Coevolution Predicts Direct Interactions between mtDNA-Encoded and nDNA-Encoded Subunits of Oxidative Phosphorylation Complex I

Gershoni, Moran; Fuchs, Angelika; Shani, Naama; Fridman, Yearit; Corral‐Debrinski, Marisol; Aharoni, Amir; Frishman, Dmitrij; Mo, Dan

doi:10.1016/j.jmb.2010.09.029

Cited by 62 publications

(61 citation statements)

References 47 publications

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“…This evidence includes a high proportion of neutral mutations in nuclear and mitochondrial genes encoding respiratory-chain subunits [16]; a concordance in evolutionary rates of these mitochondrial and nuclear genes [17][18][19]; a decline in respiratory function in nuclear cytoplasmic hybrids (cybrids) [20][21][22]; and hybrid breakdown in introgressed populations, caused by mitonuclear incompatibilities [23]. In plants, hybrid breakdown also frequently involves mitonuclear incompatibilities [24].…”

Section: But Mitochondria Demand Genomic Matchingmentioning

confidence: 99%

Mitonuclear match: Optimizing fitness and fertility over generations drives ageing within generations

Lane¹

2011

BioEssays

167

168

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Many conserved eukaryotic traits, including apoptosis, two sexes, speciation and ageing, can be causally linked to a bioenergetic requirement for mitochondrial genes. Mitochondrial genes encode proteins involved in cell respiration, which interact closely with proteins encoded by nuclear genes. Functional respiration requires the coadaptation of mitochondrial and nuclear genes, despite divergent tempi and modes of evolution. Free-radical signals emerge directly from the biophysics of mosaic respiratory chains encoded by two genomes prone to mismatch, with apoptosis being the default penalty for compromised respiration. Selection for genomic matching is facilitated by two sexes, and optimizes fitness, adaptability and fertility in youth. Mismatches cause infertility, low fitness, hybrid breakdown, and potentially speciation. The dynamics of selection for mitonuclear function optimize fitness over generations, but the same selective processes also operate within generations, driving ageing and age-related diseases. This coherent view of eukaryotic energetics offers striking insights into infertility and age-related diseases.

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Section: But Mitochondria Demand Genomic Matchingmentioning

confidence: 99%

Mitonuclear match: Optimizing fitness and fertility over generations drives ageing within generations

Lane¹

2011

BioEssays

167

168

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“…Second, Potluri et al (2009) found that the phenotypic impact of a mutation in the nDNA-encoded subunit NDUFA1 that causes progressive complex I-specific neurodegenerative disease was modulated by mtDNA genetic backgrounds (Potluri et al 2009). Accordingly, NDUFA1 was found to directly interact with two complex I mtDNA-encoded subunits (Gershoni et al 2010). Third, Rai et al (2007) found that a combination between the A10398G nonsynonymous change in mtDNA-encoded complex I subunit ND3 with nDNA-encoded variants increased susceptibility to developing type 2 diabetes mellitus (T2DM).…”

Section: Introductionmentioning

confidence: 99%

Disrupting Mitochondrial–Nuclear Coevolution Affects OXPHOS Complex I Integrity and Impacts Human Health

Gershoni

Levin

Ovadia

et al. 2014

Genome Biology and Evolution

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The mutation rate of the mitochondrial DNA (mtDNA), which is higher by an order of magnitude as compared with the nuclear genome, enforces tight mitonuclear coevolution to maintain mitochondrial activities. Interruption of such coevolution plays a role in interpopulation hybrid breakdown, speciation events, and disease susceptibility. Previously, we found an elevated amino acid replacement rate and positive selection in the nuclear DNA-encoded oxidative phosphorylation (OXPHOS) complex I subunit NDUFC2, a phenomenon important for the direct interaction of NDUFC2 with the mtDNA-encoded complex I subunit ND4. This finding underlines the importance of mitonuclear coevolution to physical interactions between mtDNA and nuclear DNA-encoded factors. Nevertheless, it remains unclear whether this interaction is important for the stability and activity of complex I. Here, we show that siRNA silencing of NDUFC2 reduced growth of human D-407 retinal pigment epithelial cells, significantly diminished mitochondrial membrane potential, and interfered with complex I integrity. Moreover, site-directed mutagenesis of a positively selected amino acid in NDUFC2 significantly interfered with the interaction of NDUFC2 with its mtDNA-encoded partner ND4. Finally, we show that a genotype combination involving this amino acid (NDUFC2 residue 46) and the mtDNA haplogroup HV likely altered susceptibility to type 2 diabetes mellitus in Ashkenazi Jews. Therefore, mitonuclear coevolution is important for maintaining mitonuclear factor interactions, OXPHOS, and for human health.

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“…Different hypotheses to explain the pattern of sex linkage of N-mt genes in birds and mammals will be resolved as the N-mt genes of more taxa with XY and ZW sex determination are mapped onto chromosomes and especially as the functions of N-mt genes and the extent to which they interact with mt genes are included in analyses (Gershoni et al, 2010). Only a subset of N-mt genes produce products that form complexes with mt genes, and a further subset of such genes engages in key interactions with mt genes.…”

mentioning

confidence: 99%

“…Mitonuclear complexes function not only in the electron transport system but also in the transcription and translation of mitochondrial genes. Genomic conflict can involve any genes that are X-linked, but restrictions on coevolution will apply only to N-mt genes whose products function in mitonuclear complexes and particularly to those N-mt genes that are most closely coordinated with mt genes (Gershoni et al, 2010). A key prediction is that N-mt genes on Z chromosomes in birds should evolve faster and be better coadapted with mt genes than N-mt genes on autosomes.…”

mentioning

confidence: 99%

Sex linkage of nuclear-encoded mitochondrial genes

Hill

2013

Heredity

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Coevolution Predicts Direct Interactions between mtDNA-Encoded and nDNA-Encoded Subunits of Oxidative Phosphorylation Complex I

Cited by 62 publications

References 47 publications

Mitonuclear match: Optimizing fitness and fertility over generations drives ageing within generations

Mitonuclear match: Optimizing fitness and fertility over generations drives ageing within generations

Disrupting Mitochondrial–Nuclear Coevolution Affects OXPHOS Complex I Integrity and Impacts Human Health

Sex linkage of nuclear-encoded mitochondrial genes

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