Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates

Background Provision of long-chain polyunsaturated fatty acids (LC-PUFA) in vertebrates occurs through the diet or via endogenous production from C18 precursors through consecutive elongations and desaturations. It has been postulated that the abundance of LC-PUFA in the marine environment has remar...

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Published in:BMC Evolutionary Biology
Main Authors: Lopes-Marques, Monica, Kabeya, Naoki, Qian, Yu, Ruivo, Raquel, Santos, Miguel, Venkatesh, Byrappa, Tocher, Douglas R, Castro, L Filipe C, Monroig, Oscar
Other Authors: University of Porto, University of Tokyo, Institute of Aquaculture, orcid:0000-0002-8603-9410, orcid:0000-0001-8712-0440
Format: Article in Journal/Newspaper
Language:English
Published: BMC 2018
Subjects:
Online Access:http://hdl.handle.net/1893/28256
https://doi.org/10.1186/s12862-018-1271-5
http://dspace.stir.ac.uk/bitstream/1893/28256/1/LopezMarquesRetentionOfFattyAcylDesaturase.pdf
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spelling ftunivstirling:oai:dspace.stir.ac.uk:1893/28256 2023-05-15T15:11:31+02:00 Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates Lopes-Marques, Monica Kabeya, Naoki Qian, Yu Ruivo, Raquel Santos, Miguel Venkatesh, Byrappa Tocher, Douglas R Castro, L Filipe C Monroig, Oscar University of Porto University of Tokyo Institute of Aquaculture orcid:0000-0002-8603-9410 orcid:0000-0001-8712-0440 2018-10-19 application/pdf http://hdl.handle.net/1893/28256 https://doi.org/10.1186/s12862-018-1271-5 http://dspace.stir.ac.uk/bitstream/1893/28256/1/LopezMarquesRetentionOfFattyAcylDesaturase.pdf en eng BMC Lopes-Marques M, Kabeya N, Qian Y, Ruivo R, Santos M, Venkatesh B, Tocher DR, Castro LFC & Monroig O (2018) Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates. BMC Evolutionary Biology, 18, Art. No.: 157. https://doi.org/10.1186/s12862-018-1271-5 157 http://hdl.handle.net/1893/28256 doi:10.1186/s12862-018-1271-5 30340454 1041093 http://dspace.stir.ac.uk/bitstream/1893/28256/1/LopezMarquesRetentionOfFattyAcylDesaturase.pdf © The Author(s). 2018 This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. http://creativecommons.org/licenses/by/4.0/ CC0 PDM CC-BY Biosynthesis Fatty acyl desaturase Gene duplication Gene loss Long-chain polyunsaturated fatty acids Journal Article VoR - Version of Record 2018 ftunivstirling https://doi.org/10.1186/s12862-018-1271-5 2022-06-13T18:42:22Z Background Provision of long-chain polyunsaturated fatty acids (LC-PUFA) in vertebrates occurs through the diet or via endogenous production from C18 precursors through consecutive elongations and desaturations. It has been postulated that the abundance of LC-PUFA in the marine environment has remarkably modulated the gene complement and function of Fads in marine teleosts. In vertebrates two fatty acyl desaturases, namely Fads1 and Fads2, encode ∆5 and ∆6 desaturases, respectively. To fully clarify the evolutionary history of LC-PUFA biosynthesis in vertebrates, we investigated the gene repertoire and function of Fads from species placed at key evolutionary nodes. Results We demonstrate that functional Fads1Δ5 and Fads2∆6 arose from a tandem gene duplication in the ancestor of vertebrates, since they are present in the Arctic lamprey. Additionally, we show that a similar condition was retained in ray-finned fish such as the Senegal bichir and spotted gar, with the identification of fads1 genes in these lineages. Functional characterisation of the isolated desaturases reveals the first case of a Fads1 enzyme with ∆5 desaturase activity in the Teleostei lineage, the Elopomorpha. In contrast, in Osteoglossomorpha genomes, while no fads1 was identified, two separate fads2 duplicates with ∆6 and ∆5 desaturase activities respectively were uncovered. Conclusions We conclude that, while the essential genetic components involved LC-PUFA biosynthesis evolved in the vertebrate ancestor, the full completion of the LC-PUFA biosynthesis pathway arose uniquely in gnathostomes. Article in Journal/Newspaper Arctic University of Stirling: Stirling Digital Research Repository Arctic Gar’ ENVELOPE(162.014,162.014,57.140,57.140) BMC Evolutionary Biology 18 1
institution Open Polar
collection University of Stirling: Stirling Digital Research Repository
