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Gene expression changes associated with the evolutionary loss of a metabolic trait: lack of lipogenesis in parasitoids

BACKGROUND: Trait loss is a pervasive phenomenon in evolution, yet the underlying molecular causes have been identified in only a handful of cases. Most of these cases involve loss-of-function mutations in one or more trait-specific genes. However, in parasitoid insects the evolutionary loss of a me...

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Autores principales: Lammers, Mark, Kraaijeveld, Ken, Mariën, Janine, Ellers, Jacintha
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6480896/
https://www.ncbi.nlm.nih.gov/pubmed/31014246
http://dx.doi.org/10.1186/s12864-019-5673-6
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author Lammers, Mark
Kraaijeveld, Ken
Mariën, Janine
Ellers, Jacintha
author_facet Lammers, Mark
Kraaijeveld, Ken
Mariën, Janine
Ellers, Jacintha
author_sort Lammers, Mark
collection PubMed
description BACKGROUND: Trait loss is a pervasive phenomenon in evolution, yet the underlying molecular causes have been identified in only a handful of cases. Most of these cases involve loss-of-function mutations in one or more trait-specific genes. However, in parasitoid insects the evolutionary loss of a metabolic trait is not associated with gene decay. Parasitoids have lost the ability to convert dietary sugars into fatty acids. Earlier research suggests that lack of lipogenesis in the parasitoid wasp Nasonia vitripennis is caused by changes in gene regulation. RESULTS: We compared transcriptomic responses to sugar-feeding in the non-lipogenic parasitoid species Nasonia vitripennis and the lipogenic Drosophila melanogaster. Both species adjusted their metabolism within 4 hours after sugar-feeding, but there were sharp differences between the expression profiles of the two species, especially in the carbohydrate and lipid metabolic pathways. Several genes coding for key enzymes in acetyl-CoA metabolism, such as malonyl-CoA decarboxylase (mcd) and HMG-CoA synthase (hmgs) differed in expression between the two species. Their combined action likely blocks lipogenesis in the parasitoid species. Network-based analysis showed connectivity of genes to be negatively correlated to the fold change of gene expression. Furthermore, genes involved in the fatty acid metabolic pathway were more connected than the set of genes of all metabolic pathways combined. CONCLUSION: High connectivity of lipogenesis genes is indicative of pleiotropic effects and could explain the absence of gene degradation. We conclude that modification of expression levels of only a few little-connected genes, such as mcd, is sufficient to enable complete loss of lipogenesis in N. vitripennis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5673-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-64808962019-05-02 Gene expression changes associated with the evolutionary loss of a metabolic trait: lack of lipogenesis in parasitoids Lammers, Mark Kraaijeveld, Ken Mariën, Janine Ellers, Jacintha BMC Genomics Research Article BACKGROUND: Trait loss is a pervasive phenomenon in evolution, yet the underlying molecular causes have been identified in only a handful of cases. Most of these cases involve loss-of-function mutations in one or more trait-specific genes. However, in parasitoid insects the evolutionary loss of a metabolic trait is not associated with gene decay. Parasitoids have lost the ability to convert dietary sugars into fatty acids. Earlier research suggests that lack of lipogenesis in the parasitoid wasp Nasonia vitripennis is caused by changes in gene regulation. RESULTS: We compared transcriptomic responses to sugar-feeding in the non-lipogenic parasitoid species Nasonia vitripennis and the lipogenic Drosophila melanogaster. Both species adjusted their metabolism within 4 hours after sugar-feeding, but there were sharp differences between the expression profiles of the two species, especially in the carbohydrate and lipid metabolic pathways. Several genes coding for key enzymes in acetyl-CoA metabolism, such as malonyl-CoA decarboxylase (mcd) and HMG-CoA synthase (hmgs) differed in expression between the two species. Their combined action likely blocks lipogenesis in the parasitoid species. Network-based analysis showed connectivity of genes to be negatively correlated to the fold change of gene expression. Furthermore, genes involved in the fatty acid metabolic pathway were more connected than the set of genes of all metabolic pathways combined. CONCLUSION: High connectivity of lipogenesis genes is indicative of pleiotropic effects and could explain the absence of gene degradation. We conclude that modification of expression levels of only a few little-connected genes, such as mcd, is sufficient to enable complete loss of lipogenesis in N. vitripennis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5673-6) contains supplementary material, which is available to authorized users. BioMed Central 2019-04-23 /pmc/articles/PMC6480896/ /pubmed/31014246 http://dx.doi.org/10.1186/s12864-019-5673-6 Text en © The Author(s). 2019 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
Lammers, Mark
Kraaijeveld, Ken
Mariën, Janine
Ellers, Jacintha
Gene expression changes associated with the evolutionary loss of a metabolic trait: lack of lipogenesis in parasitoids
title Gene expression changes associated with the evolutionary loss of a metabolic trait: lack of lipogenesis in parasitoids
title_full Gene expression changes associated with the evolutionary loss of a metabolic trait: lack of lipogenesis in parasitoids
title_fullStr Gene expression changes associated with the evolutionary loss of a metabolic trait: lack of lipogenesis in parasitoids
title_full_unstemmed Gene expression changes associated with the evolutionary loss of a metabolic trait: lack of lipogenesis in parasitoids
title_short Gene expression changes associated with the evolutionary loss of a metabolic trait: lack of lipogenesis in parasitoids
title_sort gene expression changes associated with the evolutionary loss of a metabolic trait: lack of lipogenesis in parasitoids
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6480896/
https://www.ncbi.nlm.nih.gov/pubmed/31014246
http://dx.doi.org/10.1186/s12864-019-5673-6
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