DNA Content of Individual Mitochondrial Nucleoids Varies Depending on the Culture Conditions of the Yeast Saccharomyces cerevisiae

Miyakawa, Isamu; Miyamoto, Masahide; Kuroiwa, Tsuneyoshi; Sando, Nobundo

doi:10.1508/cytologia.69.101

Cited by 18 publications

(18 citation statements)

References 17 publications

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“…For example, aerobically grown diploid cells of the yeast Saccharomyces cerevisiae contain, on average, 100 molecules of 85-kbp mtDNA. With a distance of 0.34 nm between base pairs in DNA, the total length of mtDNA reaches almost 3 mm per cell, while the diameter of the cell does not exceed 3 to 4 m. Analogously to its nuclear counterpart, mtDNA must be packaged into condensed nucleoprotein structures termed mitochondrial nucleoids (mt-nucleoids) (1)(2)(3)(4)(5)(6). The size of mt-nucleoids in S. cerevisiae ranges from 0.2 to 0.9 m, meaning that mtDNA in yeasts undergoes compaction of roughly 3 orders of magnitude.…”

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The Strictly Aerobic Yeast Yarrowia lipolytica Tolerates Loss of a Mitochondrial DNA-Packaging Protein

et al. 2014

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bMitochondrial DNA (mtDNA) is highly compacted into DNA-protein structures termed mitochondrial nucleoids (mt-nucleoids). The key mt-nucleoid components responsible for mtDNA condensation are HMG box-containing proteins such as mammalian mitochondrial transcription factor A (TFAM) and Abf2p of the yeast Saccharomyces cerevisiae. To gain insight into the function and organization of mt-nucleoids in strictly aerobic organisms, we initiated studies of these DNA-protein structures in Yarrowia lipolytica. We identified a principal component of mt-nucleoids in this yeast and termed it YlMhb1p (Y. lipolytica mitochondrial HMG box-containing protein 1). YlMhb1p contains two putative HMG boxes contributing both to DNA binding and to its ability to compact mtDNA in vitro. Phenotypic analysis of a ⌬mhb1 strain lacking YlMhb1p resulted in three interesting findings. First, although the mutant exhibits clear differences in mt-nucleoids accompanied by a large decrease in the mtDNA copy number and the number of mtDNA-derived transcripts, its respiratory characteristics and growth under most of the conditions tested are indistinguishable from those of the wild-type strain. Second, our results indicate that a potential imbalance between subunits of the respiratory chain encoded separately by nuclear DNA and mtDNA is prevented at a (post)translational level. Third, we found that mtDNA in the ⌬mhb1 strain is more prone to mutations, indicating that mtHMG box-containing proteins protect the mitochondrial genome against mutagenic events. Individual eukaryotic cells contain a population of mitochondrial DNA (mtDNA) molecules, the number of which may reach several thousand copies. For example, aerobically grown diploid cells of the yeast Saccharomyces cerevisiae contain, on average, 100 molecules of 85-kbp mtDNA. With a distance of 0.34 nm between base pairs in DNA, the total length of mtDNA reaches almost 3 mm per cell, while the diameter of the cell does not exceed 3 to 4 m. Analogously to its nuclear counterpart, mtDNA must be packaged into condensed nucleoprotein structures termed mitochondrial nucleoids (mt-nucleoids) (1-6). The size of mt-nucleoids in S. cerevisiae ranges from 0.2 to 0.9 m, meaning that mtDNA in yeasts undergoes compaction of roughly 3 orders of magnitude. Although it is known that the size and shape (oval versus globular) of mt-nucleoids, the number of mt-nucleoids (ranging from 50 to 70) per diploid cell (2), and the number of copies (up to 9) of mtDNA per mt-nucleoid (3) in S. cerevisiae depend on physiological conditions, the molecular mechanisms mediating nucleoid maintenance, dynamics, and roles in mtDNA distribution/segregation during cell division are largely not understood. This is also true for mammalian mt-nucleoids, which, in contrast to their yeast counterparts, contain a relatively small number of mtDNA molecules and are thus more solitary in nature (7,8). Description of these intra-and interspecific differences in the organization of mt-nucleoids would greatly facilitate our understanding of the m...

