Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification

Fiona M Robertson, Manu Kumar Gundappa, Fabian Grammes, Torgeir R. Hvidsten, Anthony Redmond, Sigbjorn Lien, Peter W.H. Holland, Samuel A. M. Martin, Simen R. Sandve, Daniel J. MacQueen (Corresponding Author)

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Abstract

Background The functional divergence of duplicate genes (ohnologues) retained from whole genome duplication (WGD) is thought to promote evolutionary diversification. However, species radiation and phenotypic diversification is often temporally separated from WGD. Salmonid fish, whose ancestor underwent WGD by autotetraploidization ~95 Ma fit such a 'time-lag' model of post-WGD radiation, which occurred alongside a major delay in the rediploidization process. Here we propose a model, 'lineage-specific ohnologue resolution' (LORe), to address the consequences of delayed rediploidization. Under LORe, speciation precedes rediploidization, allowing independent ohnologue divergence in sister lineages sharing an ancestral WGD event. Results Using cross-species sequence capture, phylogenomics and genome-wide analyses of ohnologue expression divergence, we demonstrate the major impact of LORe on salmonid evolution. One quarter of each salmonid genome, harbouring at least 4,550 ohnologues, has evolved under LORe, with rediploidization and functional divergence occurring on multiple independent occasions > 50 Myr post-WGD. We demonstrate the existence and regulatory divergence of many LORe ohnologues with functions in lineage-specific physiological adaptations that potentially facilitated salmonid species radiation. We show that LORe ohnologues are enriched for different functions than 'older' ohnologues that began diverging in the salmonid ancestor. Conclusions LORe has unappreciated significance as a nested component of post-WGD divergence that impacts the functional properties of genes, whilst providing ohnologues available solely for lineage-specific adaptation. Under LORe, which is predicted following many WGD events, the functional outcomes of WGD need not appear 'explosively', but can arise gradually over tens of Myr, promoting lineage-specific diversification regimes under prevailing ecological pressures.
Original languageEnglish
Article number111
JournalGenome Biology
Volume18
DOIs
Publication statusPublished - 14 Jun 2017

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genome
Genome
salmonid
divergence
Radiation
ancestry
Duplicate Genes
Physiological Adaptation
duplicate genes
gene
functional properties
Fishes
Pressure
fish
Genes
radiation

Keywords

  • whole genome duplication
  • rediploidization
  • species radiation
  • Lineage-specific Ohnologue Resolution (LORe)
  • duplicate genes
  • functional divergence
  • autotetraploidization
  • salmonid fish

Cite this

Robertson, F. M., Gundappa, M. K., Grammes, F., Hvidsten, T. R., Redmond, A., Lien, S., ... MacQueen, D. J. (2017). Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification. Genome Biology, 18, [111]. https://doi.org/10.1186/s13059-017-1241-z

Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification. / Robertson, Fiona M; Gundappa, Manu Kumar; Grammes, Fabian; Hvidsten, Torgeir R. ; Redmond, Anthony; Lien, Sigbjorn ; Holland, Peter W.H. ; Martin, Samuel A. M.; Sandve, Simen R. ; MacQueen, Daniel J. (Corresponding Author).

In: Genome Biology, Vol. 18, 111, 14.06.2017.

