Molecular evolution of invertebrate rhodopsins

The analysis of over 60 genes coding for the opsin moiety of invertebrate rhodopsins yields a phylogenetic tree as depicted in Figure 2. Invertebrate rhodopsins are members of the rhodopsin superfamily within the phylogeneti-cally related hyperfamily of G-protein coupled receptors (GPCRs) [19]. DNA sequence data for the protein coding regions of rhodopsin genes have, apart from the information on rhodopsin functions, provided useful data for the molecular taxonomy of hymenopteran insects [20]. Despite the rapidly increasing sequence information yielded by several invertebrate genome projects as well as by the visual system-oriented research focussing on rhodopsin itself, there are still gaps in the knowledge of rhodopsin evolution. A more detailed understanding is likely to be gained if sequence data become available from lower invertebrates. This would allow to link evolution of metazoan rhodopsins more directly to unicellular eucaryotes, for example the evolution of rhodopsin in the green algae Chlamydomonas and Volvox (see Chapter 4).

One gap has recently been narrowed by the cloning of a rhodopsin expressed in the larval eye spot of an "invertebrate" chordate, the tunicate Cionia [21,22]. In phylogenetic trees depicting the evolutionary relationships of rhodopsins on the basis of homologies in their primary structure, Ci-opsinl segregates into a subgroup with the rhodopsins from vertebrates and man to form a new

/ \Helheu , / HelsaV^ Dryiu ' HelpaVlelcy Helme

DromeRh5 ^^ApimeBt SchgrRh2 Manse3 j- PapglRh6 PapxuRh4

DropsRh2 DromeRh2 DropsRhl DrosiRhl. nrosil DromeRh! -f

CalviRhl1 LimpoRhl


HemsaRhl, Rh2 — Camhu^msc DromeRh7

PatyeRhl Octdo

Tod pa



PetmaPi CioinOpsI

HomsaRe. HomsaGr PetmaD DanreUv AstmeBI


Figure 2. Evolutionary relationship of invertebrate rhodopsins. Phylogenetic tree (amino acid sequence) of invertebrate rhodopsins and selected chordate rhodopsins. Included are all invertebrate rhodopsins whose complete amino acid sequence was determined by May 2002. In alphabetical order: abbreviation, species (and name of rhodopsin), accession number: Allsu, Allotheutis subulata, S71931; ApimeLw, Apis mellifera long-wavelength rhodopsin, Q17063; ApimeBl, Apis mellifera blue-sensitive rhodopsin, AAC13415, AAC 47455; ApimeUV, Apis mellifera UV-sensitive rhodopsin, AAC13418; Astme, Astyanax mexicanus blue-sensitive rhodopsin, P51471; CalviRhl, Calliphora vicina opsin Rhl, P22269; Camsc, Cambarellus shufeldtii, 016018; Camhu, Cambarus hubrichti, 018312; Camlu, Cambarus ludovicianus, 016017; Camma, Cambaras maculatus, 01915; Camab, Camponotus abdominalis opsin, Q17292; CamabUV, Camponotus abdominalis UV-sensitive rhodopsin, AAC050920; Catbo, Cataglyphis bombycinus, Q17296; CatboUV, Cataglyphis bombycinus UV-sensitive rhodopsin, AAC05091; CioinOpsI, Cionia intestinalis opsin 1, BAB68391; DanreUV, Danio rerio UV-sensitive rhodopsin; DromeRhl-Rhl, Drosophila melanogaster rhodopsins Rhl-Rh7, P06002, P08099, P04950, P08255, P91657, 001668, AAF49949, resp.; DropsRhl-Rh4, Drosophila pseudoobscura. rhodopsins Rhl-Rh4, P28678, P28679, P28680, P29404, resp.; DrosiRhl, Drosophila simulans rhodopsin Rhl, AAB31030; DrosuRhl, Drosophila subobseura rhodopsin Rhl, AAB87898; DroviRhl, Rh4, Drosophila virilis rhodopsin Rhl, Rh4, AAB31031, 017646, resp.; Dryiu, Dry as iulia, AAK58111; Helcy,

Figure 2. continued

Heliconius cydno, AAK58109; Helhe, Heliconius hewitsoni, AAK58106; Helme, Helicon-ius melpomene, AAK13246; Helpa, Heliconius pachinus, AAK58110; Helsa, Heliconius sapho, AAK58108; Helsa, Heliconius sara, AAK58107; HemsaRhl, Rh2, Hemigrapsus sanguineus compound eye opsins Rhl, Rh2, Q25157, Q25158, resp.; HomsaGr, Homo sapiens green-sensitive rhodopsin, P04001; HomsaRe, Homo sapiens red-sensitive rhod-opsin, P04000; LimpoRhl, Limulus polypemus lateral eye opsin, P35360; LimpoRh2, Limuluspolyphemus ocellar opsin, P35361; Lolsu, Loligo subulata, Q17094; Lolfo, Loligo forbesi, P24603; Mansel-3, Maduca sexta opsin 1-3, AAD11964, AAD11965, AAD11966, resp.; MegviLV, Megoura viciae long-wavelength-like opsin, AAG17119; MegviUV, Megoura viciae UV-wavelength-like opsin, AAG17120; Octdo, Octopus dofleini, P09241; Orcau, Oronectes australis, 018418; Orcvi, Oronectes virilis, 016019; PapglRhl-RH6, Papilio glaueus rhodopsin Rhl-Rh6, AAD34220, AAD34221, AAD29445, AAD34224, AAD34222, AAD34223, resp.; PapxuRhl-Rh5, Papilio xuthus rhodopsin Rhl-RH5, BAA31721, BAA31722, BAA32723, BAA93469, resp.; PatyeRhl, Patinopecten yessoensis rhodopsin Gq-coupled, 015973; PatyeRh2, Patinopecten yessoensis rhodopsin G0-coupled, 015974; PetmaPi, Petromyzon marimus pineal opsin, AAV41240; PetmaD, Petromyzon marimus rhodopsin, Q98980; Procl, Procambarus clarkii, P35356, Proml, Procambarus milleri, 016020; Prose, Procambarus seminolae, 018486; Proor, Procambarus orcinus, 018485; Prose, Procambarus seminolae, 018486; SalsaO, Salmo Salar, ancient opsin, 013018; SchgrRhl, Rh2, Schistocerca gregaria rhodopsin Rhl,Rh2, Q94741, Q26495; Sepof, Sepia officinalis, 016005; Sphsp, Sphodromantis sp., P35362; Todpa, Todarodes pacificus, P31356;

