A synthetic rainbow trout linkage map provides new insights into the salmonid whole genome duplication and the conservation of synteny among teleosts

Abstract

BackgroundRainbow trout is an economically important fish and a suitable experimental organism in many fields of biology including genome evolution, owing to the occurrence of a salmonid specific whole-genome duplication (4th WGD). Rainbow trout is among some of the most studied teleosts and has benefited from substantial efforts to develop genomic resources (e.g., linkage maps. Here, we first generated a synthetic map by merging segregation data files derived from three independent linkage maps. Then, we used it to evaluate genome conservation between rainbow trout and three teleost models, medaka, stickleback and zebrafish and to further investigate the extent of the 4th WGD in trout genome.ResultsThe INRA linkage map was updated by adding 211 new markers. After standardization of marker names, consistency of marker assignment to linkage groups and marker orders was checked across the three different data sets and only loci showing consistent location over all or almost all of the data sets were kept. This resulted in a synthetic map consisting of 2226 markers and 29 linkage groups spanning over 3600 cM. Blastn searches against medaka, stickleback, and zebrafish genomic databases resulted in 778, 824 and 730 significant hits respectively while blastx searches yielded 505, 513 and 510 significant hits. Homology search results revealed that, for most rainbow trout chromosomes, large syntenic regions encompassing nearly whole chromosome arms have been conserved between rainbow trout and its closest models, medaka and stickleback. Large conserved syntenies were also found between the genomes of rainbow trout and the reconstructed teleost ancestor. These syntenies consolidated the known homeologous affinities between rainbow trout chromosomes due to the 4th WGD and suggested new ones.ConclusionsThe synthetic map constructed herein further highlights the stability of the teleost genome over long evolutionary time scales. This map can be easily extended by incorporating new data sets and should help future rainbow trout whole genome sequence assembly. Finally, the persistence of large conserved syntenies across teleosts should facilitate the identification of candidate genes through comparative mapping, even if the occurrence of intra-chromosomal micro-rearrangement may hinder the accurate prediction their genomic location.

Comparative mapping for bighead carp (Aristichthys nobilis) against model and non-model fishes provides insights into the genomic evolution of cyprinids

“…Studies on comparative mapping have revealed that the rates of nucleotide sequence similarity were positively correlated with phylogenetic relationships among fish species (Xia et al 2010;Zheng et al 2011;Guyomard et al 2012). In this study, we found that bighead carp (Hypophthalmichthyinae) genome has a higher similarity with common carp (Cyprininae) (95.3 %) than that with zebrafish (Danioninae) (70.9 %).…”

“…With the assistance of comparative mapping, these chromosomal rearrangements could be easily observed. Inversion and translocation are quite common among different species, and they have been observed in all previously investigated fishes, including zebrafish , medaka (Kasahara et al 2007), rainbow trout (Guyomard et al 2012) and common carp (Zhang et al 2013).…”

“…(http://www.ensembl.org/index.html). Welldefined or high-density genetic linkage maps have been constructed for several food fishes, e.g., rainbow trout Oncorhynchus mykiss (Guyomard et al 2012;Rexroad et al 2008), Atlantic salmon Salmo salar (Lien et al 2011;Brenna-Hansen et al 2012), gilthead seabream Sparus aurata (Sarropoulou et al 2007), half-smooth tongue sole Cynoglossus semilaevis (Song et al 2012a) and Japanese flounder Paralichthys olivaceus (Song et al 2012b). Physical maps have also been reported in a few commercial fishes, such as channel catfish Ictalurus punctatus (Quiniou et al 2007), Nile tilapia Oreochromis niloticus (Katagiri et al 2005) and European seabass Dicentrarchus labrax (Kuhl et al 2010).…”

“…The increase of genetic and sequence/physical maps has greatly promoted comparative genomics in fishes. Comparative mapping is an efficient way to locate candidate genes on maps of non-model fishes (Guyomard et al 2012) and perform functional studies of homologous genes (Woods et al 2000). Orthologous genes in development, growth and disease resistance could be deduced for food fishes, because gene functions are often evolutionarily conserved among vertebrates (Gates et al 1999;Woods et al 2000).…”

Chromosome evolution in fishes: a new challenging proposal from Neotropical species

“…Moreover, although fishes were reported as having high rates of chromosomal rearrangements and low rates of synteny within vertebrates (Robinson-Rechavi et al, 2001a, 2001bVenkatesh, 2003;Ravi & Venkatesh, 2008), more recent investigation indicated both the presence of large syntenic blocks within Teleosts and between Teleosts and other vertebrates (Mazzuchelli et al, 2012). This indicates the stability of the genome of these fishes over long evolutionary time scales (Guyomard et al, 2012;Schartl et al, 2013). In addition a higher conserved gene order was observed in fishes than in mammals by genome comparison of three teleost species (fugu, Tetraodon, and medaka) with those of three mammalian lineages (human, mouse, and opossum), and authors reported these results as "largely due to a lower rate of interchromosomal rearrangements in the teleosts" (Kai et al, 2011).…”