Novel class of nuclear genes involved in both mRNA splicing and protein synthesis in Saccharomyces cerevisiae mitochondria

Asher, Edna Ben; Groudinsky, Olga; Dujardin, Geneviève; Altamura, Nicola; Kermorgant, Michèle; Słonimski, Piotr P.

doi:10.1007/bf00427051

Cited by 60 publications

(42 citation statements)

References 63 publications

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“…The NAM9 action spectrum differed markedly from the spectrum of the NAM] suppressor, which is the only previously isolated genenonspecific, allele-specific nuclear dominant suppressor of mit mutations. NAM] acts exclusively on mutations localized in mitochondrial introns, which suggested direct involvement in splicing (2,24). The NAM9 action spectrum refuted the direct involvement in splicing of NAM9 suppressor and suggested its purely informational, probably ribosomal, character.…”

Section: Resultsmentioning

confidence: 99%

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NAM9 nuclear suppressor of mitochondrial ochre mutations in Saccharomyces cerevisiae codes for a protein homologous to S4 ribosomal proteins from chloroplasts, bacteria, and eucaryotes.

Boguta¹,

Dmochowska²,

Borsuk³

et al. 1992

Mol. Cell. Biol.

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We report the genetic characterization, molecular cloning, and sequencing of a novel nuclear suppressor, the NAM9 gene from Saccharomyces cerevisiae, which acts on mutations of mitochondrial DNA. The strain NAM9-1 was isolated as a respiration-competent revertant of a mitochondrial mit mutant which carries the V25 ochre mutation in the oxil gene. Genetic characterization of the NAM9-1 mutation has shown that it is a nuclear dominant omnipotent suppressor alleviating several mutations in all four mitochondrial genes tested and has suggested its informational, and probably ribosomal, character. The NAM9 gene was cloned by transformation of the recipient oxil-V25 mutant to respiration competence by using a gene bank from the NAM9-1 rhoo strain.Orthogonal-field alternation gel electrophoresis analysis and genetic mapping localized the NAM9 gene on the right arm of chromosome XIV. Sequence analysis of the NAM9 gene showed that it encodes a basic protein of 485 amino acids with a presequence that could target the protein to the mitochondrial matrix. The N-terminal sequence of 200 amino acids of the deduced NAM9 product strongly resembles the S4 ribosomal proteins from chloroplasts and bacteria. Significant although less extensive similarity was found with ribosomal cytoplasmic proteins from lower eucaryotes, including S. cerevisiae. Chromosomal inactivation of the NAM9+ gene is not lethal to the cell but leads to respiration deficiency and loss of mitochondrial DNA integrity. We conclude that the NAM9 gene product is a mitochondrial ribosomal counterpart of S4 ribosomal proteins found in other systems and that the suppressor acts through decreasing the fidelity of translation.Mitochondria possess their own translation apparatus responsible for the synthesis of only a handful of the hundreds of mitochondrial proteins (for a review, see reference 59a). The biogenesis of this apparatus depends on the coordinate expression of both mitochondrial and nuclear genes (9). Although the whole set of tRNAs required for mitochondrial translation and the rRNAs of mitochondrial ribosomes are encoded by the mitochondrial genes, the mitochondrial ribosomal proteins, as well as other elements of the mitochondrial translation system, are encoded by nuclear genes and transported to mitochondria. The proteins of mitochondrial ribosomes differ from those of cytoplasmic ribosomes. Thus, two different sets of nuclear genes code for mitochondrial and cytoplasmic ribosomal proteins (r-proteins). During the last few years, genes for approximately half of the 70 to 80 yeast cytoplasmic r-proteins have been isolated and characterized (for a review, see reference 52). At present, however, very little is known about the structure and organization of genes for the mitochondrial r-proteins (MRP genes). So far, sequences for only 10 of 60 to 70 genes for mitochondrial r-proteins have been published (10, 10a, 14, 23, 33, 45-46, 51, 59). Thus, to gain more insight into the structure, chromosomal organization, and evolution of MRP genes, a more comprehe...

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Section: Resultsmentioning

confidence: 99%

“…NAM], NAM2, NAM7, and NAM8 suppressors are involved in both translation and splicing (2,13,26,40). The recessive suppressor mutations nam3 and ribosome series suppressors (5,36,37,68) seem to be analogous to Escherichia coli ribosomal ram suppressors in the sense of their allelespecific, gene-nonspecific mode of action (18).…”

mentioning

confidence: 99%

NAM9 nuclear suppressor of mitochondrial ochre mutations in Saccharomyces cerevisiae codes for a protein homologous to S4 ribosomal proteins from chloroplasts, bacteria, and eucaryotes.

Boguta¹,

Dmochowska²,

Borsuk³

et al. 1992

Mol. Cell. Biol.

