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

Mark Lammers, Ken Kraaijeveld, Janine Mariën, Jacintha Ellers

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

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.

LanguageEnglish
Article number309
JournalBMC Genomics
Volume20
DOIs
Publication statusPublished - 23 Apr 2019

Fingerprint

Lipogenesis
Gene Expression
Genes
malonyl-CoA decarboxylase
Metabolic Networks and Pathways
Hydroxymethylglutaryl-CoA Synthase
Fatty Acids
Dietary Sucrose
Wasps
Acetyl Coenzyme A
Drosophila melanogaster
Insects
Carbohydrates
Lipids

Keywords

  • Comparative transcriptomics
  • Fatty acid auxotrophy
  • Lipogenesis
  • Parasitoid lifestyle
  • Pleiotropy
  • RNA-seq
  • Trait loss

Cite this

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title = "Gene expression changes associated with the evolutionary loss of a metabolic trait: Lack of lipogenesis in parasitoids",
abstract = "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.",
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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.

In: BMC Genomics, Vol. 20, 309, 23.04.2019.

Research output: Contribution to JournalArticleAcademicpeer-review

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T1 - Gene expression changes associated with the evolutionary loss of a metabolic trait

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AU - Lammers, Mark

AU - Kraaijeveld, Ken

AU - Mariën, Janine

AU - Ellers, Jacintha

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Y1 - 2019/4/23

N2 - 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.

AB - 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.

KW - Comparative transcriptomics

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KW - RNA-seq

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