clade for chordates [21] (Figure 2). This clade is distinct from that of mollusc rhodopsins, in particular of cephalopod rhodopsins. The rhodopsins of arthropods, e.g. those of xiphosura {Limulus), crustacea (crabs and crayfish) and a number of insects are clustered into two larger rhodopsin subfamilies which differ in wavelength absorption properties. One clade consists of long wavelength (i.e. yellow, green and blue-green light) absorbing rhodopsins, the other assembles rhodopsins absorbing at shorter wavelengths, i.e. UV and blue light. These two subgroups can be further refined with respect to the spectral tuning of rhodopsin [23-26]. One lesson from such a comparison is that complex visual achievements which rely on rhodopsin divergence, like UV- and colour vision, have evolved independently several times in invertebrates and in vertebrates [26-30],

Figure 2 also depicts two exceptions to the general observation that a rhodopsin segregates with a clade representative for the taxon from which it originated. The outgrouped rhodopsins are PatyeRh2 (SCOP2) [31], a rhodopsin localized to ciliary photoreceptors of the scallop Patinopecten yessoensis, and an orphan rhodopsin, Rh7 of Drosophila melanogaster, with unknown expression pattern and function. The latter was identified by the Drosophila genome project [32], Both rhodopsin homologs cluster in the vicinity of the chordate rhodopsins. What are the determinants in the primary structure of rhodopsins that underlie such a divergence? It has been shown that cytoplasmic and extracellularly located ends of rhodopsin are more variable than the 7 TM regions [33]. The tuning of a rhodopsin s absorption maximum to a given wavelength is apparently based on a number of conserved interactions, particularly between the chromophore and the amino acid side chains within the 7 TM-helices of rhodopsin. Indeed, if one takes into account the tertiary structure of rhodopsin and establishes a phylogenetic tree solely on the basis of sequence homology within the 7 TM helices, a slightly different picture appears: The divergence of rhodopsins is more restricted than observed with the holorhodopsin, and, as expected, PatyeRh2 and DromeRh7 now cluster with subgroups of rhodopsins from molluscs and insects, respectively (Figure 3).

DropsRh2 DromeRh2\ DroviRhl "A DrosiRhl U N


DropsRhV^Rhl CalviRhl ^


PapxuRh3 ■ SchgrRhl PapglRh4

PatyeRhl c/


DropsRh4_ DromeRh4 ** DroviRh4

DropsRh3 -DromeRh3

PapxuRhS PapglRh5

Manse2' / CatboUv

LimpoRhl LimpoRh2

HemsaRhl HemsaRh2






Tod pa

N ApimeBI SchgrRh2

DromeRh7 DromeRhS

Figure 3. Evolutionary relationship of invertebrate rhodopsin transmembrane domains. The amino acid sequences of invertebrate rhodopsins were modified, such that peptides were constructed consisting only of the linked seven transmembrane domains, the C- and the N-terminus as well as intra- and extracellular loops of rhodopsins were removed for that purpose. In the phylogenetic tree of these peptides, Patye2 and DromeRh7 cluster with subgroups of rhodopsins from molluscs and insects, respectively. Abbreviations are as in Figure 2.

The determinants leading to an outgroup position in the phylogenetic tree in Figure 2 have been eliminated and must therefore reside in the extra-7TM sections of these rhodopsin sequences. An obvious divergence concerns the C-termini of both rhodopsins. The C-terminus of DromeRh7 is considerably longer than that of any other insect rhodopsin. PateyRh2, the scallop rhodopsin which is expressed in a ciliary photoreceptor cell type [32,34]-contrary to the majority of invertebrate rhodopsins which are expressed in rhabdomeral photoreceptors-also posseses an extended C-terminus. This C-terminus, however, does not exhibit a particular homology to the extended C-termini of other molluscs, for example of the cephalopod rhodopsins. It may be that in PatyeRh2 extra-7 TM sites are conserved for initiation of a transduction mechanism operating in ancestral photoreceptors of both molluscs and chordates. Following that line of arguments, one would expect that DromeRh7 is coupled to a transducin-like G-protein, like the one utilized in chordate phototransduc-tion, or that it does not serve a signal transducing function at all.

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