Coordination of gene expression between organellar and nuclear genomes

Woodson, Jesse D.; Chory, Joanne

doi:10.1038/nrg2348

Cited by 590 publications

(554 citation statements)

References 140 publications

(179 reference statements)

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“…Several studies indicate a close relationship between the rDNA arrays, ribosomal biogenesis and the mitochondria [10][11][12][13] . For instance, recent evidence points to the import of 5S rRNAs into the mitochondria through a highly regulated process 35,36 .…”

Section: Resultsmentioning

confidence: 99%

“…These results might reflect the synchronization of GE between the nuclear and mitochondrial genomes in a concerted effort to control proper levels of protein production for mitochondria assembly and intracellular homeostasis. Retrograde signalling is an essential mechanism in which organelles communicate with the nucleus to convey a response from fluctuating environmental or cellular conditions 10 . Indeed, we found that genes whose expression is negatively correlated with rDNA dosage were functionally enriched for carbonyl reductase (NADPH) activity (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…1), are present at variable levels in cells and interact with nuclear ribosomes through coordinated processes [8][9][10] . Indeed, functional relationships between the rRNA transcription and the mitochondria are evident [10][11][12][13] . Finally, analyses in Drosophila indicated that the expression of genes that localize to the mitochondria is responsive to engineered deletions that decreased rDNA CN 8 .…”

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confidence: 99%

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Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans

et al. 2014

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Ribosomes are essential intracellular machines composed of proteins and RNA molecules. The DNA sequences (rDNA) encoding ribosomal RNAs (rRNAs) are tandemly repeated and give origin to the nucleolus. Here we develop a computational method for estimating rDNA dosage (copy number) and mitochondrial DNA abundance using whole-genome short-read DNA sequencing. We estimate these attributes across hundreds of human genomes and their association with global gene expression. The analyses uncover abundant variation in rDNA dosage that is coupled with the expression of hundreds of functionally coherent gene sets. These include associations with genes coding for chromatin components that target the nucleolus, including CTCF and HP1b. Finally, the data show an inverse association between rDNA dosage and mitochondrial DNA abundance that is manifested across genotypes. Our findings uncover a novel and cryptic source of hypervariable genomic diversity with global regulatory consequences (ribosomal eQTL) in humans. The variation provides a mechanism for cellular homeostasis and for rapid and reversible adaptation.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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confidence: 99%

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Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans

et al. 2014

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“…Because mt genes are tightly coadapted with N‐mt genes (Woodson and Chory 2008; Lane 2011; Burton et al. 2013), adaptive divergence in a mt gene will inevitably entail coevolution with its coadapted N‐mt genes (Hill 2014; Levin et al.…”

Section: Speciation Via Mitonuclear Coevolution To Maintain Coadaptationmentioning

confidence: 99%

Mitonuclear coevolution as the genesis of speciation and the mitochondrial DNA barcode gap

Hill

2016

Ecology and Evolution

149

178

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Mitochondrial genes are widely used in taxonomy and systematics because high mutation rates lead to rapid sequence divergence and because such changes have long been assumed to be neutral with respect to function. In particular, the nucleotide sequence of the mitochondrial gene cytochrome c oxidase subunit 1 has been established as a highly effective DNA barcode for diagnosing the species boundaries of animals. Rarely considered in discussions of mitochondrial evolution in the context of systematics, speciation, or DNA barcodes, however, is the genomic architecture of the eukaryotes: Mitochondrial and nuclear genes must function in tight coordination to produce the complexes of the electron transport chain and enable cellular respiration. Coadaptation of these interacting gene products is essential for organism function. I extend the hypothesis that mitonuclear interactions are integral to the process of speciation. To maintain mitonuclear coadaptation, nuclear genes, which code for proteins in mitochondria that cofunction with the products of mitochondrial genes, must coevolve with rapidly changing mitochondrial genes. Mitonuclear coevolution in isolated populations leads to speciation because population‐specific mitonuclear coadaptations create between‐population mitonuclear incompatibilities and hence barriers to gene flow between populations. In addition, selection for adaptive divergence of products of mitochondrial genes, particularly in response to climate or altitude, can lead to rapid fixation of novel mitochondrial genotypes between populations and consequently to disruption in gene flow between populations as the initiating step in animal speciation. By this model, the defining characteristic of a metazoan species is a coadapted mitonuclear genotype that is incompatible with the coadapted mitochondrial and nuclear genotype of any other population.

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“…Coordinated expression of organelle genome-encoded and nuclear genome-encoded genes is fundamental to a range of cellular processes in eukaryotes 1,2 . Although mitochondrial functions are conserved among eukaryotes, genome structure and the regulatory mechanisms for gene expression in mitochondria are, surprisingly, quite divergent 3 .…”

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confidence: 99%

A poly(A)-specific ribonuclease directly regulates the poly(A) status of mitochondrial mRNA in Arabidopsis

et al. 2013

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Coordination of gene expression in the organelles and the nucleus is important for eukaryotic cell function. Transcriptional and post-transcriptional gene regulation in mitochondria remains incompletely understood in most eukaryotes, including plants. Here we show that poly(A)-specific ribonuclease, which influences the poly(A) status of cytoplasmic mRNA in many eukaryotes, directly regulates the poly(A) tract of mitochondrial mRNA in conjunction with a bacterial-type poly(A) polymerase, AGS1, in Arabidopsis. An Arabidopsis poly(A)-specific ribonuclease-deficient mutant, ahg2-1, accumulates polyadenylated mitochondrial mRNA and shows defects in mitochondrial protein complex levels. Mutations of AGS1 suppress the ahg2-1 phenotype. Mitochondrial localizations of AHG2 and AGS1 are required for their functions in the regulation of the poly(A) tract of mitochondrial mRNA. Our findings suggest that AHG2 and AGS1 constitute a regulatory system that controls mitochondrial mRNA poly(A) status in Arabidopsis.

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Coordination of gene expression between organellar and nuclear genomes

Cited by 590 publications

References 140 publications

Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans

Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans

Mitonuclear coevolution as the genesis of speciation and the mitochondrial DNA barcode gap

A poly(A)-specific ribonuclease directly regulates the poly(A) status of mitochondrial mRNA in Arabidopsis

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