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Transcriptional development of phospholipid and lipoprotein metabolism in different intestinal regions of Atlantic salmon (Salmo salar) fry

BACKGROUND: It has been suggested that the high phospholipid (PL) requirement in Atlantic salmon (Salmo salar) fry is due to insufficient intestinal de-novo synthesis causing low lipoprotein (LP) production and reduced transport capacity of dietary lipids. However, in-depth ontogenetic analysis of i...

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Autores principales: Jin, Yang, Olsen, Rolf Erik, Østensen, Mari-Ann, Gillard, Gareth Benjamin, Korsvoll, Sven Arild, Santi, Nina, Gjuvsland, Arne Bjørke, Vik, Jon Olav, Torgersen, Jacob Seilø, Sandve, Simen Rød, Olsen, Yngvar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5902856/
https://www.ncbi.nlm.nih.gov/pubmed/29661132
http://dx.doi.org/10.1186/s12864-018-4651-8
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author Jin, Yang
Olsen, Rolf Erik
Østensen, Mari-Ann
Gillard, Gareth Benjamin
Korsvoll, Sven Arild
Santi, Nina
Gjuvsland, Arne Bjørke
Vik, Jon Olav
Torgersen, Jacob Seilø
Sandve, Simen Rød
Olsen, Yngvar
author_facet Jin, Yang
Olsen, Rolf Erik
Østensen, Mari-Ann
Gillard, Gareth Benjamin
Korsvoll, Sven Arild
Santi, Nina
Gjuvsland, Arne Bjørke
Vik, Jon Olav
Torgersen, Jacob Seilø
Sandve, Simen Rød
Olsen, Yngvar
author_sort Jin, Yang
collection PubMed
description BACKGROUND: It has been suggested that the high phospholipid (PL) requirement in Atlantic salmon (Salmo salar) fry is due to insufficient intestinal de-novo synthesis causing low lipoprotein (LP) production and reduced transport capacity of dietary lipids. However, in-depth ontogenetic analysis of intestinal PL and LP synthesis with the development of salmon has yet to be performed. Therefore, in this paper we used RNA-Seq technology to investigate the expression of genes involved in PL synthesis and LP formation throughout early developmental stages and associate insufficient expression of synthesis pathways in salmon fry with its higher dietary PL requirement. There was a special focus on the understanding homologous genes, especially those from salmonid-specific fourth vertebrate whole-genome duplication (Ss4R), and their contribution to salmonid specific features of regulation of PL metabolic pathways. Salmon fry were sampled at 0.16 g (1 day before first-feeding), 2.5 and 10 g stages of development and transcriptomic analysis was applied separately on stomach, pyloric caeca and hindgut of the fish. RESULTS: In general, we found up-regulated pathways involved in synthesis of phosphatidylcholine (PtdCho), phosphatidylethanolamine (PtdEtn), and LP in pyloric caeca of salmon between 0.16 and 10 g. Thirteen differentially expressed genes (q < 0.05) in these pathways were highly up-regulated in 2.5 g salmon compared to 0.16 g, while only five more differentially expressed (q < 0.05) genes were found when the fish grew up to 10 g. Different homologous genes were found dominating in stomach, pyloric caeca and hindgut. However, the expression of dominating genes in pathways of PL and LP synthesis were much higher in pyloric caeca than stomach and hindgut. Salmon-specific homologous genes (Ss4R) had similar expression during development, while other homologs had more diverged expression. CONCLUSIONS: The up-regulation of the de-novo PtdCho and PtdEtn pathways confirm that salmon have decreasing requirement for dietary PL as the fish develops. The similar expressions between Ss4R homologous genes suggest that the functional divergence of these genes was incomplete compared to homologs derived from other genome duplication. The results of the present study have provided new information on the molecular mechanisms of phospholipid synthesis and lipoprotein formation in fish. