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Nucleic Acids Research Advance Access published online on December 11, 2008
Nucleic Acids Research, doi:10.1093/nar/gkn993
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© 2008 The Author(s)
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Genome integrity, repair and replication

Reactive oxygen species regulate DNA copy number in isolated yeast mitochondria by triggering recombination-mediated replication

Akiko Hori1,2, Minoru Yoshida1,2, Takehiko Shibata3 and Feng Ling1,*

1Chemical Genetics Laboratory, RIKEN Advanced Science Institute, Hirosawa 2-1, Wako-shi, Saitama 351-0198, 2Graduate School of Science and Engineering, Saitama University, Saitama 338-8570 and 3Cellular & Molecular Biology Laboratory, RIKEN Advanced Science Institute, Hirosawa 2-1, Wako-shi, Saitama 351-0198, Japan

*To whom correspondence should be addressed. Tel: +81 48 467 9518; Fax: +81 48 462 4676; Email: ling{at}postman.riken.go.jp

Received July 13, 2008. Revised November 13, 2008. Accepted November 25, 2008.

Mitochondrial DNA (mtDNA) encodes proteins that are essential for cellular ATP production. Reactive oxygen species (ROS) are respiratory byproducts that damage mtDNA and other cellular components. In Saccharomyces cerevisiae, the oxidized base excision-repair enzyme Ntg1 introduces a double-stranded break (DSB) at the mtDNA replication origin ori5; this DSB initiates the rolling-circle mtDNA replication mediated by the homologous DNA pairing protein Mhr1. Thus, ROS may play a role in the regulation of mtDNA copy number. Here, we show that the treatment of isolated mitochondria with low concentrations of hydrogen peroxide increased mtDNA copy number in an Ntg1- and Mhr1-dependent manner. This treatment elevated the DSB levels at ori5 of hypersuppressive [rho–] mtDNA only if Ntg1 was active. In vitro Ntg1-treatment of hypersuppressive [rho–] mtDNA extracted from hydrogen peroxide-treated mitochondria revealed increased oxidative modifications at ori5 loci. We also observed that purified Ntg1 created breaks in single-stranded DNA harboring oxidized bases, and that ori5 loci have single-stranded character. Furthermore, chronic low levels of hydrogen peroxide increased in vivo mtDNA copy number. We therefore propose that ROS act as a regulator of mtDNA copy number, acting through the Mhr1-dependent initiation of rolling-circle replication promoted by Ntg1-induced DSB in the single-stranded regions at ori5.


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