Experimental Relocation of the Mitochondrial ATP9 Gene to the Nucleus Reveals Forces Underlying Mitochondrial Genome Evolution

Bietenhader, Maïlis; Martos, Alexandre A. R.; Tétaud, Emmanuel; Aiyar, Raeka S.; Sellem, Carole H.; Kucharczyk, Róża; Clauder‐Münster, Sandra; Giraud, Marie‐France; Godard, François; Salin, Bénédicte; Sagot, Isabelle; Gagneur, Julien; Dequard-Chablat, Michelle; Contamine, Véronique; Denmat, Sylvie Hermann‐Le; Sainsard-Chanet, Annie; Steinmetz, Lars M.; Rago, Jean‐Paul di

doi:10.1371/journal.pgen.1002876

Cited by 53 publications

(47 citation statements)

References 54 publications

(71 reference statements)

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“…As predicted by our hypothesis, the mitochondrial proteins show a reduced hydrophobicity of the first TMDs in the few species in which these genes have been successfully transferred in nature (45)(46)(47). For example, the first TMD of the nu-encoded Cox2 protein in legumes is less hydrophobic than the first TMD of the mt-encoded homolog (48).…”

Section: Discussionsupporting

confidence: 55%

Mitochondrial genomes are retained by selective constraints on protein targeting

Björkholm

Harish

Hagström

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Mitochondria are energy-producing organelles in eukaryotic cells considered to be of bacterial origin. The mitochondrial genome has evolved under selection for minimization of gene content, yet it is not known why not all mitochondrial genes have been transferred to the nuclear genome. Here, we predict that hydrophobic membrane proteins encoded by the mitochondrial genomes would be recognized by the signal recognition particle and targeted to the endoplasmic reticulum if they were nuclear-encoded and translated in the cytoplasm. Expression of the mitochondrially encoded proteins Cytochrome oxidase subunit 1, Apocytochrome b, and ATP synthase subunit 6 in the cytoplasm of HeLa cells confirms export to the endoplasmic reticulum. To examine the extent to which the mitochondrial proteome is driven by selective constraints within the eukaryotic cell, we investigated the occurrence of mitochondrial protein domains in bacteria and eukaryotes. The accessory protein domains of the oxidative phosphorylation system are unique to mitochondria, indicating the evolution of new protein folds. Most of the identified domains in the accessory proteins of the ribosome are also found in eukaryotic proteins of other functions and locations. Overall, one-third of the protein domains identified in mitochondrial proteins are only rarely found in bacteria. We conclude that the mitochondrial genome has been maintained to ensure the correct localization of highly hydrophobic membrane proteins. Taken together, the results suggest that selective constraints on the eukaryotic cell have played a major role in modulating the evolution of the mitochondrial genome and proteome. mitochondria | protein domain | evolution | endoplasmatic reticulum | signal recognition particle

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Section: Discussionsupporting

confidence: 55%

Mitochondrial genomes are retained by selective constraints on protein targeting

Björkholm

Harish

Hagström

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Relocation of organellar genes to the nucleus has been achieved experimentally (66,70). An accompanying gain of fitness would indicate selective value to relocation and would falsify CoRR.…”

Section: Primary Electron Transport Components Imported Into Organellmentioning

confidence: 99%

Why chloroplasts and mitochondria retain their own genomes and genetic systems: Colocation for redox regulation of gene expression

Allen

2015

Proc. Natl. Acad. Sci. U.S.A.

249

194

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Chloroplasts and mitochondria are subcellular bioenergetic organelles with their own genomes and genetic systems. DNA replication and transmission to daughter organelles produces cytoplasmic inheritance of characters associated with primary events in photosynthesis and respiration. The prokaryotic ancestors of chloroplasts and mitochondria were endosymbionts whose genes became copied to the genomes of their cellular hosts. These copies gave rise to nuclear chromosomal genes that encode cytosolic proteins and precursor proteins that are synthesized in the cytosol for import into the organelle into which the endosymbiont evolved. What accounts for the retention of genes for the complete synthesis within chloroplasts and mitochondria of a tiny minority of their protein subunits? One hypothesis is that expression of genes for protein subunits of energy-transducing enzymes must respond to physical environmental change by means of a direct and unconditional regulatory control—control exerted by change in the redox state of the corresponding gene product. This hypothesis proposes that, to preserve function, an entire redox regulatory system has to be retained within its original membrane-bound compartment. Colocation of gene and gene product for redox regulation of gene expression (CoRR) is a hypothesis in agreement with the results of a variety of experiments designed to test it and which seem to have no other satisfactory explanation. Here, I review evidence relating to CoRR and discuss its development, conclusions, and implications. This overview also identifies predictions concerning the results of experiments that may yet prove the hypothesis to be incorrect.

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“…this strain. For these experiments, we used an ATP1 gene under the dependence of the PGK promoter and a nuclear version of the mitochondrial ATP9 that can complement a strain lacking this gene (Bietenhader et al, 2012). Ectopic expression of Atp1p restored the ability of strain nM to grow on respiratory substrates ( Figure 6A), whereas the nuclear ATP9 gene was unable to do so ( Figures 6A and S6A).…”

Section: Ectopic Expression Of Atp1 Alleviates the Respiratory Phenotmentioning

confidence: 99%

Expression of Nuclear and Mitochondrial Genes Encoding ATP Synthase Is Synchronized by Disassembly of a Multisynthetase Complex

et al. 2014

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In eukaryotic cells, oxidative phosphorylation involves multisubunit complexes of mixed genetic origin. Assembling these complexes requires an organelle-independent synchronizing system for the proper expression of nuclear and mitochondrial genes. Here we show that proper expression of the F1FO ATP synthase (complex V) depends on a cytosolic complex (AME) made of two aminoacyl-tRNA synthetases (cERS and cMRS) attached to an anchor protein, Arc1p. When yeast cells adapt to respiration the Snf1/4 glucose-sensing pathway inhibits ARC1 expression triggering simultaneous release of cERS and cMRS. Free cMRS and cERS relocate to the nucleus and mitochondria, respectively, to synchronize nuclear transcription and mitochondrial translation of ATP synthase genes. Strains releasing asynchronously the two aminoacyl-tRNA synthetases display aberrant expression of nuclear and mitochondrial genes encoding subunits of complex V resulting in severe defects of the oxidative phosphorylation mechanism. This work shows that the AME complex coordinates expression of enzymes that require intergenomic control.

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Experimental Relocation of the Mitochondrial ATP9 Gene to the Nucleus Reveals Forces Underlying Mitochondrial Genome Evolution

Cited by 53 publications

References 54 publications

Mitochondrial genomes are retained by selective constraints on protein targeting

Mitochondrial genomes are retained by selective constraints on protein targeting

Why chloroplasts and mitochondria retain their own genomes and genetic systems: Colocation for redox regulation of gene expression

Expression of Nuclear and Mitochondrial Genes Encoding ATP Synthase Is Synchronized by Disassembly of a Multisynthetase Complex

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