The grayling genome reveals selection on gene expression regulation after whole-genome duplication

Whole-genome duplication (WGD) has been a major evolutionary driver of increased genomic complexity in vertebrates. One such event occurred in the salmonid family ∼80 Ma (Ss4R) giving rise to a plethora of structural and regulatory duplicate-driven divergence, making salmonids an exemplary system to...

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Published in:Genome Biology and Evolution
Main Authors: Varadharajan, Srinidhi, Sandve, Simen Rød, Gillard, Gareth Benjamin, Tørresen, Ole K., Mulugeta, Teshome Dagne, Hvidsten, Torgeir Rhoden, Lien, Sigbjørn, Vøllestad, Leif Asbjørn, Jentoft, Sissel, Nederbragt, Alexander Johan, Jakobsen, Kjetill Sigurd
Format: Article in Journal/Newspaper
Language:English
Published: 2018
Subjects:
Online Access:https://hdl.handle.net/11250/2690310
https://doi.org/10.1093/gbe/evy201
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spelling ftunivmob:oai:nmbu.brage.unit.no:11250/2690310 2023-05-15T15:31:41+02:00 The grayling genome reveals selection on gene expression regulation after whole-genome duplication Varadharajan, Srinidhi Sandve, Simen Rød Gillard, Gareth Benjamin Tørresen, Ole K. Mulugeta, Teshome Dagne Hvidsten, Torgeir Rhoden Lien, Sigbjørn Vøllestad, Leif Asbjørn Jentoft, Sissel Nederbragt, Alexander Johan Jakobsen, Kjetill Sigurd 2018-12-04T14:23:40Z application/vnd.openxmlformats-officedocument.wordprocessingml.document https://hdl.handle.net/11250/2690310 https://doi.org/10.1093/gbe/evy201 eng eng Genome Biology and Evolution. 2018, 10 (10), 2785-2800. urn:issn:1759-6653 https://hdl.handle.net/11250/2690310 https://doi.org/10.1093/gbe/evy201 cristin:1639030 Attribution-NonCommercial-NoDerivatives 4.0 Internasjonal http://creativecommons.org/licenses/by-nc-nd/4.0/deed.no CC-BY-NC-ND 2785-2800 10 Genome Biology and Evolution Peer reviewed Journal article 2018 ftunivmob https://doi.org/10.1093/gbe/evy201 2021-09-23T20:15:50Z Whole-genome duplication (WGD) has been a major evolutionary driver of increased genomic complexity in vertebrates. One such event occurred in the salmonid family ∼80 Ma (Ss4R) giving rise to a plethora of structural and regulatory duplicate-driven divergence, making salmonids an exemplary system to investigate the evolutionary consequences of WGD. Here, we present a draft genome assembly of European grayling (Thymallus thymallus) and use this in a comparative framework to study evolution of gene regulation following WGD. Among the Ss4R duplicates identified in European grayling and Atlantic salmon (Salmo salar), one-third reflect nonneutral tissue expression evolution, with strong purifying selection, maintained over ∼50 Myr. Of these, the majority reflect conserved tissue regulation under strong selective constraints related to brain and neural-related functions, as well as higher-order protein–protein interactions. A small subset of the duplicates have evolved tissue regulatory expression divergence in a common ancestor, which have been subsequently conserved in both lineages, suggestive of adaptive divergence following WGD. These candidates for adaptive tissue expression divergence have elevated rates of protein coding- and promoter-sequence evolution and are enriched for immune- and lipid metabolism ontology terms. Lastly, lineage-specific duplicate divergence points toward underlying differences in adaptive pressures on expression regulation in the nonanadromous grayling versus the anadromous Atlantic salmon. Our findings enhance our understanding of the role of WGD in genome evolution and highlight cases of regulatory divergence of Ss4R duplicates, possibly related to a niche shift in early salmonid evolution. acceptedVersion Article in Journal/Newspaper Atlantic salmon Salmo salar Open archive Norwegian University of Life Sciences: Brage NMBU Genome Biology and Evolution 10 10 2785 2800
institution Open Polar
collection Open archive Norwegian University of Life Sciences: Brage NMBU
op_collection_id ftunivmob
language English
