Early vertebrate chromosome duplications and the evolution of the neuropeptide Y receptor gene regions

Abstract

BackgroundOne of the many gene families that expanded in early vertebrate evolution is the neuropeptide (NPY) receptor family of G-protein coupled receptors. Earlier work by our lab suggested that several of the NPY receptor genes found in extant vertebrates resulted from two genome duplications before the origin of jawed vertebrates (gnathostomes) and one additional genome duplication in the actinopterygian lineage, based on their location on chromosomes sharing several gene families. In this study we have investigated, in five vertebrate genomes, 45 gene families with members close to the NPY receptor genes in the compact genomes of the teleost fishes Tetraodon nigroviridis and Takifugu rubripes. These correspond to Homo sapiens chromosomes 4, 5, 8 and 10.ResultsChromosome regions with conserved synteny were identified and confirmed by phylogenetic analyses in H. sapiens, M. musculus, D. rerio, T. rubripes and T. nigroviridis. 26 gene families, including the NPY receptor genes, (plus 3 described recently by other labs) showed a tree topology consistent with duplications in early vertebrate evolution and in the actinopterygian lineage, thereby supporting expansion through block duplications. Eight gene families had complications that precluded analysis (such as short sequence length or variable number of repeated domains) and another eight families did not support block duplications (because the paralogs in these families seem to have originated in another time window than the proposed genome duplication events). RT-PCR carried out with several tissues in T. rubripes revealed that all five NPY receptors were expressed in the brain and subtypes Y2, Y4 and Y8 were also expressed in peripheral organs.ConclusionWe conclude that the phylogenetic analyses and chromosomal locations of these gene families support duplications of large blocks of genes or even entire chromosomes. Thus, these results are consistent with two early vertebrate tetraploidizations forming a paralogon comprising human chromosomes 4, 5, 8 and 10 and one teleost tetraploidization. The combination of positional and phylogenetic data further strengthens the identification of orthologs and paralogs in the NPY receptor family.

The sea lamprey meiotic map improves resolution of ancient vertebrate genome duplications

“…However, these studies did not explicitly address alternate evolutionary models or departures from 1a:4d (expected under 2R). Still other studies have focused on a smaller number of genomic regions that are thought to represent the largest and best-conserved regions of fourfold paralogy (Larsson et al 2008;Canestro et al 2009;Kuraku et al 2009), although the existence of these well-defined regions is consistent with several proposed models. Finally, two recent studies used draft lamprey genomes to examine the relative timing of WGD and divergence events, but relied on the assumption that gnathostome genomes were indeed the product of two rounds of wholegenome duplication (Mehta et al 2013;Smith et al 2013).…”

“…The "single WGD" model identifies three sets of macro-and microchromosomes that experienced duplication prior to 1R (specifically, derivatives of ancA, ancC, and ancE). Notably, these three proposed duplications account for essentially all of the fourfold paralogous conserved syntenies that have been classically studied in the context of the 2R hypothesis, including large synteny groups that are exemplified by paralogs of Hox and RAR (ancE), MHC and ALDH1 (ancA), and NPYR (ancC) loci (Larsson et al 2008;Canestro et al 2009;Kuraku et al 2009). Previous reconstructions of the ALDH1-syntenic region also strongly implicate a pre-1R intrachromosomal duplication of ancA followed by chromosomal fission (Canestro et al 2009), consistent with the single WGD model.…”

“…Based on genome size, chromosome morphology, and isozyme counts, Susumu Onho proposed as early as 1970 that at least one WGD must have occurred prior to the diversification of the ancestral amniote or tetrapod lineage (Ohno 1970). Support for the 2R hypothesis rests partially on phylogenetic analyses of gene families and discrete synteny groups that have retained a significant number of genes that presumably trace to two WGDs (Larsson et al 2008;Canestro et al 2009;Kuraku et al 2009) (but see Hughes 1999;Asrar et al 2013). Additional support for 2R comes from studies that examined the number and distribution of homologous segments within the human genome (Dehal and Boore 2005) among jawed vertebrates (gnathostomes) (Nakatani et al 2007;Murat et al 2012) and between gnathostomes and amphioxus (Branchiostoma floridae: a cephalochordate) (Abi-Rached et al 2002;Putnam et al 2008).…”

Neuropeptide Y Receptors Y1and Y2are Present in Neurons and Glial Cells in Rat Retinal Cells in Culture

“…14, 16 From a consideration of the phylogenetic preservation, it is expected that the NPY and NPY receptor distribution in the retina does not vary significantly between species. NPY-ir is present in amacrine cells in the majority of species studied (fish, frogs, lizards, rodents, baboons, pigs, cats, chickens, and pigeons).…”

Evolution of vertebrate opioid receptors

“…Investigation of conserved synteny may facilitate identification of orthologs and gives important clues to the mechanisms by which the genes were duplicated. We used this approach to investigate the evolution of a few other gene families, namely the neuropeptide Y (NPY) family of peptides (27) and the large family of NPY receptors (28). These families were found to have expanded as a result of extensive chromosome duplications, most likely resulting from two tetraploidizations, i.e., genome duplications, that occurred early in vertebrate evolution (29).…”