A genome-wide map of mitochondrial DNA recombination in yeast

Genetics

Volumn 198, Issue 2, 2014, Pages 755-771

  Fritsch, Emilie S ^a   Chabbert, Christophe D ^a   Klaus, Bernd ^a   Steinmetz, Lars M ^a,b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CROSSOVER JUNCTION ENDODEOXYRIBONUCLEASE; DNA FRAGMENT; FUNGAL DNA; MITOCHONDRIAL DNA; RIBOSOME RNA; SINGLE STRANDED DNA; SPACER DNA; TRANSFER RNA;

ARTICLE; DIPLOIDY; DNA RECOMBINATION; DNA TEMPLATE; FUNGAL GENE; FUNGAL GENETICS; FUNGAL GENOME; FUNGAL STRAIN; GENE CLUSTER; GENE DELETION; GENE DISRUPTION; GENE LOCATION; GENE MAPPING; GENE SEQUENCE; GENETIC MARKER; GENOTYPE; HIGH THROUGHPUT SEQUENCING; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; MEIOTIC RECOMBINATION; MITOCHONDRIAL GENE; MITOCHONDRIAL GENOME; MITOCHONDRION; NONHUMAN; REGULATORY MECHANISM; REPORTER GENE; SACCHAROMYCES CEREVISIAE; CHROMOSOME MAP; DNA SEQUENCE; GENETIC RECOMBINATION; GENETICS; MUTATION RATE;

CHROMOSOME MAPPING; DNA, MITOCHONDRIAL; GENOME, FUNGAL; MUTATION RATE; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS, DNA;

EID: 84908037385     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.166637     Document Type: Article

References (84)

