Gene-Diet Interactions: Dietary Rescue of Metabolic Effects in spen-Depleted Drosophila melanogaster

Genetics. 2020 Apr;214(4):961-975. doi: 10.1534/genetics.119.303015. Epub 2020 Feb 27.

Abstract

Obesity and its comorbidities are a growing health epidemic. Interactions between genetic background, the environment, and behavior (i.e., diet) greatly influence organismal energy balance. Previously, we described obesogenic mutations in the gene Split ends (Spen) in Drosophila melanogaster, and roles for Spen in fat storage and metabolic state. Lipid catabolism is impaired in Spen-deficient fat storage cells, accompanied by a compensatory increase in glycolytic flux and protein catabolism. Here, we investigate gene-diet interactions to determine if diets supplemented with specific macronutrients can rescue metabolic dysfunction in Spen-depleted animals. We show that a high-yeast diet partially rescues adiposity and developmental defects. High sugar partially improves developmental timing as well as longevity of mated females. Gene-diet interactions were heavily influenced by developmental-stage-specific organismal needs: extra yeast provides benefits early in development (larval stages) but becomes detrimental in adulthood. High sugar confers benefits to Spen-depleted animals at both larval and adult stages, with the caveat of increased adiposity. A high-fat diet is detrimental according to all tested criteria, regardless of genotype. Whereas Spen depletion influenced phenotypic responses to supplemented diets, diet was the dominant factor in directing the whole-organism steady-state metabolome. Obesity is a complex disease of genetic, environmental, and behavioral inputs. Our results show that diet customization can ameliorate metabolic dysfunction underpinned by a genetic factor.

Keywords: Drosophila melanogaster; Spen; fat body; gene–diet interaction; metabolism.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Diet*
  • Dietary Carbohydrates / metabolism
  • Drosophila Proteins / deficiency
  • Drosophila Proteins / genetics*
  • Drosophila melanogaster
  • Fat Body / metabolism
  • Gene-Environment Interaction*
  • Glycolysis
  • Homeodomain Proteins / genetics*
  • Larva / growth & development
  • Larva / metabolism
  • Lipid Metabolism
  • Metabolome*
  • RNA-Binding Proteins / genetics*

Substances

  • Dietary Carbohydrates
  • Drosophila Proteins
  • Homeodomain Proteins
  • RNA-Binding Proteins
  • Spen protein, Drosophila