Evolution and spectral tuning of visual pigments in birds and mammals

Variation in the types and spectral characteristics of visual pigments is a common mechanism for the adaptation of the vertebrate visual system to prevailing light conditions. The extent of this diversity in mammals and birds is discussed in detail in this review, alongside an in-depth consideration of the molecular changes involved. In mammals, a nocturnal stage in early evolution is thought to underlie the reduction in the number of classes of cone visual pigment genes from four to only two, with the secondary loss of one of these genes in many monochromatic nocturnal and marine species. The trichromacy seen in many primates arises from either a polymorphism or duplication of one of these genes. In contrast, birds have retained the four ancestral cone visual pigment genes, with a generally conserved expression in either single or double cone classes. The loss of sensitivity to ultraviolet (UV) irradiation is a feature of both mammalian and avian visual evolution, with UV sensitivity retained among mammals by only a subset of rodents and marsupials. Where it is found in birds, it is not ancestral but newly acquired.     

Reconstitution of ancestral green visual pigments of zebrafish and molecular mechanism of their spectral differentiation

We previously reported that zebrafish have four tandemly duplicated green (RH2) opsin genes (RH2-1, RH2-2, RH2-3, and RH2-4). Absorption spectra vary widely among the four photopigments reconstituted with 11-cis retinal, with their peak absorption spectra (lambda(max)) being 467, 476, 488, and 505 nm, respectively. In this study, we inferred the ancestral amino acid (aa) sequences of the zebrafish RH2 opsins by likelihood-based Bayesian statistics and reconstituted the ancestral opsins by site-directed mutagenesis. The ancestral pigment (A1) to the four zebrafish RH2 pigments and that (A3) to RH2-3 and RH2-4 showed lambda(max) at 506 nm, while that (A2) to RH2-1 and RH2-2 showed a lambda(max) at 474 nm, indicating that a spectral shift had occurred toward the shorter wavelength on the evolutionary lineages A1 to A2 by 32 nm, A2 to RH2-1 by 7 nm, and A3 to RH2-3 by 18 nm. Pigment chimeras and site-directed mutagenesis revealed a large contribution (approximately 15 nm) of glutamic acid to glutamine substitution at residue 122 (E122Q) to the A1 to A2 and A3 to RH2-3 spectral shifts. However, the remaining spectral differences appeared to result from complex interactive effects of a number of aa replacements, each of which has only a minor spectral contribution (1-3 nm). The four zebrafish RH2 pigments cover nearly an entire range of lambda(max) distribution among vertebrate RH2 pigments and provide an excellent model to study spectral tuning mechanisms of RH2 in vertebrates.     

Evolution of vertebrate retinal photoreception

Recent findings shed light on the steps underlying the evolution of vertebrate photoreceptors and retina. Vertebrate ciliary photoreceptors are not as wholly distinct from invertebrate rhabdomeric photoreceptors as is sometimes thought. Recent information on the phylogenies of ciliary and rhabdomeric opsins has helped in constructing the likely routes followed during evolution. Clues to the factors that led the early vertebrate retina to become invaginated can be obtained by combining recent knowledge about the origin of the pathway for dark re-isomerization of retinoids with knowledge of the inability of ciliary opsins to undergo photoreversal, along with consideration of the constraints imposed under the very low light levels in the deep ocean. Investigation of the origin of cell classes in the vertebrate retina provides support for the notion that cones, rods and bipolar cells all originated from a primordial ciliary photoreceptor, whereas ganglion cells, amacrine cells and horizontal cells all originated from rhabdomeric photoreceptors. Knowledge of the molecular differences between cones and rods, together with knowledge of the scotopic signalling pathway, provides an understanding of the evolution of rods and of the rods'' retinal circuitry. Accordingly, it has been possible to propose a plausible scenario for the sequence of evolutionary steps that led to the emergence of vertebrate photoreceptors and retina.     

Molecular mechanism for the initial process of visual excitation. IV. Energy surfaces of visual pigments and photoisomerization mechanism

Using the twisted conformations of the chromophores for visual pigments and intermediates which were theoretically determined in the previous paper, energy surfaces of the pigment at −190‡ C were obtained as functions of the torsional anglesθ _9–10 andθ _11–12 or of the torsional anglesθ _9–10 andθ _13–14. In these calculations, the existence of specific reaction paths between rhodopsin (R) and bathorhodopsin (B), between isorhodopsin I (I) and bathorhodopsin, and between isorhodopsin II (I′) and bathorhodopsin were assumed. It was shown that the total energy surfaces of the excited states had minimaC ₁ atθ _9–10 ∼ −10‡ andθ _11–12 ∼ −80‡,C ₂ atθ _9–10 ∼ −85‡ andθ _11–12 ∼ −5‡, andC ₃ atθ _9–10 ∼ 0‡ andθ _13–14 ∼ −90‡. These minima are considered to correspond to the thermally barrierless common states as denoted by Rosenfeld et al. Using the total energy surfaces in the ground and excited states, the molecular mechanism of the photoisomerization reaction was suggested. Quantum yields for the photoconversions among R, I, I′ and B were related to the rates of vibrational relaxations, radiationless transitions and thermal excitations. Some discussion was made of the temperature effect on the quantum yield. Similar calculations of the energy surfaces were also made at other temperatures where lumirhodopsin or metarhodopsin I is stable. Relative energy levels of the pigments and the intermediates were discussed.     