Research output: Contribution to journalArticle

Robertson, FM, Gundappa, MK, Grammes, F, Hvidsten, TR, Redmond, A, Lien, S, Holland, PWH, Martin, SAM, Sandve, SR & MacQueen, DJ 2017, 'Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification', Genome Biology, vol. 18, 111. https://doi.org/10.1186/s13059-017-1241-z
Robertson, Fiona M ; Gundappa, Manu Kumar ; Grammes, Fabian ; Hvidsten, Torgeir R. ; Redmond, Anthony ; Lien, Sigbjorn ; Holland, Peter W.H. ; Martin, Samuel A. M. ; Sandve, Simen R. ; MacQueen, Daniel J. / Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification. In: Genome Biology. 2017 ; Vol. 18.
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title = "Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification",
abstract = "Background The functional divergence of duplicate genes (ohnologues) retained from whole genome duplication (WGD) is thought to promote evolutionary diversification. However, species radiation and phenotypic diversification is often temporally separated from WGD. Salmonid fish, whose ancestor underwent WGD by autotetraploidization ~95 Ma fit such a 'time-lag' model of post-WGD radiation, which occurred alongside a major delay in the rediploidization process. Here we propose a model, 'lineage-specific ohnologue resolution' (LORe), to address the consequences of delayed rediploidization. Under LORe, speciation precedes rediploidization, allowing independent ohnologue divergence in sister lineages sharing an ancestral WGD event. Results Using cross-species sequence capture, phylogenomics and genome-wide analyses of ohnologue expression divergence, we demonstrate the major impact of LORe on salmonid evolution. One quarter of each salmonid genome, harbouring at least 4,550 ohnologues, has evolved under LORe, with rediploidization and functional divergence occurring on multiple independent occasions > 50 Myr post-WGD. We demonstrate the existence and regulatory divergence of many LORe ohnologues with functions in lineage-specific physiological adaptations that potentially facilitated salmonid species radiation. We show that LORe ohnologues are enriched for different functions than 'older' ohnologues that began diverging in the salmonid ancestor. Conclusions LORe has unappreciated significance as a nested component of post-WGD divergence that impacts the functional properties of genes, whilst providing ohnologues available solely for lineage-specific adaptation. Under LORe, which is predicted following many WGD events, the functional outcomes of WGD need not appear 'explosively', but can arise gradually over tens of Myr, promoting lineage-specific diversification regimes under prevailing ecological pressures.",
keywords = "whole genome duplication, rediploidization, species radiation, Lineage-specific Ohnologue Resolution (LORe) , duplicate genes, functional divergence, autotetraploidization , salmonid fish",
author = "Robertson, {Fiona M} and Gundappa, {Manu Kumar} and Fabian Grammes and Hvidsten, {Torgeir R.} and Anthony Redmond and Sigbjorn Lien and Holland, {Peter W.H.} and Martin, {Samuel A. M.} and Sandve, {Simen R.} and MacQueen, {Daniel J.}",
note = "Funding The study was funded by a Natural Environment Research Council (NERC) grant (NBAF704). FMR is funded by a NERC Doctoral Training Grant (NE/L50175X/1). MKG is funded by an Elphinstone PhD Scholarship from the University of Aberdeen, with additional financial support from a scholarship from the Government of Karnataka, India. Availability of data and materials Illumina sequence reads for the sequence capture study were deposited in NCBI (Bioproject PRJNA325617). All sequence alignments and phylogenetic trees used for phylogenomics are provided in Additional file 2 . Illumina sequence reads for the tissue expression study performed under controlled conditions can be found in the NCBI SRA database (accessions SRX608594, SRS64003, SRS640030, SRS640015, SRS640003, SRS639997, SRS639041, SRS640021, SRS639990l, SRS639861, SRS640009, SRS639992, SRS639037, SRS640002, SRS639994). Illumina sequence reads for the fresh to saltwater transition experiment were deposited in the European Nucleotide Archive (accession number SRP095919).",
year = "2017",
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doi = "10.1186/s13059-017-1241-z",
language = "English",
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journal = "Genome Biology",
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TY - JOUR

T1 - Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification

AU - Robertson, Fiona M

AU - Gundappa, Manu Kumar

AU - Grammes, Fabian

AU - Hvidsten, Torgeir R.

AU - Redmond, Anthony

AU - Lien, Sigbjorn

AU - Holland, Peter W.H.

AU - Martin, Samuel A. M.

AU - Sandve, Simen R.

AU - MacQueen, Daniel J.

N1 - Funding The study was funded by a Natural Environment Research Council (NERC) grant (NBAF704). FMR is funded by a NERC Doctoral Training Grant (NE/L50175X/1). MKG is funded by an Elphinstone PhD Scholarship from the University of Aberdeen, with additional financial support from a scholarship from the Government of Karnataka, India. Availability of data and materials Illumina sequence reads for the sequence capture study were deposited in NCBI (Bioproject PRJNA325617). All sequence alignments and phylogenetic trees used for phylogenomics are provided in Additional file 2 . Illumina sequence reads for the tissue expression study performed under controlled conditions can be found in the NCBI SRA database (accessions SRX608594, SRS64003, SRS640030, SRS640015, SRS640003, SRS639997, SRS639041, SRS640021, SRS639990l, SRS639861, SRS640009, SRS639992, SRS639037, SRS640002, SRS639994). Illumina sequence reads for the fresh to saltwater transition experiment were deposited in the European Nucleotide Archive (accession number SRP095919).

