The Atlantic salmon genome provides insights into rediploidization

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Abstract

The 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-quality genome assembly for Atlantic salmon ( Salmo salar), and show that large genomic reorganizations, coinciding with bursts of transposon-mediated repeat expansions, were crucial for the post-Ss4R rediploidization process. Comparisons of duplicate gene expression patterns across a wide range of tissues with orthologous genes from a pre-Ss4R outgroup unexpectedly demonstrate far more instances of neofunctionalization than subfunctionalization. Surprisingly, we find that genes that were retained as duplicates after the teleost-specific whole-genome duplication 320 million years ago were not more likely to be retained after the Ss4R, and that the duplicate retention was not influenced to a great extent by the nature of the predicted protein interactions of the gene products. Finally, we demonstrate that the Atlantic salmon assembly can serve as a reference sequence for the study of other salmonids for a range of purposes.

Supplementary information

The online version of this article (doi:10.1038/nature17164) contains supplementary material, which is available to authorized users.

Abstract

The genome sequence is presented for the Atlantic salmon (Salmo salar), providing information about a rediploidization following a salmonid-specific whole-genome duplication event that resulted in an autotetraploidization.

Supplementary information

The online version of this article (doi:10.1038/nature17164) contains supplementary material, which is available to authorized users.

A window on salmonid genome evolution

William Davidson and colleagues report sequencing and assembly of the Atlantic salmon genome, which they demonstrate as a useful reference to also improve the genome assembly of other salmanoids. Their analyses provide insights into duplicate retention patterns across two rounds of whole-genome duplication that have occurred in this lineage.

Supplementary information

The online version of this article (doi:10.1038/nature17164) contains supplementary material, which is available to authorized users.

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Most cited references 62

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Trimmomatic: a flexible trimmer for Illumina sequence data

Anthony M. Bolger, Marc Lohse, Bjoern Usadel (2014)

Motivation: Although many next-generation sequencing (NGS) read preprocessing tools already existed, we could not find any tool or combination of tools that met our requirements in terms of flexibility, correct handling of paired-end data and high performance. We have developed Trimmomatic as a more flexible and efficient preprocessing tool, which could correctly handle paired-end data. Results: The value of NGS read preprocessing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output that is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested. Availability and implementation: Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available at http://www.usadellab.org/cms/index.php?page=trimmomatic Contact: usadel@bio1.rwth-aachen.de Supplementary information: Supplementary data are available at Bioinformatics online.

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STAR: ultrafast universal RNA-seq aligner.

Alexander Dobin, Carrie A. Davis, Felix Schlesinger … (2013)

Accurate alignment of high-throughput RNA-seq data is a challenging and yet unsolved problem because of the non-contiguous transcript structure, relatively short read lengths and constantly increasing throughput of the sequencing technologies. Currently available RNA-seq aligners suffer from high mapping error rates, low mapping speed, read length limitation and mapping biases. To align our large (>80 billon reads) ENCODE Transcriptome RNA-seq dataset, we developed the Spliced Transcripts Alignment to a Reference (STAR) software based on a previously undescribed RNA-seq alignment algorithm that uses sequential maximum mappable seed search in uncompressed suffix arrays followed by seed clustering and stitching procedure. STAR outperforms other aligners by a factor of >50 in mapping speed, aligning to the human genome 550 million 2 × 76 bp paired-end reads per hour on a modest 12-core server, while at the same time improving alignment sensitivity and precision. In addition to unbiased de novo detection of canonical junctions, STAR can discover non-canonical splices and chimeric (fusion) transcripts, and is also capable of mapping full-length RNA sequences. Using Roche 454 sequencing of reverse transcription polymerase chain reaction amplicons, we experimentally validated 1960 novel intergenic splice junctions with an 80-90% success rate, corroborating the high precision of the STAR mapping strategy. STAR is implemented as a standalone C++ code. STAR is free open source software distributed under GPLv3 license and can be downloaded from http://code.google.com/p/rna-star/.

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MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

Kazutaka Katoh, Daron Standley (2013)

We report a major update of the MAFFT multiple sequence alignment program. This version has several new features, including options for adding unaligned sequences into an existing alignment, adjustment of direction in nucleotide alignment, constrained alignment and parallel processing, which were implemented after the previous major update. This report shows actual examples to explain how these features work, alone and in combination. Some examples incorrectly aligned by MAFFT are also shown to clarify its limitations. We discuss how to avoid misalignments, and our ongoing efforts to overcome such limitations.