description Whole-genome duplication (WGD) has been a major evolutionary driver of increased genomic complexity in vertebrates. One such event occurred in the salmonid family ∼80 Ma (Ss4R) giving rise to a plethora of structural and regulatory duplicate-driven divergence, making salmonids an exemplary system to investigate the evolutionary consequences of WGD. Here, we present a draft genome assembly of European grayling (Thymallus thymallus) and use this in a comparative framework to study evolution of gene regulation following WGD. Among the Ss4R duplicates identified in European grayling and Atlantic salmon (Salmo salar), one-third reflect nonneutral tissue expression evolution, with strong purifying selection, maintained over ∼50 Myr. Of these, the majority reflect conserved tissue regulation under strong selective constraints related to brain and neural-related functions, as well as higher-order protein–protein interactions. A small subset of the duplicates have evolved tissue regulatory expression divergence in a common ancestor, which have been subsequently conserved in both lineages, suggestive of adaptive divergence following WGD. These candidates for adaptive tissue expression divergence have elevated rates of protein coding- and promoter-sequence evolution and are enriched for immune- and lipid metabolism ontology terms. Lastly, lineage-specific duplicate divergence points toward underlying differences in adaptive pressures on expression regulation in the nonanadromous grayling versus the anadromous Atlantic salmon. Our findings enhance our understanding of the role of WGD in genome evolution and highlight cases of regulatory divergence of Ss4R duplicates, possibly related to a niche shift in early salmonid evolution. acceptedVersion
format Article in Journal/Newspaper
author Varadharajan, Srinidhi
Sandve, Simen Rød
Gillard, Gareth Benjamin
Tørresen, Ole K.
Mulugeta, Teshome Dagne
Hvidsten, Torgeir Rhoden
Lien, Sigbjørn
Vøllestad, Leif Asbjørn
Jentoft, Sissel
Nederbragt, Alexander Johan
Jakobsen, Kjetill Sigurd
spellingShingle Varadharajan, Srinidhi
Sandve, Simen Rød
Gillard, Gareth Benjamin
Tørresen, Ole K.
Mulugeta, Teshome Dagne
Hvidsten, Torgeir Rhoden
Lien, Sigbjørn
Vøllestad, Leif Asbjørn
Jentoft, Sissel
Nederbragt, Alexander Johan
Jakobsen, Kjetill Sigurd
The grayling genome reveals selection on gene expression regulation after whole-genome duplication
author_facet Varadharajan, Srinidhi
Sandve, Simen Rød
Gillard, Gareth Benjamin
Tørresen, Ole K.
Mulugeta, Teshome Dagne
Hvidsten, Torgeir Rhoden
Lien, Sigbjørn
Vøllestad, Leif Asbjørn
Jentoft, Sissel
Nederbragt, Alexander Johan
Jakobsen, Kjetill Sigurd
author_sort Varadharajan, Srinidhi
title The grayling genome reveals selection on gene expression regulation after whole-genome duplication
title_short The grayling genome reveals selection on gene expression regulation after whole-genome duplication
title_full The grayling genome reveals selection on gene expression regulation after whole-genome duplication
title_fullStr The grayling genome reveals selection on gene expression regulation after whole-genome duplication
title_full_unstemmed The grayling genome reveals selection on gene expression regulation after whole-genome duplication
title_sort grayling genome reveals selection on gene expression regulation after whole-genome duplication
publishDate 2018
url https://hdl.handle.net/11250/2690310
https://doi.org/10.1093/gbe/evy201
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source 2785-2800
10
Genome Biology and Evolution
op_relation Genome Biology and Evolution. 2018, 10 (10), 2785-2800.
urn:issn:1759-6653
https://hdl.handle.net/11250/2690310
https://doi.org/10.1093/gbe/evy201
cristin:1639030
op_rights Attribution-NonCommercial-NoDerivatives 4.0 Internasjonal
http://creativecommons.org/licenses/by-nc-nd/4.0/deed.no
op_rightsnorm CC-BY-NC-ND
op_doi https://doi.org/10.1093/gbe/evy201
container_title Genome Biology and Evolution
container_volume 10
container_issue 10
container_start_page 2785
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