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The Strictly Aerobic Yeast Yarrowia lipolytica Tolerates Loss of a Mitochondrial DNA-Packaging Protein

et al. 2014

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“…Mitochondrial nucleoids contain more than one equivalent of mtDNA per nucleoid (102,147). MacAlpine et al (90) found that the distribution of mtDNA in the nucleoids was under the control of the general amino acid control circuit.…”

Section: Acetohydroxyacid Reductoisomerase and Mtdnamentioning

confidence: 99%

Moonlighting Proteins in Yeasts

Gancedo

Flores

2008

Microbiol Mol Biol Rev

150

123

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SUMMARY Proteins able to participate in unrelated biological processes have been grouped under the generic name of moonlighting proteins. Work with different yeast species has uncovered a great number of moonlighting proteins and shown their importance for adequate functioning of the yeast cell. Moonlighting activities in yeasts include such diverse functions as control of gene expression, organelle assembly, and modification of the activity of metabolic pathways. In this review, we consider several well-studied moonlighting proteins in different yeast species, paying attention to the experimental approaches used to identify them and the evidence that supports their participation in the unexpected function. Usually, moonlighting activities have been uncovered unexpectedly, and up to now, no satisfactory way to predict moonlighting activities has been found. Among the well-characterized moonlighting proteins in yeasts, enzymes from the glycolytic pathway appear to be prominent. For some cases, it is shown that despite close phylogenetic relationships, moonlighting activities are not necessarily conserved among yeast species. Organisms may utilize moonlighting to add a new layer of regulation to conventional regulatory networks. The existence of this type of proteins in yeasts should be taken into account when designing mutant screens or in attempts to model or modify yeast metabolism.

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“…Subsequently, we isolated mt-nucleoids from the spheroplasts of yeast cells, maintaining their structure in vivo, and showed that specific DNA-binding proteins compactly packaged 3-4 copies of mtDNA into chromatin-like structures (Miyakawa et al 1987(Miyakawa et al , 1995(Miyakawa et al , 2010. In addition, we demonstrated that a single mt-nucleoid in rho + cells, which are grown anaerobically, contains ∼20 copies of mtDNA, but a single mt-nucleoid in cells grown aerobically in the same medium contains only 1-2 copies of mtDNA (Miyakawa et al 2004). These results show that the size and number of mt-nucleoids per cell are not constant but rather dynamically change depending on culture conditions or the stage of life cycle of the yeast cells, as well as the copy number of mtDNA per cell.…”

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confidence: 55%

Morphology of mitochondrial nucleoids in respiratory-deficient yeast cells varies depending on the unit length of the mitochondrial DNA sequence

Okamoto¹,

Inai²,

Miyakawa³

2016

FEMS Yeast Research

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One sentence summary: The authors investigated the mitochondrial nucleoids in Saccharomyces cerevisiae and found that the morphology of mitochondrial nucleoids in rho -cells significantly varies depending on the unit length of their mtDNA.Editor: Monique Bolotin-Fukuhara ABSTRACTWe investigated the morphology of mitochondrial nucleoids (mt-nucleoids) and mitochondria in Saccharomyces cerevisiae rho + and rho − cells with DAPI staining and mitochondria-targeted GFP. Whereas the mt-nucleoids appeared as strings of beads in wild-type rho + cells at log phase, the mt-nucleoids in hypersuppressive rho − cells (HS40 rho − cells) appeared as distinct punctate structures. In order to elucidate whether the punctate mt-nucleoids are common to other rho − cells, we observed the mt-nucleoids in rho − strains that retain different unit lengths of the mitochondrial DNA (mtDNA) sequence.As a result, rho − cells that have long mtDNA sequences, of more than 30 kb, had mt-nucleoids with a strings-of-beads appearance in tubular mitochondria. In contrast, rho − cells that have short mtDNA sequences, of <1 kb, had punctate mt-nucleoids in tubular mitochondria. This indicates that the morphology of mt-nucleoids in rho − cells significantly varies depending on the unit length of their mtDNA sequence. Analyses of mt-nucleoids suggest that the punctate mt-nucleoids in HS40 rho − cells consist of concatemeric mtDNAs and oligomeric circular mtDNAs associated with Abf2p and other nucleoid proteins.

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DNA Content of Individual Mitochondrial Nucleoids Varies Depending on the Culture Conditions of the Yeast Saccharomyces cerevisiae

Cited by 18 publications

References 17 publications

The Strictly Aerobic Yeast Yarrowia lipolytica Tolerates Loss of a Mitochondrial DNA-Packaging Protein

The Strictly Aerobic Yeast Yarrowia lipolytica Tolerates Loss of a Mitochondrial DNA-Packaging Protein

Moonlighting Proteins in Yeasts

Morphology of mitochondrial nucleoids in respiratory-deficient yeast cells varies depending on the unit length of the mitochondrial DNA sequence

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