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4651-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-59028562018-04-23 Transcriptional development of phospholipid and lipoprotein metabolism in different intestinal regions of Atlantic salmon (Salmo salar) fry Jin, Yang Olsen, Rolf Erik Østensen, Mari-Ann Gillard, Gareth Benjamin Korsvoll, Sven Arild Santi, Nina Gjuvsland, Arne Bjørke Vik, Jon Olav Torgersen, Jacob Seilø Sandve, Simen Rød Olsen, Yngvar BMC Genomics Research Article BACKGROUND: It has been suggested that the high phospholipid (PL) requirement in Atlantic salmon (Salmo salar) fry is due to insufficient intestinal de-novo synthesis causing low lipoprotein (LP) production and reduced transport capacity of dietary lipids. However, in-depth ontogenetic analysis of intestinal PL and LP synthesis with the development of salmon has yet to be performed. Therefore, in this paper we used RNA-Seq technology to investigate the expression of genes involved in PL synthesis and LP formation throughout early developmental stages and associate insufficient expression of synthesis pathways in salmon fry with its higher dietary PL requirement. There was a special focus on the understanding homologous genes, especially those from salmonid-specific fourth vertebrate whole-genome duplication (Ss4R), and their contribution to salmonid specific features of regulation of PL metabolic pathways. Salmon fry were sampled at 0.16 g (1 day before first-feeding), 2.5 and 10 g stages of development and transcriptomic analysis was applied separately on stomach, pyloric caeca and hindgut of the fish. RESULTS: In general, we found up-regulated pathways involved in synthesis of phosphatidylcholine (PtdCho), phosphatidylethanolamine (PtdEtn), and LP in pyloric caeca of salmon between 0.16 and 10 g. Thirteen differentially expressed genes (q < 0.05) in these pathways were highly up-regulated in 2.5 g salmon compared to 0.16 g, while only five more differentially expressed (q < 0.05) genes were found when the fish grew up to 10 g. Different homologous genes were found dominating in stomach, pyloric caeca and hindgut. However, the expression of dominating genes in pathways of PL and LP synthesis were much higher in pyloric caeca than stomach and hindgut. Salmon-specific homologous genes (Ss4R) had similar expression during development, while other homologs had more diverged expression. CONCLUSIONS: The up-regulation of the de-novo PtdCho and PtdEtn pathways confirm that salmon have decreasing requirement for dietary PL as the fish develops. The similar expressions between Ss4R homologous genes suggest that the functional divergence of these genes was incomplete compared to homologs derived from other genome duplication. The results of the present study have provided new information on the molecular mechanisms of phospholipid synthesis and lipoprotein formation in fish. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4651-8) contains supplementary material, which is available to authorized users. BioMed Central 2018-04-16 /pmc/articles/PMC5902856/ /pubmed/29661132 http://dx.doi.org/10.1186/s12864-018-4651-8 Text en © The Author(s). 2018 Open AccessThis 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.
spellingShingle Research Article
Jin, Yang
Olsen, Rolf Erik
Østensen, Mari-Ann
Gillard, Gareth Benjamin
Korsvoll, Sven Arild
Santi, Nina
Gjuvsland, Arne Bjørke
Vik, Jon Olav
Torgersen, Jacob Seilø
Sandve, Simen Rød
Olsen, Yngvar
Transcriptional development of phospholipid and lipoprotein metabolism in different intestinal regions of Atlantic salmon (Salmo salar) fry
title Transcriptional development of phospholipid and lipoprotein metabolism in different intestinal regions of Atlantic salmon (Salmo salar) fry
title_full Transcriptional development of phospholipid and lipoprotein metabolism in different intestinal regions of Atlantic salmon (Salmo salar) fry
title_fullStr Transcriptional development of phospholipid and lipoprotein metabolism in different intestinal regions of Atlantic salmon (Salmo salar) fry
title_full_unstemmed Transcriptional development of phospholipid and lipoprotein metabolism in different intestinal regions of Atlantic salmon (Salmo salar) fry
title_short Transcriptional development of phospholipid and lipoprotein metabolism in different intestinal regions of Atlantic salmon (Salmo salar) fry
title_sort transcriptional development of phospholipid and lipoprotein metabolism in different intestinal regions of atlantic salmon (salmo salar) fry
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5902856/
https://www.ncbi.nlm.nih.gov/pubmed/29661132
http://dx.doi.org/10.1186/s12864-018-4651-8
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