1. Arrieta-Montiel, M. P., V. Shedge, J. Davila, A. C. Christensen, and S. A. Mackenzie, 2009 Diversity of the Arabidopsis mitochondrial genome occurs via nuclear-controlled recombination activity. Genetics 183: 1261–1268.
2. Baudat, F., and A. Nicolas, 1997 Clustering of meiotic doublestrand breaks on yeast chromosome III. Proc. Natl. Acad. Sci. USA 94: 5213–5218.
3. Benjamini, Y., and Y. Hochberg, 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57(1): 289–300.
4. Bianchi, N.O., M. S. Bianchi, and S. M. Richard, 2001 Mitochondrial genome instability in human cancers. Mutat. Res. 488: 9–23.
5. Brewer, L. R., R. Friddle, A. Noy, E. Baldwin, S. S. Martin et al., 2003 Packaging of single DNA molecules by the yeast mitochondrial protein Abf2p. Biophys. J. 85: 2519–2524.
6. Brick, K., F. Smagulova, P. Khil, R. D. Camerini-Otero, and G. V. Petukhova, 2012 Genetic recombination is directed away from functional genomic elements in mice. Nature 485: 642–645.
7. Buhler, C., R. Shroff, and M. Lichten, 2009 Genome-wide mapping of meiotic DNA double-strand breaks in Saccharomyces cerevisiae. Methods Mol. Biol. 557: 143–164.
8. Chen, X. J., and R. A. Butow, 2005 The organization and inheritance of the mitochondrial genome. Nat. Rev. Genet. 6: 815–825.
9. Clark-Walker, G. D., 1991 Contrasting mutation rates in mitochondrial and nuclear genes of yeasts vs. mammals. Curr. Genet. 20: 195–198.
10. D’aurelio, M., 2004 Heterologous mitochondrial DNA recombination in human cells. Hum. Mol. Genet. 13: 3171–3179.
11. Davila, J. I., M. P. Arrieta-Montiel, Y. Wamboldt, J. Cao, J. Hagmann et al., 2011 Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. BMC Biol. 9: 64.
12. Defontaine, A., F. M. Lecocq, and J. N. Hallet, 1991 A rapid miniprep method for the preparation of yeast mitochondrial DNA. Nucleic Acids Res. 19: 185.
13. de Zamaroczy, M., and G. Bernardi, 1986 The GC clusters of the mitochondrial genome of yeast and their evolutionary origin. Gene 41: 1–22.
14. Dieckmann, C. L., and B. Gandy, 1987 Preferential recombination between GC clusters in yeast mitochondrial DNA. EMBO J. 6: 4197–4203.
15. Dimitrov L., R. Brem, L. Kruglyak, and D. Gottschling, 2009 Polymorphisms in multiple genes contribute to the spontaneous mitochondrial genome instability of Saccharomyces cerevisiae S288C strains. Genetics 183: 365–383.
16. Doudican, N. A., B. Song, G. S. Shadel, and P. W. Doetsch, 2005 Oxidative DNA damage causes mitochondrial genomic instability in Saccharomyces cerevisiae. Mol. Cell. Biol. 25: 5196–5204.
17. Dujon, B., P. P. Slonimski, and L. Weill, 1974 Mitochondrial genetics IX: a model for recombination and segregation of mitochondrial genomes in Saccharomyces cerevisiae. Genetics 78: 415.
18. Eyre-Walker, A., and P. Awadalla, 2001 Does human mtDNA recombine? J. Mol. Evol. 53: 430–435.
19. Ezekiel, U. R., and H. P. Zassenhaus, 1993 Localization of a cruciform cutting endonuclease to yeast mitochondria. Mol. Gen. Genet. 240: 414–418.
20. Fikus, M.U., P. A. Mieczkowski, P. Koprowski, J. Rytka, E. Sledziewska- Gójska et al., 2000 The product of the DNA damage-inducible gene of Saccharomyces cerevisiae, DIN7, specifically functions in mitochondria. Genetics 154: 73–81.
21. Fourie, G., N. A. van der Merwe, B. D. Wingfield, M. Bogale, B. Tudzynski et al., 2013 Evidence for inter-specific recombination among the mitochondrial genomes of Fusarium species in the Gibberella fujikuroi complex. BMC Genomics 14: 605.
22. Foury, F., T. Roganti, N. Lecrenier, and B. Purnelle, 1998 The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae. FEBS Lett. 440: 325–331.
23. Fukui, H., and C. T. Moraes, 2009 Mechanisms of formation and accumulation of mitochondrial DNA deletions in aging neurons. Hum. Mol. Genet. 18: 1028–1036.
24. Galtier, N., 2011 The intriguing evolutionary dynamics of plant mitochondrial DNA. BMC Biol. 9: 61.
25. Gerton, J. L., J. DeRisi, R. Shroff, M. Lichten, P. O. Brown et al., 2000 Inaugural article: global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 97: 11383–11390.
26. Gibb, S., and K. Strimmer, 2012 MALDIquant: a versatile R package for the analysis of mass spectrometry data. Bioinformatics 28: 2270–2271.
27. Gietz, R. D., and R. H. Schiestl, 2007a Frozen competent yeast cells that can be transformed with high efficiency using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2: 1–4.
28. Gietz, R. D., and R. H. Schiestl, 2007b High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2: 31–34.
29. Goffeau, A., B. G. Barrell, H. Bussey, R. W. Davis, B. Dujon et al., 1996 Life with 6000 genes. Science 274: 546, 563–567.