The evolution of early vertebrate photoreceptors

Meeting the challenge of sampling an ancient aquatic landscape by the early vertebrates was crucial to their survival and would establish a retinal bauplan to be used by all subsequent vertebrate descendents. Image-forming eyes were under tremendous selection pressure and the ability to identify suitable prey and detect potential predators was thought to be one of the major drivers of speciation in the Early Cambrian. Based on the fossil record, we know that hagfishes, lampreys, holocephalans, elasmobranchs and lungfishes occupy critical stages in vertebrate evolution, having remained relatively unchanged over hundreds of millions of years. Now using extant representatives of these ‘living fossils’, we are able to piece together the evolution of vertebrate photoreception. While photoreception in hagfishes appears to be based on light detection and controlling circadian rhythms, rather than image formation, the photoreceptors of lampreys fall into five distinct classes and represent a critical stage in the dichotomy of rods and cones. At least four types of retinal cones sample the visual environment in lampreys mediating photopic (and potentially colour) vision, a sampling strategy retained by lungfishes, some modern teleosts, reptiles and birds. Trichromacy is retained in cartilaginous fishes (at least in batoids and holocephalans), where it is predicted that true scotopic (dim light) vision evolved in the common ancestor of all living gnathostomes. The capacity to discriminate colour and balance the tradeoff between resolution and sensitivity in the early vertebrates was an important driver of eye evolution, where many of the ocular features evolved were retained as vertebrates progressed on to land.     

Constitutive activity of a UV cone opsin

Vertebrate visual pigment proteins contain a conserved carboxylic acid residue in the third transmembrane helix. In rhodopsin, Glu113 serves as a counterion to the positively charged protonated Schiff base formed by 11-cis retinal attached to Lys296. Activation involves breaking of this ion pair. In UV cone pigments, the retinyl Schiff base is unprotonated, and hence such a salt bridge is not present; yet the pigment is inactive in the dark. Mutation of Glu108, which corresponds to rhodopsin's Glu113, to Gln yields a pigment that remains inactive in the dark. The apoproteins of both the wild-type and mutant, however, are constitutively active with the mutant being of significantly higher activity. Thus, one important role for preserving the negatively charged glutamate in the third helix of UV pigments is to maintain a less active opsin in a manner similar to rhodopsin. Ligand binding itself in the absence of a salt bridge is sufficient for deactivation.     

Expression and comparative characterization of Gq-coupled invertebrate visual pigments and melanopsin

A non-visual pigment melanopsin, which is localized in photosensitive retinal ganglion cells and is involved in the circadian photoentrainment and pupillary responses in mammals, is phylogenetically close to the visual pigments of invertebrates, such as insects and cephalopods. Recent studies suggested that melanopsin is a bistable pigment and drives a Gq-mediated signal transduction cascade, like the invertebrate visual pigments. Because detailed electrophysiological properties are somewhat different between the visual cells and the photosensitive ganglion cells, we here expressed and purified the invertebrate visual pigment and melanopsin to comparatively investigate their Gq-activation abilities. We successfully expressed and purified UV and blue light-sensitive visual pigments of the honeybee as well as the amphioxus melanopsin. Although the purified UV-sensitive pigment and the melanopsin lost their bistable nature during purification, reconstitution of the pigments in lipid vesicles resulted in return of the bistable nature. The light-dependent Gq-activation abilities among these reconstituted pigments are similar, suggesting that the electrophysiological differences do not depend on the Gq-activation step but rather on the other signal transduction steps and/or on cell properties. Our findings are also important in that this is the first report describes a heterologous large-scale expression of the Gq-coupled invertebrate visual pigments in cultured cells.     

脊椎动物视蛋白基因分子进化的研究进展

视觉是动物获取外界信息的重要途径,在动物的捕食、配偶选择及讯息传递等方面均有重要作用,对动物的进化具有深远而广泛的影响[1].经过科学家的不懈努力,生态因素被认为是引导视觉系统进化的一个主要因素[1,2].     

Morphological differentiation of the central visual cells R7/8 in various regions of the blowfly eye

The central rhabdomeres in the retina of the blowfly Calliphora erythrocephala and the house fly Musca domestica are not structurally uniform. In Calliphora, four classes of central rhabdomeres were found; they are formed by a total of seven types of central visual cells, clearly distinguished by the following structural features: length of the rhabdomeres R7 or R8, position of the nucleus, rhabdomere twist, fine structure in the R7/R8 transition region, and cross-sectional area of the rhabdomeres. In the lateral part of the eye only the most common central-rhabdomere class, ‘sl.’ is present, whereas in the frontal and dorsal parts classes ‘sl’ and ‘ls’ are found in a particular numerical ratio. Near the frontal eye margin the rare class ‘per’ also appears, with two separate rhabdomeres, R7per and R8s; the morphological properties of R7per are midway between those of peripheral and central visual cells. The special ommatidia at the dorsal margin of the eye are characterized by the central rhabdomeres ‘marg’. The known functional properties of the visual cells in the fly eye can be readily assigned to these classes (Table 1, Fig. 12). The non-uniform distribution of the various kinds of central rhabdomeres suggests functional differentiation of the eye region.