PY - 2017/6/14

Y1 - 2017/6/14

N2 - Background The functional divergence of duplicate genes (ohnologues) retained from whole genome duplication (WGD) is thought to promote evolutionary diversification. However, species radiation and phenotypic diversification is often temporally separated from WGD. Salmonid fish, whose ancestor underwent WGD by autotetraploidization ~95 Ma fit such a 'time-lag' model of post-WGD radiation, which occurred alongside a major delay in the rediploidization process. Here we propose a model, 'lineage-specific ohnologue resolution' (LORe), to address the consequences of delayed rediploidization. Under LORe, speciation precedes rediploidization, allowing independent ohnologue divergence in sister lineages sharing an ancestral WGD event. Results Using cross-species sequence capture, phylogenomics and genome-wide analyses of ohnologue expression divergence, we demonstrate the major impact of LORe on salmonid evolution. One quarter of each salmonid genome, harbouring at least 4,550 ohnologues, has evolved under LORe, with rediploidization and functional divergence occurring on multiple independent occasions > 50 Myr post-WGD. We demonstrate the existence and regulatory divergence of many LORe ohnologues with functions in lineage-specific physiological adaptations that potentially facilitated salmonid species radiation. We show that LORe ohnologues are enriched for different functions than 'older' ohnologues that began diverging in the salmonid ancestor. Conclusions LORe has unappreciated significance as a nested component of post-WGD divergence that impacts the functional properties of genes, whilst providing ohnologues available solely for lineage-specific adaptation. Under LORe, which is predicted following many WGD events, the functional outcomes of WGD need not appear 'explosively', but can arise gradually over tens of Myr, promoting lineage-specific diversification regimes under prevailing ecological pressures.

AB - Background The functional divergence of duplicate genes (ohnologues) retained from whole genome duplication (WGD) is thought to promote evolutionary diversification. However, species radiation and phenotypic diversification is often temporally separated from WGD. Salmonid fish, whose ancestor underwent WGD by autotetraploidization ~95 Ma fit such a 'time-lag' model of post-WGD radiation, which occurred alongside a major delay in the rediploidization process. Here we propose a model, 'lineage-specific ohnologue resolution' (LORe), to address the consequences of delayed rediploidization. Under LORe, speciation precedes rediploidization, allowing independent ohnologue divergence in sister lineages sharing an ancestral WGD event. Results Using cross-species sequence capture, phylogenomics and genome-wide analyses of ohnologue expression divergence, we demonstrate the major impact of LORe on salmonid evolution. One quarter of each salmonid genome, harbouring at least 4,550 ohnologues, has evolved under LORe, with rediploidization and functional divergence occurring on multiple independent occasions > 50 Myr post-WGD. We demonstrate the existence and regulatory divergence of many LORe ohnologues with functions in lineage-specific physiological adaptations that potentially facilitated salmonid species radiation. We show that LORe ohnologues are enriched for different functions than 'older' ohnologues that began diverging in the salmonid ancestor. Conclusions LORe has unappreciated significance as a nested component of post-WGD divergence that impacts the functional properties of genes, whilst providing ohnologues available solely for lineage-specific adaptation. Under LORe, which is predicted following many WGD events, the functional outcomes of WGD need not appear 'explosively', but can arise gradually over tens of Myr, promoting lineage-specific diversification regimes under prevailing ecological pressures.

KW - whole genome duplication

KW - rediploidization

KW - species radiation

KW - Lineage-specific Ohnologue Resolution (LORe)

KW - duplicate genes

KW - functional divergence

KW - autotetraploidization

KW - salmonid fish

U2 - 10.1186/s13059-017-1241-z

DO - 10.1186/s13059-017-1241-z

M3 - Article

C2 - 28615063

VL - 18

JO - Genome Biology

JF - Genome Biology

SN - 1474-760X

M1 - 111

ER -