30. Gray, M. W., 2012 Mitochondrial evolution. Cold Spring Harb. Perspect. Biol. 4: a011403.
31. Gray, M. W., G. Burger, and B. F. Lang, 1999 Mitochondrial evolution. Science 283: 1476–1481.
32. Grün, B., I. Kosmidis, and A. Zeileis, 2011 Extended beta regression in R: shaken, stirred, mixed, and partitioned. J. Stat. Softw. 48: 1–25.
33. Hori, A., M. Yoshida, T. Shibata, and F. Ling, 2009 Reactive oxygen species regulate DNA copy number in isolated yeast mitochondria by triggering recombination-mediated replication. Nucleic Acids Res. 37: 749–761.
34. Jacquier, A., and B. Dujon, 1985 An intron-encoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene. Cell 41: 383–394.
35. Jung, P. P., J. Schacherer, J.-L. Souciet, S. Potier, P. Wincker et al., 2009 The complete mitochondrial genome of the yeast Pichia sorbitophila. FEMS Yeast Res. 9: 903–910.
36. Jung, P. P., A. Friedrich, C. Reisser, J. Hou, and J. Schacherer, 2012 Mitochondrial genome evolution in a single protoploid yeast species. G3 2: 1103–1111.
37. Kalifa, L., D. F. Quintana, L. K. Schiraldi, N. Phadnis, G. L. Coles et al., 2012 Mitochondrial genome maintenance: roles for nuclear nonhomologous end joining proteins in Saccharomyces cerevisiae. Genetics 190: 951–964.
38. Kleff, S., B. Kemper, and R. Sternglanz, 1992 Identification and characterization of yeast mutants and the gene for a cruciform cutting endonuclease. EMBO J. 11: 699–704.
39. Kong, A., G. Thorleifsson, D. F. Gudbjartsson, G. Masson, A. Sigurdsson et al., 2010 Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467: 1099–1103.
40. Kraytsberg, Y., M. Schwartz, T. A. Brown, K. Ebralidse, W. S. Kunz et al., 2004 Recombination of human mitochondrial DNA. Science 304: 981.
41. Kucej, M., B. Kucejova, R. Subramanian, X. J. Chen, and R. A. Butow, 2008 Mitochondrial nucleoids undergo remodeling in response to metabolic cues. J. Cell Sci. 121: 1861–1868.
42. Ladoukakis, E. D., and E. Zouros, 2001 Direct evidence for homologous recombination in mussel (Mytilus galloprovincialis) mitochondrial DNA. Mol. Biol. Evol. 18: 1168–1175.
43. Lakshmipathy, U., and C. Campbell, 1999 The human DNA ligase III gene encodes nuclear and mitochondrial proteins. Mol. Cell. Biol. 19: 3869–3876.
44. Lee, H.-C., P.-H. Yin, J.-C. Lin, C.-C. Wu, C.-Y. Chen et al., 2006 Mitochondrial genome instability and mtDNA depletion in human cancers. Ann. N. Y. Acad. Sci. 1042: 109–122.
45. Lee, H.-Y., J.-Y. Chou, L. Cheong, N.-H. Chang, S.-Y. Yang et al., 2008 Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135: 1065–1073.
46. Ling, F., and T. Shibata, 2002 Recombination-dependent mtDNA partitioning: in vivo role of Mhr1p to promote pairing of homologous DNA. EMBO J. 21: 4730–4740.
47. Ling, F., F. Makishima, N. Morishima, and T. Shibata, 1995 A nuclear mutation defective in mitochondrial recombination in yeast. EMBO J. 14: 4090–4101.
48. Ling, F., H. Morioka, E. Ohtsuka, and T. Shibata, 2000 A role for MHR1, a gene required for mitochondrial genetic recombination, in the repair of damage spontaneously introduced in yeast mtDNA. Nucleic Acids Res. 28: 4956–4963.
49. Ling, F., A. Hori, and T. Shibata, 2007 DNA recombination-initiation plays a role in the extremely biased inheritance of yeast [rho-] mitochondrial DNA that contains the replication origin ori5. Mol. Cell. Biol. 27: 1133–1145.
50. Ling, F., T. Mikawa, and T. Shibata, 2011 Enlightenment of yeast mitochondrial homoplasmy: diversified roles of gene conversion. Genes 2: 169–190.
51. Ling, F., A. Hori, A. Yoshitani, R. Niu, M. Yoshida et al., 2013 Din7 and Mhr1 expression levels regulate double-strand-breakinduced replication and recombination of mtDNA at ori5 in yeast. Nucleic Acids Res. 41: 5799–5816.
52. Lockshon, D., S. G. Zweifel, L. L. Freeman-Cook, H. E. Lorimer, B. J. Brewer et al., 1995 A role for recombination junctions in the segregation of mitochondrial DNA in yeast. Cell 81: 947–955.
53. Lynch, M., and J. L. Blanchard, 1998 Deleterious mutation accumulation in organelle genomes. Genetica 102–103: 29–39.
54. Lynch, M., W. Sung, K. Morris, N. Coffey, C. R. Landry et al., 2008 A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc. Natl. Acad. Sci. USA 105: 9272–9277.
55. Macreadie, I. G., R. M. Scott, A. R. Zinn, and R. A. Butow, 1985 Transposition of an intron in yeast mitochondria requires a protein encoded by that intron. Cell 41: 395–402.
56. Mancera, E., R. Bourgon, A. Brozzi, W. Huber, and L. M. Steinmetz, 2008 High-resolution mapping of meiotic crossovers and noncrossovers in yeast. Nature 454: 479–485.
57. McKenna, A., M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis et al., 2010 The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20: 1297–1303.