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Author and article information

Contributors

Stig W. Omholt: stig.omholt@ntnu.no

William S. Davidson: wdavidso@sfu.ca

Journal

Journal ID (nlm-ta): Nature

Journal ID (iso-abbrev): Nature

Title: Nature

Publisher: Nature Publishing Group UK (London )

ISSN (Print): 0028-0836

ISSN (Electronic): 1476-4687

Publication date (Electronic): 18 April 2016

Publication date PMC-release: 18 April 2016

Publication date (Print): 2016

Volume: 533

Issue: 7602

Pages: 200-205

Affiliations

[1 ]GRID grid.19477.3c, ISNI 0000 0004 0607 975X, Department of Animal and Aquacultural Sciences, , Centre for Integrative Genetics (CIGENE), Norwegian University of Life Sciences, ; Ås NO-1432, Norway

[2 ]GRID grid.143640.4, ISNI 0000 0004 1936 9465, Department of Biology, , University of Victoria, Victoria, ; British Columbia, V8W 3N5 Canada

[3 ]GRID grid.469946.0, J. Craig Venter Institute, ; 9704 Medical Center Drive, Rockville, 20850 Maryland USA

[4 ]GRID grid.19477.3c, ISNI 0000 0004 0607 975X, Department of Chemistry, , Biotechnology and Food Science, Norwegian University of Life Sciences, ; Ås NO-1432, Norway

[5 ]GRID grid.467081.c, ISNI 0000 0004 0613 9724, Department of Plant Physiology, , Umeå Plant Science Centre, Umeå University, ; Umeå, 90187 Sweden

[6 ]Institute for Physical Sciences and Technology, University of Maryland, College Park, Maryland, 20742-2431 USA

[7 ]GRID grid.135963.b, ISNI 0000 0001 2109 0381, Department of Molecular Biology, , University of Wyoming, ; Laramie, Wyoming, 82071 USA

[8 ]GRID grid.264727.2, ISNI 0000 0001 2248 3398, Center for Computational Genetics and Genomics, Temple University, ; Philadelphia, 19122-6078 Pennsylvania USA

[9 ]GRID grid.264727.2, ISNI 0000 0001 2248 3398, Department of Biology, , Temple University, ; Philadelphia, 19122-6078 Pennsylvania USA

[10 ]GRID grid.443909.3, ISNI 0000 0004 0385 4466, Center for Mathematical Modeling, University of Chile, ; Santiago 8370456, Chile

[11 ]GRID grid.443909.3, ISNI 0000 0004 0385 4466, Center for Genome Regulation, University of Chile, ; Santiago 8370415, Chile

[12 ]GRID grid.5510.1, ISNI 0000 0004 1936 8921, Medical Genetics, Oslo University Hospital and University of Oslo, ; Oslo, NO-0424 Norway

[13 ]GRID grid.410549.d, ISNI 0000 0000 9542 2193, Department of Virology, , Norwegian Veterinary Institute, ; Oslo, NO-0454 Norway

[14 ]GRID grid.5510.1, ISNI 0000 0004 1936 8921, Department of Biosciences, , Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, ; Oslo, NO-0316 Norway

[15 ]CHORI, Oakland, 94609 California USA

[16 ]GRID grid.457441.7, AquaGen, ; Trondheim, NO-7462 Norway

[17 ]GRID grid.22736.32, ISNI 0000 0004 0451 2652, Nofima, ; Tromsø, NO-9291 Norway

[18 ]National Center for Cool and Cold Water Aquaculture, ARS-USDA, Kearneysville, 25430 West Virginia USA

[19 ]Beckman Genomics, Danvers, Massachusetts, 01923 USA

[20 ]GRID grid.428337.9, Courtagen Life Sciences, ; Woburn, 01801 Massachusetts USA

[21 ]GRID grid.21155.32, ISNI 0000 0001 2034 1839, BGI-Shenzhen, ; Shenzhen, 518083 China

[22 ]GRID grid.412179.8, ISNI 0000 0001 2191 5013, Department of Biology, , Laboratory of Molecular Ecology, Genomics, and Evolutionary Studies, University of Santiago, ; Santiago 9170022, Chile

[23 ]GRID grid.443909.3, ISNI 0000 0004 0385 4466, Faculty of Medicine, University of Chile, ; Santiago 8380453, Chile

[24 ]GRID grid.248762.d, ISNI 0000 0001 0702 3000, Genome Sciences Centre, BC Cancer Agency, Vancouver, ; British Columbia, V5Z 4S6 Canada

[25 ]GRID grid.61971.38, ISNI 0000 0004 1936 7494, Department of Molecular Biology and Biochemistry, , Simon Fraser University, ; Burnaby, V5A 1S6 British Columbia Canada

[26 ]GRID grid.7914.b, ISNI 0000 0004 1936 7443, Department of Informatics, , University of Bergen, ; Bergen, NO-6020 Norway

[27 ]GRID grid.5947.f, ISNI 0000 0001 1516 2393, Department of Biology, , Centre for Biodiversity Dynamics, NTNU - Norwegian University of Science and Technology, ; Trondheim, NO-7491 Norway

Article

Publisher ID: BFnature17164

DOI: 10.1038/nature17164

PMC ID: 8127823

PubMed ID: 27088604

SO-VID: a383abaa-87d9-46f4-b6bc-05583fa0533c

License:

This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

History

Date received : 10 September 2015

Date accepted : 26 January 2016

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ScienceOpen disciplines: Uncategorized

Keywords: genome evolution,genome

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ScienceOpen disciplines: Uncategorized

Keywords: genome evolution, genome

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The Atlantic salmon genome provides insights into rediploidization

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Abstract

Supplementary information

Abstract

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A window on salmonid genome evolution

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Genome Integrity

Most cited references 62

Trimmomatic: a flexible trimmer for Illumina sequence data

STAR: ultrafast universal RNA-seq aligner.

MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

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Cited by 445

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