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Evolution of dopamine receptor genes of the D1 class in vertebrates.
Yamamoto K
,
Mirabeau O
,
Bureau C
,
Blin M
,
Michon-Coudouel S
,
Demarque M
,
Vernier P
.
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The receptors of the dopamine neurotransmitter belong to two unrelated classes named D1 and D2. For the D1 receptor class, only two subtypes are found in mammals, the D1A and D1B, receptors, whereas additional subtypes, named D1C, D1D, and D1X, have been found in other vertebrate species. Here, we analyzed molecular phylogeny, gene synteny, and gene expression pattern of the D1 receptor subtypes in a large range of vertebrate species, which leads us to propose a new view of the evolution of D1 dopamine receptor genes. First, we show that D1C and D1D receptor sequences are encoded by orthologous genes. Second, the previously identified Cypriniform D1X sequence is a teleost-specific paralog of the D1B sequences found in all groups of jawed vertebrates. Third, zebrafish and several sauropsid species possess an additional D1-like gene, which is likely to form another orthology group of vertebrate ancestral genes, which we propose to name D1E. Ancestral jawed vertebrates are thus likely to have possessed four classes of D1 receptor genes-D1A, D1B(X), D1C(D), and D1E-which arose from large-scale gene duplications. The D1C receptor gene would have been secondarily lost in the mammalian lineage, whereas the D1E receptor gene would have been lost independently in several lineages of modern vertebrates. The D1A receptors are well conserved throughout jawed vertebrates, whereas sauropsid D1C receptors have rapidly diverged, to the point that they were misidentified as D1D. The functional significance of the D1C receptor loss is not known. It is possible that the function may have been substituted with D1A or D1B receptors in mammals, following the disappearance of D1C receptors in these species.
Fig. 1. Phylogenetic relationships of D1 and D2 classes of dopamine receptors compared with other monoamine receptors in vertebrates. The first branch support value corresponds to the bootstrap from Maximum-likelihood method, and the second value corresponds to the posterior probability from Bayesian method. Note that different class of dopaminergic, adrenergic, and serotoninergic receptors are not more related to each other than to the other class of monoamine receptors. Instead, monoamine receptors coupled to the same class of G proteins tend to be clustered together.
Fig. 2. A representative phylogenetic tree of the vertebrate D1 receptors obtained using two different methods. (A) A phylogenetic tree obtained from maximum likelihood method using protein sequences, while (B) was obtained from Bayesian analysis using the first two codons of the corresponding nucleotide sequences. The trees were rooted on Amphioxus D1-like receptors. The branch support values (boot strap value in A, and posterior probabilities in B) are indicated in red, and the length of the horizontal lines is proportional to sequence divergence (scale bar: 0.1 arbitrary units in A and 0.4 arbitrary units in B), except those of Amphioxus (Brachiostoma AmphiAmR1 and D1/β; the scales are shown along the branch). The two trees provide complementary information, leading four major clades of D1-like dopamine receptors in jawed vertebrates. Arrows in (A) indicate teleost-specific genome duplication, which probably had born two copies of D1A, D1B, and D1C.
Fig. 3. Comparative gene syntenies of the chromosome loci bearing the D1-like receptor genes in representative vertebrate species. Lamprey D1-like gene is illustrated in purple, putative D1A genes are illustrated in red, D1B genes in blue, and D1X in gray. The genes previously recognized to be D1C (found in anamniotes) are in light green, and the ones to be D1D (found in sauropsids) are in dark green. The shared synteny between D1C and D1D strongly suggests that they are orthologous genes. Note that the mammalian chromosomes lack the D1C or D1D gene at the loci but otherwise demonstrate the conserved synteny with other species. Newly identified genes found in anole lizard, turkey, and zebrafish are illustrated in yellow, named D1E. The comparison between turkey and anole lizard strongly suggests that they are orthologous genes, and the conserved synteny lacking the D1E loci on the chicken and mouse chromosomes indicates the secondary loss of D1E in these species. Some extent of conservation (e.g., TNFRSF10 and LOXL2) is found on the zebrafish chromosome 5 and D1E neighbors of sauropsids, suggesting that the homologous loci may have been present before the divergence of jawed vertebrates.
Fig. 4. A hypothetical evolutionary scenario of D1 class dopamine receptor genes in chordates. The four D1-class genes, D1A, D1B (including teleostean D1X), D1C (including sauropsid D1D), and D1E are provably duplicated in the early stage of vertebrate evolution. The duplication process from one to four is not clear. Based on the hypothesis of large-scale gene/genome duplications, together with the phylogenetic position of lamprey D1-like gene, it is possible that ancestral D1 gene was duplicated into ancestors of D1A/B and D1C/E before the separation of cyclostome and gnathostome, and then the two paralogs were further duplicated before the divergence of gathostome lineage. D1C and D1E were secondarily lost in some lineages, resulting in only two paralogs in mammals, for example.
Fig. 5. In situ hybridization of D1A, D1B, and D1C (previously known as D1D) on transverse sections of chick telencephalon (midline to the right). The three genes are differentially expressed in the telencephalon. D1A is abundant in the striatum (A), D1B is in the striatum and the mesopallium (B), and D1C(D) is only in the pallium (C), notably in the mesopallium (E). The D1C(D) expression was found in the hippocampus as well (D). H, hyper pallium; Hp, hippocampus; M, mesopallium; N, nidopallium; Str, striatum. Scale bars = 1 mm for A, B, C, and 200 µm for D, E.
Fig. 7. Schematic drawing showing gene expression patterns of D1-class dopamine receptor genes in the telencephala of rodents, birds, and frogs. D1A expression (red circles) in the striatum is well conserved in tetrapods. The expression pattern in the pallium, by contrast, is not much conserved. D1C is selectively expressed in the avian pallium, whereas absent in mammals. Also note the prominent D1B expression in the mammalian hippocampus, whereas D1C is expressed in the avian hippocampus.
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