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Molecular and Cellular Biology, February 2007, p. 1133-1145, Vol. 27, No. 3
0270-7306/07/$08.00+0     doi:10.1128/MCB.00770-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

DNA Recombination-Initiation Plays a Role in the Extremely Biased Inheritance of Yeast [rho–] Mitochondrial DNA That Contains the Replication Origin ori5{triangledown} ,{dagger}

Feng Ling,1 Akiko Hori,1,2 and Takehiko Shibata1*

RIKEN Discovery Research Institute, Hirosawa 2-1, Wako-shi, Saitama 351-0198, Japan,1 Graduate School of Science and Engineering, Saitama University, 255 Shimo-ohkubo, Sakura-ku, Saitama 338-8570, Japan2

Received 2 May 2006/ Returned for modification 5 July 2006/ Accepted 6 November 2006

Hypersuppressiveness, as observed in Saccharomyces cerevisiae, is an extremely biased inheritance of a small mitochondrial DNA (mtDNA) fragment that contains a replication origin (HS [rho–] mtDNA). Our previous studies showed that concatemers (linear head-to-tail multimers) are obligatory intermediates for mtDNA partitioning and are primarily formed by rolling-circle replication mediated by Mhr1, a protein required for homologous mtDNA recombination. In this study, we found that Mhr1 is required for the hypersuppressiveness of HS [ori5] [rho–] mtDNA harboring ori5, one of the replication origins of normal ([rho+]) mtDNA. In addition, we detected an Ntg1-stimulated double-strand break at the ori5 locus. Purified Ntg1, a base excision repair enzyme, introduced a double-stranded break by itself into HS [ori5] [rho–] mtDNA at ori5 isolated from yeast cells. Both hypersuppressiveness and concatemer formation of HS [ori5] [rho–] mtDNA are simultaneously suppressed by the ntg1 null mutation. These results support a model in which, like homologous recombination, rolling-circle HS [ori5] [rho–] mtDNA replication is initiated by double-stranded breakage in ori5, followed by Mhr1-mediated homologous pairing of the processed nascent DNA ends with circular mtDNA. The hypersuppressiveness of HS [ori5] [rho–] mtDNA depends on a replication advantage furnished by the higher density of ori5 sequences and on a segregation advantage furnished by the higher genome copy number on transmitted concatemers.

* Corresponding author. Mailing address: RIKEN Discovery Research Institute, Hirosawa 2-1, Wako-shi, Saitama 351-0198, Japan. Phone: 81-48-467-9528. Fax: 81-48-462-1227. E-mail: tshibata{at}postman.riken.go.jp.

{triangledown} Published ahead of print on 20 November 2006.

{dagger} Supplemental material for this article may be found at http://mcb.asm.org/.

Molecular and Cellular Biology, February 2007, p. 1133-1145, Vol. 27, No. 3
0270-7306/07/$08.00+0     doi:10.1128/MCB.00770-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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