The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates

Berthelot, Camille; Brunet, Frédéric; Chalopin, Domitille; Juanchich, Amélie; Bernard, Maria; Noël, Benjamin; Bento, Pascal; Silva, Corinne Da; Labadie, Karine; Alberti, Adriana; Aury, Jean‐Marc; Louis, Alexandra; Déhais, Patrice; Bardou, Philippe; Montfort, Jérôme; Klopp, Christophe; Cabau, Cédric; Gaspin, Christine; Thorgaard, Gary H.; Boussaha, Mekki; Quillet, Edwige; Guyomard, René; Galiana, Delphine; Bobe, Julien; Volff, Jean‐Nicolas; Genêt, Carine; Wincker, Patrick; Jaillon, Olivier; Crollius, Hugues Roest; Guiguen, Yann

doi:10.1038/ncomms4657

Cited by 861 publications

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“…Our results challenge the recent claim that rediploidization in salmonids has been a gradual process unlinked to significant genome rearrangements 13 . They also challenge current views about the relative importance of sub-and neofunctionalization in vertebrate genomes (reviewed in ref.…”

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confidence: 57%

“…To test the feasibility of such a comparative genomics approach, we used the Atlantic salmon assembly to construct chromosome sequences for the non-chromosome anchored rainbow trout genome sequence 13 . We were able to map 99.5% of rainbow trout scaffolds >100 kilobases (kb) (total 1.22 Gb) to the Atlantic salmon chromosome sequences ( Supplementary Information section 1.5).…”

Section: A Reference Genome For Salmonidsmentioning

confidence: 99%

“…13) into 29 rainbow trout chromosome sequences ( Supplementary Information section 9). This was done by first using the rainbow trout linkage map to determine the proximate order of 2,439 trout scaffolds containing SNPs, which we found to be sufficient for determining conserved blocks.…”

Section: A Reference Genome For Salmonidsmentioning

confidence: 99%

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The Atlantic salmon genome provides insights into rediploidization

Lien

Koop

Sandve

et al. 2016

Nature

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The 22,000-year-old cave painting of an Atlantic salmon (Salmo salar) near the Vézère River in France is a reminder of our fascination with, and dependence on, Atlantic salmon throughout human history. Atlantic salmon belongs to the salmonid lineage which comprises 11 genera, with at least 70 species that exhibit a wide range of ecological adaptations and use a variety of marine and freshwater life history strategies 1 . Salmonids hold important positions as socially iconic species and economic resources within aquaculture, wild fisheries and recreational sport fisheries. Moreover, they serve as key indicator species of the health of North Atlantic and Pacific coastal and river ecosystems.All teleosts share at least three rounds of whole-genome duplication (WGD), 1R and 2R before the divergence of lamprey from the jawed vertebrates 2 , and a third teleost-specific WGD (Ts3R) at the base of the teleosts ~320 million years ago (Mya) [3][4][5] . Very little is known about the mechanisms of genomic and chromosomal reorganization after WGD in vertebrates because the 1R, 2R and Ts3R occurred so long ago that few clear signatures of post-WGD reorganization events remain. In contrast, a fourth WGD (the Ss4R salmonid-specific autotetraploidization event) occurred in the common ancestor of salmonids ~80 Mya after their divergence from Esociformes ~125 Mya 6-8 (Fig. 1), and the continued presence of multivalent pairing at meiosis and evidence of tetrasomic inheritance in salmonid species suggests that diploidy is not yet fully re-established 6,9,10 . Salmonids thus appear to provide an unprecedented opportunity for studying vertebrate genome evolution after an autotetraploid WGD 11,12 over a time period that is long enough to reveal long-term evolutionary patterns, but short enough to give a high-resolution picture of the process. In addition, they provide an excellent setting for contextualizing genome evolution with a dramatic post-WGD species radiation and intricate adaptations to a whole range of life history regimes.Here we present a high-quality reference genome assembly of the Atlantic salmon, and use it to describe major patterns characterizing the post-Ss4R salmonid genome evolution over the past 80 million years (Myr). Our results challenge the recent claim that rediploidization in salmonids has been a gradual process unlinked to significant genome rearrangements 13 . They also challenge current views about the relative importance of sub-and neofunctionalization in vertebrate genomes (reviewed in ref. 14), and the importance of dosage balance as a gene duplicate retention mechanism 15 . Genome characterizationThe Atlantic salmon reference genome assembly (GenBank: GCA_000233375.4) adds up to 2.97 gigabases (Gb) with aThe whole-genome duplication 80 million years ago of the common ancestor of salmonids (salmonid-specific fourth vertebrate whole-genome duplication, Ss4R) provides unique opportunities to learn about the evolutionary fate of a duplicated vertebrate genome in 70 extant lineages. Here we present a high...

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confidence: 57%

Section: A Reference Genome For Salmonidsmentioning

confidence: 99%

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The Atlantic salmon genome provides insights into rediploidization

Lien

Koop

Sandve

et al. 2016

Nature

972

1,387

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“…The family is estimated to be between 63.2 and 58.1 million years old 27, 28 . A whole genome duplication event occurred before the radiation of the salmonid family 29– 32 which has provided time for divergence of ohnologous genes (paralogous genes originated by whole genome duplication event). Furthermore, recent estimates from the rainbow trout ( Oncorhynchus mykiss ) genome suggest that ohnologous genes were lost at a rate of about 170 ohnologous genes per million years and by utilizing multiple data sources the genome assembly problem of this family can be solved 32 .…”

Section: Introductionmentioning

confidence: 99%

The developmental transcriptome of contrasting Arctic charr (Salvelinus alpinus) morphs

et al. 2015

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Species and populations with parallel evolution of specific traits can help illuminate how predictable adaptations and divergence are at the molecular and developmental level. Following the last glacial period, dwarfism and specialized bottom feeding morphology evolved rapidly in several landlocked Arctic charr Salvelinus alpinus populations in Iceland. To study the genetic divergence between small benthic morphs and limnetic morphs, we conducted RNA-sequencing charr embryos at four stages in early development. We studied two stocks with contrasting morphologies: the small benthic (SB) charr from Lake Thingvallavatn and Holar aquaculture (AC) charr.The data reveal significant differences in expression of several biological pathways during charr development. There was also an expression difference between SB- and AC-charr in genes involved in energy metabolism and blood coagulation genes. We confirmed differing expression of five genes in whole embryos with qPCR, including lysozyme and natterin-like which was previously identified as a fish-toxin of a lectin family that may be a putative immunopeptide. We also verified differential expression of 7 genes in the developing head that associated consistently with benthic v.s.limnetic morphology (studied in 4 morphs). Comparison of single nucleotide polymorphism (SNP) frequencies reveals extensive genetic differentiation between the SB and AC-charr (~1300 with more than 50% frequency difference). Curiously, three derived alleles in the otherwise conserved 12s and 16s mitochondrial ribosomal RNA genes are found in benthic charr.The data implicate multiple genes and molecular pathways in divergence of small benthic charr and/or the response of aquaculture charr to domestication. Functional, genetic and population genetic studies on more freshwater and anadromous populations are needed to confirm the specific loci and mutations relating to specific ecological traits in Arctic charr.

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“…These results indicate that they are fish USP18 orthologs. Notably, more than one USP18 gene copy is observed in some fish species, for example, two copies in rainbow trout, which is likely ascribed to an additional and relatively recent whole-genome duplication (WGD) event in salmonids (Berthelot et al, 2014). In zebrafish, two size-different USP18 proteins are predicated (USP18-x1 and USP18-x2).…”

Section: Discussionmentioning

confidence: 99%