Phototransduction and the evolution of photoreceptors

Abstract

Photoreceptors in metazoans can be grouped into two classes, with their photoreceptive membrane derived either from cilia or microvilli. Both classes use some form of the visual pigment protein opsin, which together with 11-cis retinaldehyde absorbs light and activates a G-protein cascade, resulting in the opening or closing of ion channels. Considerable attention has recently been given to the molecular evolution of the opsins and other photoreceptor proteins; much is also known about transduction in the various photoreceptor types. Here we combine this knowledge in an attempt to understand why certain photoreceptors might have conferred particular selective advantages during evolution. We suggest that microvillar photoreceptors became predominant in most invertebrate species because of their single-photon sensitivity, high temporal resolution, and large dynamic range, and that rods and a duplex retina provided primitive chordates and vertebrates with similar sensitivity and dynamic range, but with a smaller expenditure of ATP.

Figure 1. Phylogenetic tree of metazoans showing only animal groups or species discussed in this review, with photoreceptor types in principal eyes illustrated as ciliary (red) or microvillar (blue)

No attempt has been made to specify relationships among principal groups of bilaterians, since these remain controversial. Cnidarian embryos may have microvillar photoreceptors (see text), and it is likely that both photore-ceptor types were present very early in the evolution of metazoans. Mammals and other vertebrates have ciliary photoreceptors (rods and cones) and do not have photoreceptors with microvilli, but they may use a transduction cascade similar to the one used by microvillar photoreceptors in the intrinsically light-sensitive ganglion cells [16]. Phylogenetic tree is based upon [54,94,99]. Drawings of photoreceptors are from [,,,,,–103].

Figure 2. Opsins: a large family of closely related G-protein receptors that mediate phototransduction in all known metazoans

(A) Crystal structure of bovine rhodopsin with seven transmembrane helical domains labeled with Roman numerals. The carboxyl terminus (above) faces the cytoplasm, the amino terminus (below) the extracellular space (or inside of disk of rod). Linking regions are labeled as C-I, C-II, etc. for cytoplasm and E-I, E-II, etc. for extracellular space (or inside of disk). (B) Lysine in the seventh transmembrane domain of opsin forms a covalent bond with the aldehyde of the chromophore retinal. Light produces a photoisomerization of 11-cis retinal to all-trans retinal and changes the conformation of the rest of the opsin protein, facilitating the binding of G-protein and triggering the phototransduction cascade (Figure 4). Most metazoans use retinal, but 3-dehydroretinal is found in some fresh-water vertebrates, and 3-hydroxyretinal in many insects. (C) Phylogenetic tree of opsins discussed in article; ciliary photoreceptors (red lines) have c-opsins and G₀ opsins, and microvillar (blue lines) have r-opsins. Proteins in these three subfamilies show differences in amino acid sequence that are thought to be responsible for their different properties and interactions with different G proteins. The three different forms of photopigment (and others not shown) diverged very early probably among primitive metazoans. We show only the major branches of opsin families; considerable diversity exists within these families, for example between the different pigments for Drosophila or for SW and LW mammalian cone pigments, and more complete phylogenetic trees showing some of this diversity can be found in references [–8,55], which provided the data for our figure. LW cones absorb light at long wavelengths (green to red); SW cones, in the blue and UV. Note that cone pigments evolved before rod. Structure in (A) reprinted with permission from [104].)

Figure 3. Transduction scheme of microvillar photoreceptor

(A) Microvillar photoreceptor (left) and detail of microvilli with adjacent submicrovillar cisternae (SMCs) containing Ca²⁺ (right). (B) Major proteins and mechanisms in microvillar trans-duction. Schema is based on results from fly. In other species, IP₃-induced Ca²⁺ release from the SMCs (not shown in diagram) is known to make an important contribution to microvillar transduction. Abbreviations: hν, light; Rh*, activated form of the photopigment rhodopsin; G_q, G protein containing α_q subunit; GDP, guanosine diphosphate; GTP, guanosine triphosphate; PLC, phospholipase C; PIP₂, phosphatidylinositol 4,5-bisphosphate; IP₃, inositol 1,4,5-triphosphate; DAG, diacylgly-cerol; PKC, protein kinase C; rER, rough endoplasmic reticulum; NINAC, class III myosin; and INAD, a protein containing PDZ binding domains responsible for forming the signaling complex in a fly microvillus.

Figure 4. The vertebrate rod

(A) Schematic anatomy of representative vertebrate rod. (B) Major proteins and mechanisms in vertebrate rod transduction. Abbreviations: hν, light; Rh*, activated form of the photopigment rhodopsin; GTP, guanosine triphosphate; GDP, guanosine diphosphate; cGMP, guanosine 3′,5′-cyclic monophosphate; GMP, guanosine monophosphate; PDE, guanosine nucleotide phosphodiesterase; RK, rhodopsin kinase; RGS complex, group of three proteins including RGS9 which accelerate the hydrolysis of GTP by the alpha subunit of transducin; and P_i, inorganic phosphate.

Figure 5. Light responses of rods and fly photoreceptors

(A) Comparison of current waveform of light responses to 10 ms light flashes (arrow) of rod (above) and rod bipolar cell (below) from mouse. Light intensities were (for rod) 6.2, 12, and 25 photons/µm²; and for bipolar cell 0.6, 1.2, and 2.5 photons/µm². For both rod and bipolar cell, amplitude increases with increasing light intensity but with little change in kinetics of waveform. The dashed line shows that bipolar cells mostly sum the initial part of the rod response, where variability is smallest [77,78]. Recordings generously provided by A. Sampath (see Figures 2 and 3 of [83]). (B) Quantum-bumps from Drosophila photoreceptor. A two second-long dim light flash (bar: about four effective photons s⁻¹), elicits a train of discrete single photon responses, variable in amplitude but on average about 10 pA. The small (2 pA) events are caused by spontaneous G-protein activation. (C) Superimposed responses from a Drosophila photoreceptor to six 1 ms dim flashes (arrow) each containing only one effective photon. The single photon responses arise abruptly following a finite and variable latency and vary in amplitude. The summed response is consequently much noisier than is the bipolar cell response.