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Mitochondrial DNA repairs double-strand breaks in yeast chromosomes

Abstract

The endosymbiotic theory for the origin of eukaryotic cells1 proposes that genetic information can be transferred from mitochondria to the nucleus of a cell, and genes that are probably of mitochondrial origin have been found in nuclear chromosomes2. Occasionally, short or rearranged sequences homologous to mitochondrial DNA are seen in the chromosomes of different organisms including yeast, plants and humans3. Here we report a mechanism by which fragments of mitochondrial DNA, in single or tandem array, are transferred to yeast chromosomes under natural conditions during the repair of double-strand breaks in haploid mitotic cells. These repair insertions originate from non-contiguous regions of the mitochondrial genome. Our analysis of the Saccharomyces cerevisiae mitochondrial genome4 indicates that the yeast nuclear genome does indeed contain several short sequences of mitochondrial origin which are similar in size and composition to those that repair double-strand breaks. These sequences are located predominantly in non-coding regions of the chromosomes, frequently in the vicinity of retrotransposon long terminal repeats, and appear as recent integration events. Thus, colonization of the yeast genome by mitochondrial DNA is an ongoing process.

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Figure 1: Flow-diagram of the experimental design.
Figure 2: Sequencing of repaired double-strand breaks.
Figure 3: Description of mitochondrial DNA found in the nucleus.

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Acknowledgements

We thank F. Foury for having provided the entire mitochondrial sequence of S. cerevisiae, D. Alexandraki for the yeast strain Δykl222c , A. Harrington for purified mitochondrial DNA, A. Thierry for the Δ yme1 strategy, F. Tekaia and A. Perrin for bioinformatics, M. Buckingham and T. Pugsley for comments on the manuscript and Henri Buc in whose laboratory some of these experiments were performed. This work was supported by a grant from the European Commission (EUROFAN). B.D. is a member of Institut Universitaire de France.

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Correspondence to Miria Ricchetti.

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Ricchetti, M., Fairhead, C. & Dujon, B. Mitochondrial DNA repairs double-strand breaks in yeast chromosomes. Nature 402, 96–100 (1999). https://doi.org/10.1038/47076

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