Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA

Jodi Nunnari, Wallace F. Marshall, Aaron Straight, Andrew Murray, John W. Sedat, Peter Walter

Research output: Contribution to journalArticle

352 Citations (Scopus)

Abstract

To gain insight into the process of mitochondrial transmission in yeast, we directly labeled mitochondrial proteins and mitochondrial DNA (mtDNA) and observed their fate after the fusion of two cells. To this end, mitochondrial proteins in haploid cells of opposite mating type were labeled with different fluorescent dyes and observed by fluorescence microscopy after mating of the cells. Parental mitochondrial protein markers rapidly redistributed and colocalized throughout zygotes, indicating that during mating, parental mitochondria fuse and their protein contents intermix, consistent with results previously obtained with a single parentally derived protein marker. Analysis of the three-dimensional structure and dynamics of mitochondria in living cells with wide-field fluorescence microscopy indicated that mitochondria form a single dynamic network, whose continuity is maintained by a balanced frequency of fission and fusion events. Thus, the complete mixing of mitochondrial proteins can be explained by the formation of one continuous mitochondrial compartment after mating. In marked contrast to the mixing of parental mitochondrial proteins after fusion, mtDNA (labeled with the thymidine analogue 5-bromodeoxyuridine) remained distinctly localized to one half of the zygotic cell. This observation provides a direct explanation for the genetically observed nonrandom patterns of mtDNA transmission. We propose that anchoring of mtDNA within the organelle is linked to an active segregation mechanism that ensures accurate inheritance of mtDNA along with the organelle.

Original languageEnglish (US)
Pages (from-to)1233-1242
Number of pages10
JournalMolecular Biology of the Cell
Volume8
Issue number7
StatePublished - 1997

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Mitochondrial Dynamics
Mitochondrial Proteins
Mitochondrial DNA
Saccharomyces cerevisiae
Mitochondria
Fluorescence Microscopy
Organelles
Cell Fusion
Zygote
Haploidy
Bromodeoxyuridine
Fluorescent Dyes
Thymidine
Proteins
Yeasts

ASJC Scopus subject areas

  • Molecular Biology
  • Genetics
  • Cell Biology

Cite this

Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. / Nunnari, Jodi; Marshall, Wallace F.; Straight, Aaron; Murray, Andrew; Sedat, John W.; Walter, Peter.

In: Molecular Biology of the Cell, Vol. 8, No. 7, 1997, p. 1233-1242.

Research output: Contribution to journalArticle

Nunnari, Jodi ; Marshall, Wallace F. ; Straight, Aaron ; Murray, Andrew ; Sedat, John W. ; Walter, Peter. / Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. In: Molecular Biology of the Cell. 1997 ; Vol. 8, No. 7. pp. 1233-1242.
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