(a) Visual pigment interactions in rhabdomeric photoreceptors
Cephalopods present some of the best-studied rhabdomeric photoreceptor systems in terms of microvillar structure within the retina and structure of the visual pigment. In fact, rhodopsin from the squid Todarodes pacificus is only the second opsin, and the single non-vertebrate opsin, to have been crystallized [50]. Early studies of cephalopod photoreceptor structure reveal that the microvilli contain a cytoplasmic core bundle of actin filaments with crossbridges to the membranes, as well as special membrane junctions linking adjoining microvilli [53]. Microvillar actin cores have also been characterized in Drosophila and crayfish rhabdoms [54,55]. The observed actin cores and the core-to-membrane crossbridges fit with the idea from studies of Drosophila phototransduction of a ‘signalplex’—a macromolecular complex linking the visual pigment and associated phototransduction proteins with the cytoskeleton (figure 3; for review see [56]). Although these protein cross-microvillar and cytoskeletal interactions have been studied in very few invertebrate species, together they suggest a highly structured mechanism for increasing the ordering of chromophore alignment.
In conjunction with these studies, evolutionary studies of expressed opsin genes in stomatopod crustaceans have provided some tantalizing evidence that higher order protein interactions may be a common feature of rhabdomeric photoreceptors. In most arthropod visual systems, the photoreceptors that detect polarized light express visual pigments that are also expressed in photoreceptors devoted to the task of colour discrimination. However, in some stomatopod crustacean visual systems, these two tasks have been de-coupled, with the photoreceptors specialized for polarized light detection expressing different opsin genes than those optimized for colour discrimination [57]. This allows for the comparison of opsin gene sequences from photoreceptors devoted to different tasks, with the goal of elucidating specific mechanisms within the opsin protein that may contribute to PS. Preliminary studies indicate that the genes expressed in polarization-sensitive photoreceptors are evolutionarily distinct from those in colour-sensitive photoreceptors (figure 4). Furthermore, comparative evolutionary analyses have identified a set of amino acids that are diversifying among stomatopod opsins that are likely to interact with machinery inside the cell, either in the phototransduction system or with cytoskeletal elements similar to the Drosophila signalplex [58].
In addition to these hypothetical protein/cytoskeleton interactions, Murakami & Kouyama’s [50] crystallization study of squid rhodopsin suggested several protein-protein interactions among visual pigments. First, squid visual pigments are thought to form dimers in the membrane. Second, Murakami & Kouyama [50] also found a tight association across microvillar membranes between the amino-terminal polypeptides of neighbouring monomers, which is suggested to play a role in the hexagonal packing of the microvilli. In fact, these authors suggested that the across-membrane protein-protein interactions may be stronger than the dimer interactions within the membrane. This is one of the first indications that visual pigments could have protein-protein contacts across adjacent microvillar membranes. These proposed protein-protein interactions within and across membranes form a tetrameric structure in which four chromophores are oriented in a nearly parallel arrangement, and they may also play a role in the highly parallel ordering of microvilli needed for polarized light detection.
Functioning either individually or in combination, these visual pigment protein-protein and protein-cytoskeletal interactions observed in Drosophila and cephalopods, and suggested in stomatopods, may provide a rigid organization of visual pigment molecules that contributes to PS by ordering and aligning the chromophores parallel to the axis of the microvillus. However, these studies represent a very limited sampling of invertebrate diversity. Much more research on the interactions among visual pigments and cytoskeletal elements from animals containing rhabdomeric photoreceptors is needed.