Mitonuclear interactions shape both direct and parental effects of diet on fitness, and involve a SNP in mitoribosomal 16s rRNA

Dobson, A. , Voigt, S., Kumpitsch, L., Langer, L., Voigt, E., Ibrahim, R., Dowling, D. and Reinhardt, K. (2023) Mitonuclear interactions shape both direct and parental effects of diet on fitness, and involve a SNP in mitoribosomal 16s rRNA. PLoS Biology, 21(8), e3002218. (doi: 10.1371/journal.pbio.3002218) (PMID:37603597) (PMCID:PMC10441796)

Abstract

Nutrition is a primary determinant of health, but responses to nutrition vary with genotype. Epistasis between mitochondrial and nuclear genomes may cause some of this variation, but which mitochondrial loci and nutrients participate in complex gene-by-gene-by-diet interactions? Furthermore, it remains unknown whether mitonuclear epistasis is involved only in the immediate responses to changes in diet, or whether mitonuclear genotype might modulate sensitivity to variation in parental nutrition, to shape intergenerational fitness responses. Here, in Drosophila melanogaster, we show that mitonuclear epistasis shapes fitness responses to variation in dietary lipids and amino acids. We also show that mitonuclear genotype modulates the parental effect of dietary lipid and amino acid variation on offspring fitness. Effect sizes for the interactions between diet, mitogenotype, and nucleogenotype were equal to or greater than the main effect of diet for some traits, suggesting that dietary impacts cannot be understood without first accounting for these interactions. Associating phenotype to mtDNA variation in a subset of populations implicated a C/T polymorphism in mt:lrRNA, which encodes the 16S rRNA of the mitochondrial ribosome. This association suggests that directionally different responses to dietary changes can result from variants on mtDNA that do not change protein coding sequence, dependent on epistatic interactions with variation in the nuclear genome.

• Item Type: Articles
• Additional Information: This work was supported by a Dresden Fellowship funded by the Excellence Initiative of the German Federal and State Governments to A.D., a UKRI Future Leaders Fellowship (MR/S033939/1) to A.D., a University of Glasgow Lord Kelvin Adam Smith Fellowship to A.D., and Deutsche Forschungsgemeinschaft grant RE 1666/9-1 to K.R.
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Dobson, Dr Adam and Ibrahim, Rita
• Authors: Dobson, A., Voigt, S., Kumpitsch, L., Langer, L., Voigt, E., Ibrahim, R., Dowling, D., and Reinhardt, K.
• College/School: College of Medical Veterinary and Life Sciences > School of Molecular Biosciences
• Journal Name: PLoS Biology
• Publisher: Public Library of Science
• ISSN: 1544-9173
• ISSN (Online): 1545-7885
• Copyright Holders: Copyright © 2023 The Authors
• First Published: First published in PLoS Biology 21(8):e3002218
• Publisher Policy: Reproduced under a Creative Commons License

Project Code	Award No	Project Name	Principal Investigator	Funder's Name	Funder Ref	Lead Dept
305846		Remote control: How do microbiota promote animal health?	Adam Dobson	Medical Research Council (MRC)	MR/S033939/1	School of Molecular Biosciences