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Mitochondria as environments for the nuclear genome in Drosophila: mitonuclear G×G×E

Mitochondria evolved from a union of microbial cells belonging to distinct lineages that were likely anaerobic. The evolution of eukaryotes required a massive reorganization of the 2 genomes and eventual adaptation to aerobic environments. The nutrients and oxygen that sustain eukaryotic metabolism...

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Autores principales: Rand, David M, Mossman, James A, Spierer, Adam N, Santiago, John A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8851671/
https://www.ncbi.nlm.nih.gov/pubmed/34964900
http://dx.doi.org/10.1093/jhered/esab066
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author Rand, David M
Mossman, James A
Spierer, Adam N
Santiago, John A
author_facet Rand, David M
Mossman, James A
Spierer, Adam N
Santiago, John A
author_sort Rand, David M
collection PubMed
description Mitochondria evolved from a union of microbial cells belonging to distinct lineages that were likely anaerobic. The evolution of eukaryotes required a massive reorganization of the 2 genomes and eventual adaptation to aerobic environments. The nutrients and oxygen that sustain eukaryotic metabolism today are processed in mitochondria through coordinated expression of 37 mitochondrial genes and over 1000 nuclear genes. This puts mitochondria at the nexus of gene-by-gene (G×G) and gene-by-environment (G×E) interactions that sustain life. Here we use a Drosophila model of mitonuclear genetic interactions to explore the notion that mitochondria are environments for the nuclear genome, and vice versa. We construct factorial combinations of mtDNA and nuclear chromosomes to test for epistatic interactions (G×G), and expose these mitonuclear genotypes to altered dietary environments to examine G×E interactions. We use development time and genome-wide RNAseq analyses to assess the relative contributions of mtDNA, nuclear chromosomes, and environmental effects on these traits (mitonuclear G×G×E). We show that the nuclear transcriptional response to alternative mitochondrial “environments” (G×G) has significant overlap with the transcriptional response of mitonuclear genotypes to altered dietary environments. These analyses point to specific transcription factors (e.g., giant) that mediated these interactions, and identified coexpressed modules of genes that may account for the overlap in differentially expressed genes. Roughly 20% of the transcriptome includes G×G genes that are concordant with G×E genes, suggesting that mitonuclear interactions are part of an organism’s environment.
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spelling pubmed-88516712022-02-18 Mitochondria as environments for the nuclear genome in Drosophila: mitonuclear G×G×E Rand, David M Mossman, James A Spierer, Adam N Santiago, John A J Hered Symposium Articles Mitochondria evolved from a union of microbial cells belonging to distinct lineages that were likely anaerobic. The evolution of eukaryotes required a massive reorganization of the 2 genomes and eventual adaptation to aerobic environments. The nutrients and oxygen that sustain eukaryotic metabolism today are processed in mitochondria through coordinated expression of 37 mitochondrial genes and over 1000 nuclear genes. This puts mitochondria at the nexus of gene-by-gene (G×G) and gene-by-environment (G×E) interactions that sustain life. Here we use a Drosophila model of mitonuclear genetic interactions to explore the notion that mitochondria are environments for the nuclear genome, and vice versa. We construct factorial combinations of mtDNA and nuclear chromosomes to test for epistatic interactions (G×G), and expose these mitonuclear genotypes to altered dietary environments to examine G×E interactions. We use development time and genome-wide RNAseq analyses to assess the relative contributions of mtDNA, nuclear chromosomes, and environmental effects on these traits (mitonuclear G×G×E). We show that the nuclear transcriptional response to alternative mitochondrial “environments” (G×G) has significant overlap with the transcriptional response of mitonuclear genotypes to altered dietary environments. These analyses point to specific transcription factors (e.g., giant) that mediated these interactions, and identified coexpressed modules of genes that may account for the overlap in differentially expressed genes. Roughly 20% of the transcriptome includes G×G genes that are concordant with G×E genes, suggesting that mitonuclear interactions are part of an organism’s environment. Oxford University Press 2021-12-29 /pmc/articles/PMC8851671/ /pubmed/34964900 http://dx.doi.org/10.1093/jhered/esab066 Text en © The American Genetic Association. 2021. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Symposium Articles
Rand, David M
Mossman, James A
Spierer, Adam N
Santiago, John A
Mitochondria as environments for the nuclear genome in Drosophila: mitonuclear G×G×E
title Mitochondria as environments for the nuclear genome in Drosophila: mitonuclear G×G×E
title_full Mitochondria as environments for the nuclear genome in Drosophila: mitonuclear G×G×E
title_fullStr Mitochondria as environments for the nuclear genome in Drosophila: mitonuclear G×G×E
title_full_unstemmed Mitochondria as environments for the nuclear genome in Drosophila: mitonuclear G×G×E
title_short Mitochondria as environments for the nuclear genome in Drosophila: mitonuclear G×G×E
title_sort mitochondria as environments for the nuclear genome in drosophila: mitonuclear g×g×e
topic Symposium Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8851671/
https://www.ncbi.nlm.nih.gov/pubmed/34964900
http://dx.doi.org/10.1093/jhered/esab066
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