Functional divergence of type 2 deiodinase paralogs in the atlantic salmon

Marlene Cowie Lorgen, Elisa Casadei, Elżbieta Król, Alex Douglas, Mike J Birnie, Lars O E Ebbesson, Tom O Nilsen, William C Jordan, Even H Jørgensen, Hugues Dardente, David G Hazlerigg, Samuel A M Martin

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

Thyroid hormone (TH) is an ancestral signal linked to seasonal life history transitions throughout vertebrates. TH action depends upon tissue-localized regulation of levels of active TH (triiodothyronine, T3), through spatiotemporal expression of thyroid hormone deiodinase (dio) genes. We investigated the dio gene family in juvenile Atlantic salmon (Salmo salar) parr, which prepare for seaward migration in the spring (smoltification) through TH-dependent changes in physiology. We identified two type 2 deiodinase paralogs, dio2a and dio2b, responsible for conversion of thyroxine (T4) to T3. During smoltification, dio2b was induced in the brain and gills in zones of cell proliferation following increasing day length. Contrastingly, dio2a expression was induced in the gills by transfer to salt water (SW), with the magnitude of the response proportional to the plasma chloride level. This response reflected a selective enrichment for osmotic response elements (OREs) in the dio2a promoter region. Transcriptomic profiling of gill tissue from fish transferred to SW plus or minus the deiodinase inhibitor, iopanoic acid, revealed SW-induced increases in cellular respiration as the principal consequence of gill dio2 activity. Divergent evolution of dio2 paralogs supports organ-specific timing of the TH-dependent events governing the phenotypic plasticity required for migration to sea.

Original languageEnglish
Pages (from-to)936-941
Number of pages6
JournalCurrent Biology
Volume25
Issue number7
Early online date19 Mar 2015
DOIs
Publication statusPublished - 30 Mar 2015

Fingerprint

Salmo salar
Iodide Peroxidase
thyroid hormones
Thyroid Hormones
Saline water
gills
triiodothyronine
saline water
Salts
Triiodothyronine
smoltification
Water
Iopanoic Acid
Cell Respiration
Genes
Tissue
Response Elements
Thyroxine
divergent evolution
Genetic Promoter Regions

Keywords

  • Atlantic Salmon
  • Type 2 Deiodinase Paralogs

Cite this

Functional divergence of type 2 deiodinase paralogs in the atlantic salmon. / Lorgen, Marlene Cowie; Casadei, Elisa; Król, Elżbieta; Douglas, Alex; Birnie, Mike J; Ebbesson, Lars O E; Nilsen, Tom O; Jordan, William C; Jørgensen, Even H; Dardente, Hugues; Hazlerigg, David G; Martin, Samuel A M.

In: Current Biology, Vol. 25, No. 7, 30.03.2015, p. 936-941.

Research output: Contribution to journalArticle

Lorgen, MC, Casadei, E, Król, E, Douglas, A, Birnie, MJ, Ebbesson, LOE, Nilsen, TO, Jordan, WC, Jørgensen, EH, Dardente, H, Hazlerigg, DG & Martin, SAM 2015, 'Functional divergence of type 2 deiodinase paralogs in the atlantic salmon', Current Biology, vol. 25, no. 7, pp. 936-941. https://doi.org/10.1016/j.cub.2015.01.074
Lorgen, Marlene Cowie ; Casadei, Elisa ; Król, Elżbieta ; Douglas, Alex ; Birnie, Mike J ; Ebbesson, Lars O E ; Nilsen, Tom O ; Jordan, William C ; Jørgensen, Even H ; Dardente, Hugues ; Hazlerigg, David G ; Martin, Samuel A M. / Functional divergence of type 2 deiodinase paralogs in the atlantic salmon. In: Current Biology. 2015 ; Vol. 25, No. 7. pp. 936-941.
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T1 - Functional divergence of type 2 deiodinase paralogs in the atlantic salmon

AU - Lorgen, Marlene Cowie

AU - Casadei, Elisa

AU - Król, Elżbieta

AU - Douglas, Alex

AU - Birnie, Mike J

AU - Ebbesson, Lars O E

AU - Nilsen, Tom O

AU - Jordan, William C

AU - Jørgensen, Even H

AU - Dardente, Hugues

AU - Hazlerigg, David G

AU - Martin, Samuel A M

N1 - Acknowledgments: This study was supported by a grant from the Biotechnology and Biological Sciences Research Council (BB/H008063/1) UK to D.G.H. and S.A.M.M. and the Research Council Norway (project #222215) to L.O.E.E. M.L. was funded by a Marine Alliance for Science and Technology for Scotland PhD studentship. The authors wish to thank Valentina Tronci for excellent technical assistance. Copyright © 2015 Elsevier Ltd. All rights reserved.

PY - 2015/3/30

Y1 - 2015/3/30

N2 - Thyroid hormone (TH) is an ancestral signal linked to seasonal life history transitions throughout vertebrates. TH action depends upon tissue-localized regulation of levels of active TH (triiodothyronine, T3), through spatiotemporal expression of thyroid hormone deiodinase (dio) genes. We investigated the dio gene family in juvenile Atlantic salmon (Salmo salar) parr, which prepare for seaward migration in the spring (smoltification) through TH-dependent changes in physiology. We identified two type 2 deiodinase paralogs, dio2a and dio2b, responsible for conversion of thyroxine (T4) to T3. During smoltification, dio2b was induced in the brain and gills in zones of cell proliferation following increasing day length. Contrastingly, dio2a expression was induced in the gills by transfer to salt water (SW), with the magnitude of the response proportional to the plasma chloride level. This response reflected a selective enrichment for osmotic response elements (OREs) in the dio2a promoter region. Transcriptomic profiling of gill tissue from fish transferred to SW plus or minus the deiodinase inhibitor, iopanoic acid, revealed SW-induced increases in cellular respiration as the principal consequence of gill dio2 activity. Divergent evolution of dio2 paralogs supports organ-specific timing of the TH-dependent events governing the phenotypic plasticity required for migration to sea.

AB - Thyroid hormone (TH) is an ancestral signal linked to seasonal life history transitions throughout vertebrates. TH action depends upon tissue-localized regulation of levels of active TH (triiodothyronine, T3), through spatiotemporal expression of thyroid hormone deiodinase (dio) genes. We investigated the dio gene family in juvenile Atlantic salmon (Salmo salar) parr, which prepare for seaward migration in the spring (smoltification) through TH-dependent changes in physiology. We identified two type 2 deiodinase paralogs, dio2a and dio2b, responsible for conversion of thyroxine (T4) to T3. During smoltification, dio2b was induced in the brain and gills in zones of cell proliferation following increasing day length. Contrastingly, dio2a expression was induced in the gills by transfer to salt water (SW), with the magnitude of the response proportional to the plasma chloride level. This response reflected a selective enrichment for osmotic response elements (OREs) in the dio2a promoter region. Transcriptomic profiling of gill tissue from fish transferred to SW plus or minus the deiodinase inhibitor, iopanoic acid, revealed SW-induced increases in cellular respiration as the principal consequence of gill dio2 activity. Divergent evolution of dio2 paralogs supports organ-specific timing of the TH-dependent events governing the phenotypic plasticity required for migration to sea.

KW - Atlantic Salmon

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JO - Current Biology

JF - Current Biology

SN - 0960-9822

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