op_collection_id ftunivstirling
language English
topic Biosynthesis
Fatty acyl desaturase
Gene duplication
Gene loss
Long-chain polyunsaturated fatty acids
spellingShingle Biosynthesis
Fatty acyl desaturase
Gene duplication
Gene loss
Long-chain polyunsaturated fatty acids
Lopes-Marques, Monica
Kabeya, Naoki
Qian, Yu
Ruivo, Raquel
Santos, Miguel
Venkatesh, Byrappa
Tocher, Douglas R
Castro, L Filipe C
Monroig, Oscar
Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates
topic_facet Biosynthesis
Fatty acyl desaturase
Gene duplication
Gene loss
Long-chain polyunsaturated fatty acids
description Background Provision of long-chain polyunsaturated fatty acids (LC-PUFA) in vertebrates occurs through the diet or via endogenous production from C18 precursors through consecutive elongations and desaturations. It has been postulated that the abundance of LC-PUFA in the marine environment has remarkably modulated the gene complement and function of Fads in marine teleosts. In vertebrates two fatty acyl desaturases, namely Fads1 and Fads2, encode ∆5 and ∆6 desaturases, respectively. To fully clarify the evolutionary history of LC-PUFA biosynthesis in vertebrates, we investigated the gene repertoire and function of Fads from species placed at key evolutionary nodes. Results We demonstrate that functional Fads1Δ5 and Fads2∆6 arose from a tandem gene duplication in the ancestor of vertebrates, since they are present in the Arctic lamprey. Additionally, we show that a similar condition was retained in ray-finned fish such as the Senegal bichir and spotted gar, with the identification of fads1 genes in these lineages. Functional characterisation of the isolated desaturases reveals the first case of a Fads1 enzyme with ∆5 desaturase activity in the Teleostei lineage, the Elopomorpha. In contrast, in Osteoglossomorpha genomes, while no fads1 was identified, two separate fads2 duplicates with ∆6 and ∆5 desaturase activities respectively were uncovered. Conclusions We conclude that, while the essential genetic components involved LC-PUFA biosynthesis evolved in the vertebrate ancestor, the full completion of the LC-PUFA biosynthesis pathway arose uniquely in gnathostomes.
author2 University of Porto
University of Tokyo
Institute of Aquaculture
orcid:0000-0002-8603-9410
orcid:0000-0001-8712-0440
format Article in Journal/Newspaper
author Lopes-Marques, Monica
Kabeya, Naoki
Qian, Yu
Ruivo, Raquel
Santos, Miguel
Venkatesh, Byrappa
Tocher, Douglas R
Castro, L Filipe C
Monroig, Oscar
author_facet Lopes-Marques, Monica
Kabeya, Naoki
Qian, Yu
Ruivo, Raquel
Santos, Miguel
Venkatesh, Byrappa
Tocher, Douglas R
Castro, L Filipe C
Monroig, Oscar
author_sort Lopes-Marques, Monica
title Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates
title_short Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates
title_full Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates
title_fullStr Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates
title_full_unstemmed Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates
title_sort retention of fatty acyl desaturase 1 (fads1) in elopomorpha and cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates
publisher BMC
publishDate 2018
url http://hdl.handle.net/1893/28256
https://doi.org/10.1186/s12862-018-1271-5
http://dspace.stir.ac.uk/bitstream/1893/28256/1/LopezMarquesRetentionOfFattyAcylDesaturase.pdf
long_lat ENVELOPE(162.014,162.014,57.140,57.140)
geographic Arctic
Gar’
geographic_facet Arctic
Gar’
genre Arctic
genre_facet Arctic
op_relation Lopes-Marques M, Kabeya N, Qian Y, Ruivo R, Santos M, Venkatesh B, Tocher DR, Castro LFC & Monroig O (2018) Retention of fatty acyl desaturase 1 (fads1) in Elopomorpha and Cyclostomata provides novel insights into the evolution of long-chain polyunsaturated fatty acid biosynthesis in vertebrates. BMC Evolutionary Biology, 18, Art. No.: 157. https://doi.org/10.1186/s12862-018-1271-5
157
http://hdl.handle.net/1893/28256
doi:10.1186/s12862-018-1271-5
30340454
1041093
http://dspace.stir.ac.uk/bitstream/1893/28256/1/LopezMarquesRetentionOfFattyAcylDesaturase.pdf
op_rights © The Author(s). 2018 This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
http://creativecommons.org/licenses/by/4.0/
op_rightsnorm CC0
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CC-BY
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