Abstract
BackgroundA number of non-visual responses to light in vertebrates, such as circadian rhythm control and pupillary light reflex, are mediated by melanopsins, G-protein coupled membrane receptors, conjugated to a retinal chromophore. In non-mammalian vertebrates, melanopsin expression is variable within the retina and extra-ocular tissues. Two paralog melanopsin genes were classified in vertebrates, Opn4x and Opn4m. Snakes are highly diversified vertebrates with a wide range of daily activity patterns, which raises questions about differences in structure, function and expression pattern of their melanopsin genes. In this study, we analyzed the melanopsin genes expressed in the retinas of 18 snake species from three families (Viperidae, Elapidae, and Colubridae), and also investigated extra-retinal tissue expression.ResultsPhylogenetic analysis revealed that the amplified gene belongs to the Opn4x group, and no expression of the Opn4m was found. The same paralog is expressed in the iris, but no extra-ocular expression was detected. Molecular evolutionary analysis indicated that melanopsins are evolving primarily under strong purifying selection, although lower evolutionary constraint was detected in snake lineages (ω = 0.2), compared to non-snake Opn4x and Opn4m (ω = 0.1). Statistical analysis of selective constraint suggests that snake phylogenetic relationships have driven stronger effects on melanopsin evolution, than the species activity pattern. In situ hybridization revealed the presence of melanopsin within cells in the outer and inner nuclear layers, in the ganglion cell layer, and intense labeling in the optic nerve.ConclusionsThe loss of the Opn4m gene and extra-ocular photosensitive tissues in snakes may be associated with a prolonged nocturnal/mesopic bottleneck in the early history of snake evolution. The presence of melanopsin-containing cells in all retinal nuclear layers indicates a globally photosensitive retina, and the expression in classic photoreceptor cells suggest a regionalized co-expression of melanopsin and visual opsins.
Highlights
A number of non-visual responses to light in vertebrates, such as circadian rhythm control and pupillary light reflex, are mediated by melanopsins, G-protein coupled membrane receptors, conjugated to a retinal chromophore
Studies with knockout mice models revealed the role of this photopigment in the circadian rhythm control [13,14,15,16] and following studies showed that melanopsins are responsible for other non-visual responses to light, such as pupillary light reflex, melatonin suppression, and skin color changes [17,18,19,20,21,22,23,24,25,26,27]
Gene identification and phylogenetic position of melanopsin of snakes Partial sequences of the melanopsin gene (~ 1400 bp) of 18 snake species (Additional file 1: Table S1) were successfully amplified with the primers designed based on snake melanopsin sequences
Summary
A number of non-visual responses to light in vertebrates, such as circadian rhythm control and pupillary light reflex, are mediated by melanopsins, G-protein coupled membrane receptors, conjugated to a retinal chromophore. We analyzed the melanopsin genes expressed in the retinas of 18 snake species from three families (Viperidae, Elapidae, and Colubridae), and investigated extra-retinal tissue expression For their survival, animals depend on the ability to capture and process information from the surrounding environment. Absorption of a photon by the chromophore causes its photoisomerization from 11-cis to all-trans form, which leads to conformational changes of the opsin, allowing a G-protein to bind and activate the phototransduction cascade within the photoreceptor cell [8,9,10] This process leads to the closure or opening of ion channels in the plasma membrane, depending on the photoreceptor cell type, and the photoreceptor’s electrical response to light [11, 12]. Studies with knockout mice models revealed the role of this photopigment in the circadian rhythm control [13,14,15,16] and following studies showed that melanopsins are responsible for other non-visual responses to light, such as pupillary light reflex, melatonin suppression, and skin color changes [17,18,19,20,21,22,23,24,25,26,27]
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