58. Mieczkowski, P. A., M. U. Fikus, and Z. Ciesla, 1997 Characterization of a novel DNA damage-inducible gene of Saccharomyces cerevisiae, DIN7, which is a structural homolog of the RAD2 and RAD27 DNA repair genes. Mol. Gen. Genet. 253: 655–665.
59. Munz, P., H. Amstutz, J. Kohli, and U. Leupold, 1982 Recombination between dispersed serine tRNA genes in Schizosaccharomyces pombe. Nature 300: 225–231.
60. Petes, T. D., 2001 Meiotic recombination hot spots and cold spots. Nat. Rev. Genet. 2: 360–369.
61. Pérez-Martínez, X., S. A. Broadley, and T. D. Fox, 2003 Mss51p promotes mitochondrial Cox1p synthesis and interacts with newly synthesized Cox1p. EMBO J. 22: 5951–5961.
62. Phadnis, N., R. Mehta, N. Meednu, and E. A. Sia, 2006 Ntg1p, the base excision repair protein, generates mutagenic intermediates in yeast mitochondrial DNA. DNA Repair 5: 829–839.
63. Pratt-Hyatt, M. J., K. M. Kapadia, T. E. Wilson, and D. R. Engelke, 2006 Increased recombination between active tRNA genes. DNA Cell Biol. 25: 359–364.
64. Preuten, T., E. Cincu, J. Fuchs, R. Zoschke, K. Liere et al., 2010 Fewer genes than organelles: extremely low and variable gene copy numbers in mitochondria of somatic plant cells. Plant J. 64: 948–959.
65. Shay, J. W., D. J. Pierce, and H. Werbin, 1990 Mitochondrial DNA copy number is proportional to total cell DNA under a variety of growth conditions. J. Biol. Chem. 265: 14802–14807.
66. Shibata, T., and F. Ling, 2007 DNA recombination protein-dependent mechanism of homoplasmy and its proposed functions. Mitochondrion 7: 17–23.
67. Smithson, M., and J. Verkuilen, 2006 A better lemon squeezer? Maximum-likelihood regression with beta-distributed dependent variables. Psychol. Methods 11: 54–71.
68. Solieri, L., 2010 Mitochondrial inheritance in budding yeasts: towards an integrated understanding. Trends Microbiol. 18: 521–530.
69. Solieri, L., O. Antúnez, J. E. Pérez Ortín, E. Barrio, and P. Giudici, 2008 Mitochondrial inheritance and fermentative: oxidative balance in hybrids between Saccharomyces cerevisiae and Saccharomyces uvarum. Yeast 25: 485–500.
70. Song, S., Z. F. Pursell, W. C. Copeland, M. J. Longley, T. A. Kunkel et al., 2005 DNA precursor asymmetries in mammalian tissue mitochondria and possible contribution to mutagenesis through reduced replication fidelity. Proc. Natl. Acad. Sci. USA 102: 4990–4995.
71. Storici, F., L. K. Lewis, and M. A. Resnick, 2001 In vivo site-directed mutagenesis using oligonucleotides. Nat. Biotechnol. 19: 773-776.
72. Strausberg, R. L., and R. A. Butow, 1981 Gene conversion at the VAR1 locus on yeast mitochondrial DNA. Proc. Natl. Acad. Sci. USA 78: 494–498.
73. Strausberg, R. L., and P. S. Perlman, 1978 The effect of zygotic bud position on the transmission of mitochondrial genes in Saccharomyces cerevisiae. Mol. Gen. Genet. 163: 131–144.
74. Strausberg, R. L., R. D. Vincent, P. S. Perlman, and R. A. Butow, 1978 Asymmetric gene conversion at inserted segments on yeast mitochondrial DNA. Nature 276: 577–583.
75. Székvölgyi, L., and A. Nicolas, 2010 From meiosis to postmeiotic events: homologous recombination is obligatory but flexible. FEBS J. 277: 571–589.
76. Wahls, W. P., E. R. Siegel, and M. K. Davidson, 2008 Meiotic recombination hotspots of fission yeast are directed to loci that express non-coding RNA. PLoS ONE 3: e2887.
77. Wallace, D. C., 2007 Why do we still have a maternally inherited mitochondrial DNA? Insights from evolutionary medicine. Annu. Rev. Biochem. 76: 781–821.
78. Wei, W., J. H. McCusker, R. W. Hyman, T. Jones, Y. Ning et al., 2007 Genome sequencing and comparative analysis of Saccharomyces cerevisiae strain YJM789. Proc. Natl. Acad. Sci. USA 104: 12825–12830.
79. White, M. F., and D. M. Lilley, 1997 The resolving enzyme CCE1 of yeast opens the structure of the four-way DNA junction. J. Mol. Biol. 266: 122–134.
80. Wilkening, S., M. M. Tekkedil, G. Lin, E. S. Fritsch, W. Wei et al., 2013 Genotyping 1000 yeast strains by next-generation sequencing. BMC Genomics 14: 90.
81. Wu, T. D., and C. K. Watanabe, 2005 GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21: 1859–1875.
82. Zeyl, C., B. Andreson, and E. Weninck, 2005 Nuclear-mitochondrial epistasis for fitness in Saccharomyces cerevisiae. Evolution 59: 910–914.
83. Zinn, A. R., and R. A. Butow, 1985 Nonreciprocal exchange between alleles of the yeast mitochondrial 21S rRNA gene: kinetics and the involvement of a double-strand break. Cell 40: 887–895.
84. Zinn, A. R., J. K. Pohlman, P. S. Perlman, and R. A. Butow, 1987 Kinetic and segregational analysis of mitochondrial DNA recombination in yeast. Plasmid 17: 248–256.