Dataset Information

Mitonuclear Epistasis for Development Time and Its Modification by Diet in Drosophila.

ABSTRACT: Mitochondrial (mtDNA) and nuclear genes have to operate in a coordinated manner to maintain organismal function, and the regulation of this homeostasis presents a substantial source of potential epistatic (G × G) interactions. How these interactions shape the fitness landscape is poorly understood. Here we developed a novel mitonuclear epistasis model, using selected strains of the Drosophila Genetic Reference Panel (DGRP) and mitochondrial genomes from within Drosophila melanogaster and D. simulans to test the hypothesis that mtDNA × nDNA interactions influence fitness. In total we built 72 genotypes (12 nuclear backgrounds × 6 mtDNA haplotypes, with 3 from each species) to dissect the relationship between genotype and phenotype. Each genotype was assayed on four food environments. We found considerable variation in several phenotypes, including development time and egg-to-adult viability, and this variation was partitioned into genetic (G), environmental (E), and higher-order (G × G, G × E, and G × G × E) components. Food type had a significant impact on development time and also modified mitonuclear epistases, evidencing a broad spectrum of G × G × E across these genotypes. Nuclear background effects were substantial, followed by mtDNA effects and their G × G interaction. The species of mtDNA haplotype had negligible effects on phenotypic variation and there was no evidence that mtDNA variation has different effects on male and female fitness traits. Our results demonstrate that mitonuclear epistases are context dependent, suggesting the selective pressure acting on mitonuclear genotypes may vary with food environment in a genotype-specific manner.

SUBMITTER: Mossman JA

PROVIDER: S-EPMC4858792 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

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Mitonuclear Epistasis for Development Time and Its Modification by Diet in Drosophila.

Mossman Jim A JA Biancani Leann M LM Zhu Chen-Tseh CT Rand David M DM

Genetics 20160310 1

Mitochondrial (mtDNA) and nuclear genes have to operate in a coordinated manner to maintain organismal function, and the regulation of this homeostasis presents a substantial source of potential epistatic (G × G) interactions. How these interactions shape the fitness landscape is poorly understood. Here we developed a novel mitonuclear epistasis model, using selected strains of the Drosophila Genetic Reference Panel (DGRP) and mitochondrial genomes from within Drosophila melanogaster and D. simu ...[more]

PMID: 26966258

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Project description:Mitochondrial function requires the coordinated expression of dozens of gene products from the mitochondrial genome and hundreds from the nuclear genomes. The systems that emerge from these interactions convert the food we eat and the oxygen we breathe into energy for life, while regulating a wide range of other cellular processes. These facts beg the question of whether the gene-by-gene interactions (G x G) that enable mitochondrial function are distinct from the gene-by-environment interactions (G x E) that fuel mitochondrial activity. We examine this question using a Drosophila model of mitonuclear interactions in which experimental combinations of mtDNA and nuclear chromosomes generate pairs of mitonuclear genotypes to test for epistatic interactions (G x G). These mitonuclear genotypes are then exposed to altered dietary or oxygen environments to test for G x E interactions. We use development time to assess dietary effects, and genome wide RNAseq analyses to assess hypoxic effects on transcription, which can be partitioned in to mito, nuclear, and environmental (G x G x E) contributions to these complex traits. We find that mitonuclear epistasis is universal, and that dietary and hypoxic treatments alter the epistatic interactions. We further show that the transcriptional response to alternative mitonuclear interactions has significant overlap with the transcriptional response to alternative oxygen environments. Gene coexpression analyses suggest that these shared genes are more central in networks of gene interactions, implying some functional overlap between epistasis and genotype by environment interactions. These results are discussed in the context of evolutionary fitness, the genetic basis of complex traits, and the challenge of achieving precision in personalized medicine. © 2018 The Authors. IUBMB Life published by Wiley Periodicals, Inc. on behalf of International Union of Biochemistry and Molecular Biology, 70(12):1275-1288, 2018.

Project description:Trait expression in metazoans is strongly influenced by the balance of macronutrients (i.e. protein, carbohydrate and fat) in the diet. At the same time, an individual's genetic background seems to regulate the magnitude of phenotypic response to a particular diet. It needs to be better understood whether interactions between diet, genetic background and trait expression are found in unicellular eukaryotes. A protist-the slime mould, Physarum polycephalum can choose diets based on protein-to-carbohydrate (P:C) content to support optimal growth rate. Yet, the role of genetic background (variation in the mitochondrial and nuclear DNAs) in mediating growth rate response to dietary P:C ratios in the slime mould is unknown. Here, we studied the effects of interactions between mitochondrial and nuclear DNA haplotypes and diet (i.e. G × G × E interactions) on the growth rate of P. polycephalum. A genetic panel of six distinct strains of P. polycephalum that differ in their mitochondrial and nuclear DNA haplotypes was used to measure growth rate across five diets that varied in their P:C ratio and total calories. We first determined the strains' growth rate (total biomass and surface area) when grown on a set menu with access to a particular diet. We then assessed whether the growth rate of strains increased on a buffet menu with access to all diets. Our findings show that the growth rate of P. polycephalum is generally higher on diets containing more carbohydrates than protein and that total calories negatively affect the growth rate. Three-way interactions between mitochondrial, nuclear haplotypes and dietary P:C ratios affected the strains' surface area of growth but not biomass. Intriguingly, strains did not increase their surface area and biomass when they had access to all diets on the buffet menu. Our findings have broad implications for our understanding of the effect of mitonuclear interactions on trait expression across diverse eukaryotic lineages.

Dataset Information

Mitonuclear Epistasis for Development Time and Its Modification by Diet in Drosophila.

Publications

Mitonuclear Epistasis for Development Time and Its Modification by Diet in Drosophila.

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