Mitonuclear interactions shape both direct and parental effects of diet on fitness and involve a SNP in mitoribosomal 16s rRNA
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 rema...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2023-08-01
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| Series: | PLoS Biology |
| Online Access: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10441796/?tool=EBI |
| _version_ | 1797737297802690560 |
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| author | Adam J. Dobson Susanne Voigt Luisa Kumpitsch Lucas Langer Emmely Voigt Rita Ibrahim Damian K. Dowling Klaus Reinhardt |
| author_facet | Adam J. Dobson Susanne Voigt Luisa Kumpitsch Lucas Langer Emmely Voigt Rita Ibrahim Damian K. Dowling Klaus Reinhardt |
| author_sort | Adam J. Dobson |
| collection | DOAJ |
| description | 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. Why do genetically distinct individuals show differing responses to dietary change? This study investigates how genetic differences in mitochondria and the nucleus interact to determine fitness response to direct manipulation of diet, finding that the effects depend on essential amino acids and lipids, and a SNP in the mitochondrial 16S rRNA. |
| first_indexed | 2024-03-12T13:26:39Z |
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| id | doaj.art-8eba41efe58f4e7ab5fce80d86655a64 |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-03-12T13:26:39Z |
| publishDate | 2023-08-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-8eba41efe58f4e7ab5fce80d86655a642023-08-25T05:30:52ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-08-01218Mitonuclear interactions shape both direct and parental effects of diet on fitness and involve a SNP in mitoribosomal 16s rRNAAdam J. DobsonSusanne VoigtLuisa KumpitschLucas LangerEmmely VoigtRita IbrahimDamian K. DowlingKlaus ReinhardtNutrition 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. Why do genetically distinct individuals show differing responses to dietary change? This study investigates how genetic differences in mitochondria and the nucleus interact to determine fitness response to direct manipulation of diet, finding that the effects depend on essential amino acids and lipids, and a SNP in the mitochondrial 16S rRNA.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10441796/?tool=EBI |
| spellingShingle | Adam J. Dobson Susanne Voigt Luisa Kumpitsch Lucas Langer Emmely Voigt Rita Ibrahim Damian K. Dowling Klaus Reinhardt Mitonuclear interactions shape both direct and parental effects of diet on fitness and involve a SNP in mitoribosomal 16s rRNA PLoS Biology |
| title | Mitonuclear interactions shape both direct and parental effects of diet on fitness and involve a SNP in mitoribosomal 16s rRNA |
| title_full | Mitonuclear interactions shape both direct and parental effects of diet on fitness and involve a SNP in mitoribosomal 16s rRNA |
| title_fullStr | Mitonuclear interactions shape both direct and parental effects of diet on fitness and involve a SNP in mitoribosomal 16s rRNA |
| title_full_unstemmed | Mitonuclear interactions shape both direct and parental effects of diet on fitness and involve a SNP in mitoribosomal 16s rRNA |
| title_short | Mitonuclear interactions shape both direct and parental effects of diet on fitness and involve a SNP in mitoribosomal 16s rRNA |
| title_sort | mitonuclear interactions shape both direct and parental effects of diet on fitness and involve a snp in mitoribosomal 16s rrna |
| url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10441796/?tool=EBI |
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