pathways. We found two opsins in the same cell: the blue-sensitive pinopsin and a previously unidentified green-sensitive opsin, which we name parietopsin. Signaling components included gustducin-alpha and Galphao, but not rod or cone transducin-alpha. Single-cell recordings demonstrated that Go mediates the depolarizing response. Gustducin-alpha resembles transducin-alpha functionally and likely mediates the hyperpolarizing response. The parietopsin-Go signaling pair provides clues about how rod and cone phototransduction might have evolved.

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Available from: Chih-Ying Su,
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    • "Photoreceptors of the parietal eye contain both an S pinopsin and an M parietopsin ( Su et al . , 2006 ) that mediate hyperpolarizing responses to short wavelengths and depolarizing responses to long wavelengths ( Soles - sio and Engbretson , 1993 ) . The two pigments generate opposing responses by coupling to different G proteins ( Su et al . , 2006 ) . In contrast , all visual pigments are thought to couple to the same transducin G protein in salamander cones ( Ma et al . , 2001b ) , and no such response differences were detected within individual salamander cones that expressed multiple pigments . Instead , response waveform was the same for all wave - lengths , in accordance wit"
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    ABSTRACT: Whereas more than one type of visual opsin is present in the retina of most vertebrates, it was thought that each type of photoreceptor expressed 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 a hundred times lower than that 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 co-expression 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., 2013. © 2013 Wiley Periodicals, Inc.
    The Journal of Comparative Neurology 07/2014; 522(10). DOI:10.1002/cne.23531 · 3.23 Impact Factor
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    • "All the lacertid data come from the present study. Other sequences are from various sources: AH007736.1 (Kawamura and Yokoyama, 1996), DQ100325 (Su et al., 2006), AF074045.1 (T. Yuki, H. Osamu, Y. Masao and T. Fumio, unpublished data) and AY024356.1 (Yokoyama and Blow, 2001). "
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    ABSTRACT: Ultraviolet (UV) vision and UV colour patches have been reported in a wide range of taxa and are increasingly appreciated as an integral part of vertebrate visual perception and communication systems. Previous studies with Lacertidae, a lizard family with diverse and complex coloration, have revealed the existence of UV-reflecting patches that may function as social signals. However, confirmation of the signalling role of UV coloration requires demonstrating that the lizards are capable of vision in the UV waveband. Here we use a multidisciplinary approach to characterize the visual sensitivity of a diverse sample of lacertid species. Spectral transmission measurements of the ocular media show that wavelengths down to 300 nm are transmitted in all the species sampled. Four retinal oil droplet types can be identified in the lacertid retina. Two types are pigmented and two are colourless. Fluorescence microscopy reveals that a type of colourless droplet is UV-transmitting and may thus be associated with UV-sensitive cones. DNA sequencing shows that lacertids have a functional SWS1 opsin, very similar at 13 critical sites to that in the presumed ancestral vertebrate (which was UV-sensitive) and other UV-sensitive lizards. Finally, males of Podarcis muralis are capable of discriminating between two views of the same stimulus that differ only in the presence/absence of UV radiance. Taken together, these results provide convergent evidence of UV vision in lacertids, very likely by means of an independent photopigment. Moreover, the presence of four oil droplet types suggests that lacertids have a four-cone colour vision system.
    Journal of Experimental Biology 06/2014; DOI:10.1242/jeb.104281 · 2.90 Impact Factor
    • "These authors suggested that the G o -coupled pathway might be more ancient compared to the gustducin pathway, as it can be traced back to the common ancestor of vertebrates and invertebrate molluscs (coelomates). Parietopsin showed the highest degree of amino acid identity (40 %) to parapinopsin (Su et al. 2006 ) and has been linked to other biological functions that include detecting the spatial orientation of the sun and electromagnetic fi elds (Foa et al. 2009 ; Nishimura et al. 2010 ). "
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    ABSTRACT: In addition to classical image-forming vision, the vertebrates exhibit a range of non-image-forming light detection systems that utilise opsin photopigments. Within the CNS these systems are present in a range of anatomical locations that include both eye and brain. In mammals the eye is both responsible and required for all commonly measured responses to light. By contrast, non-mammalian vertebrates possess a wide range of intrinsically photoreceptive sites. Members of the non-visual opsin family include exorhodopsin, pinopsin, vertebrate ancient opsin (VA), parietopsin, parapinopsin, teleost multiple tissue opsin (TMT), encephalopsin (OPN3), neuropsin (OPN5), peropsin, retinal G protein-coupled receptor (RGR) and melanopsin (OPN4). Opsin-based photopigments have evolved to mediate specific photoreceptive tasks in different light environments, each exhibit functional properties that are tuned to the biological task in which they are involved. Examination of the classes of opsin involved reveals a range of adaptions particularly in spectral sensitivity, chromophore handling and signalling mechanisms. The loss of extraocular light detection in the mammals is associated with an evolutionary reduction in the non-visual opsin representation in the mammalian genome. One clear exception to this is the retention of the melanopsin (OPN4M) gene and the expression of this opsin protein in a single class of mammalian retinal ganglion cell. Exploring the diversity of melanopsin proteins in the lower vertebrates suggests that the property of chromophore biochemistry and bistability does not necessarily define an opsin class and may have evolved more than once.
    Evolution of Visual and Non-visual Pigments, 01/2014: pages 65-103; , ISBN: 978-1-4614-4354-4
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