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“…In other strain backgrounds, ATP8/6 mRNAs are at even lower levels and respiratory growth is more severely restricted (8). Nam1p has been suggested to have a role in mitochondrial translation (45) and has recently been shown to associate with the mitochondrial RNA polymerase. A model has been presented suggesting that transcription and translation of mitochondrial RNAs are coupled at the inner membrane (22).…”

Section: Fig 5 Solubility Properties Of Aep3pmentioning

confidence: 99%

Aep3p Stabilizes the Mitochondrial Bicistronic mRNA Encoding Subunits 6 and 8 of the H+-translocating ATP Synthase of Saccharomyces cerevisiae

Ellis

Helfenbein

Tzagoloff

et al. 2004

Journal of Biological Chemistry

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Subunits 6 and 8 of the mitochondrial ATPase in Saccharomyces cerevisiae are encoded by the mitochondrial genome and translated from bicistronic mRNAs containing both reading frames. The stability of the two major species of ATP8/6 mRNA, which differ in the length of the 5 -untranslated region, depends on the expression of several nuclear-encoded factors. In the present study, the product of the gene designated AEP3 (open reading frame YPL005W) is shown to be required for stabilization and/or processing of both ATP8/6 mRNA species. In an aep3-disruptant strain, the shorter ATP8/6 mRNA was undetectable, and the level of the longer mRNA was reduced to ϳ35% that of wild type. Localization of a hemagglutinin-tagged version of Aep3p showed that the protein is an extrinsic constituent of the mitochondrial inner membrane facing the matrix.

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“…The data led to the conclusion that Nam1p was required for the processing and/or stability of cytb and cox1 intron-containing pre-mRNAs and of the atp6 transcript (which does not contain introns) (116). Interestingly, NAM1 inactivation leads to 20 to 50% petite production in a strain with an intron-containing mitochondrial genome (16) while there is no increase in petite production (with respect to wild type) when the mitochondrial genome does not contain introns (116). According to the authors, the high level of petites observed in the first context may be explained by a defect in mitochondrial translation due to a starvation for tRNA Glu , which is cotranscribed with the cytb gene, the intron-containing cytb transcript being unstable in the absence of Nam1p.…”

Section: The Translation-atp Synthase Connection Backgroundmentioning

confidence: 99%

Maintenance and Integrity of the Mitochondrial Genome: a Plethora of Nuclear Genes in the Budding Yeast

Contamine

Picard

2000

Microbiol Mol Biol Rev

262

209

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SUMMARY Instability of the mitochondrial genome (mtDNA) is a general problem from yeasts to humans. However, its genetic control is not well documented except in the yeast Saccharomyces cerevisiae. From the discovery, 50 years ago, of the petite mutants by Ephrussi and his coworkers, it has been shown that more than 100 nuclear genes directly or indirectly influence the fate of the rho+ mtDNA. It is not surprising that mutations in genes involved in mtDNA metabolism (replication, repair, and recombination) can cause a complete loss of mtDNA (rho0 petites) and/or lead to truncated forms (rho−) of this genome. However, most loss-of-function mutations which increase yeast mtDNA instability act indirectly: they lie in genes controlling functions as diverse as mitochondrial translation, ATP synthase, iron homeostasis, fatty acid metabolism, mitochondrial morphology, and so on. In a few cases it has been shown that gene overexpression increases the levels of petite mutants. Mutations in other genes are lethal in the absence of a functional mtDNA and thus convert this petite-positive yeast into a petite-negative form: petite cells cannot be recovered in these genetic contexts. Most of the data are explained if one assumes that the maintenance of the rho+ genome depends on a centromere-like structure dispensable for the maintenance of rho− mtDNA and/or the function of mitochondrially encoded ATP synthase subunits, especially ATP6. In fact, the real challenge for the next 50 years will be to assemble the pieces of this puzzle by using yeast and to use complementary models, especially in strict aerobes.

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Novel class of nuclear genes involved in both mRNA splicing and protein synthesis in Saccharomyces cerevisiae mitochondria

Cited by 60 publications

References 63 publications

NAM9 nuclear suppressor of mitochondrial ochre mutations in Saccharomyces cerevisiae codes for a protein homologous to S4 ribosomal proteins from chloroplasts, bacteria, and eucaryotes.

NAM9 nuclear suppressor of mitochondrial ochre mutations in Saccharomyces cerevisiae codes for a protein homologous to S4 ribosomal proteins from chloroplasts, bacteria, and eucaryotes.

Aep3p Stabilizes the Mitochondrial Bicistronic mRNA Encoding Subunits 6 and 8 of the H+-translocating ATP Synthase of Saccharomyces cerevisiae

Maintenance and Integrity of the Mitochondrial Genome: a Plethora of Nuclear Genes in the Budding Yeast

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