Eliminating Both Canonical and Short-Patch Mismatch Repair in Drosophila melanogaster Suggests a New Meiotic Recombination Model

PLoS Genetics

Volumn 10, Issue 9, 2014, Pages

  Crown, K Nicole ^a   McMahan, Susan ^a   Sekelsky, Jeff ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HETERODUPLEX DNA; UNCLASSIFIED DRUG; CRUCIFORM DNA; DNA HELICASE; HETERODUPLEX;

ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME SEGREGATION; COMPLEX FORMATION; CONTROLLED STUDY; CROSSING OVER; DNA STRAND BREAKAGE; DROSOPHILA MELANOGASTER; EXCISION REPAIR; FEMALE; GENE CONVERSION; GENE INACTIVATION; HOLLIDAY JUNCTION; MALE; MISMATCH REPAIR; MITOTIC RECOMBINATION; MOLECULAR MODEL; NONHUMAN; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; YEAST; ANIMAL; DOUBLE STRANDED DNA BREAK; GENETICS; MEIOSIS; METABOLISM;

ANIMALS; CHROMOSOME SEGREGATION; CROSSING OVER, GENETIC; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA MISMATCH REPAIR; DNA, CRUCIFORM; DROSOPHILA MELANOGASTER; MEIOSIS; NUCLEIC ACID HETERODUPLEXES;

EID: 84907584492     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004583     Document Type: Article

References (61)

1. Kohl KP, Sekelsky J, (2013) Meiotic and mitotic recombination in meiosis. Genetics 194: 327–334.
2. Bishop DK, Zickler D, (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117: 9–15.
3. Schwacha A, Kleckner N, (1995) Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83: 783–791.
4. Hunter N, Kleckner N, (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell 106: 59–70.
5. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW, (1983) The double-strand-break repair model for recombination. Cell 33: 25–35.
6. Lafleuriel J, Degroote F, Depeiges A, Picard G, (2007) Impact of the loss of AtMSH2 on double-strand break-induced recombination between highly diverged homeologous sequences in Arabidopsis thaliana germinal tissues. Plant Mol Biol 63: 833–846.
7. Martini E, Borde V, Legendre M, Audic S, Regnault B, et al. (2011) Genome-wide analysis of heteroduplex DNA in mismatch repair-deficient yeast cells reveals novel properties of meiotic recombination pathways. PLoS Genet 7: e1002305.
8. Radford SJ, Sabourin MM, McMahan S, Sekelsky J, (2007) Meiotic recombination in Drosophila Msh6 mutants yields discontinuous gene conversion tracts. Genetics 176: 53–62.
9. Svetlanov A, Baudat F, Cohen PE, de Massy B, (2008) Distinct functions of MLH3 at recombination hot spots in the mouse. Genetics 178: 1937–1945.
10. Guillon H, Baudat F, Grey C, Liskay RM, de Massy B, (2005) Crossover and noncrossover pathways in mouse meiosis. Mol Cell 20: 563–573.
11. Kunkel TA, Erie DA, (2005) DNA mismatch repair. Annu Rev Biochem 74: 681–710.
12. Sekelsky JJ, Brodsky MH, Burtis KC, (2000) DNA repair in Drosophila: insights from the Drosophila genome sequence. J Cell Biol 150: F31–36.
13. Fleck O, Lehmann E, Schar P, Kohli J, (1999) Involvement of nucleotide-excision repair in msh2 pms1-independent mismatch repair. Nat Genet 21: 314–317.
14. Coïc E, Gluck L, Fabre F, (2000) Evidence for short-patch mismatch repair in Saccharomyces cerevisiae. EMBO J 19: 3408–3417.
15. Oda S, Humbert O, Fiumicino S, Bignami M, Karran P, (2000) Efficient repair of A/C mismatches in mouse cells deficient in long-patch mismatch repair. EMBO J 19: 1711–1718.
16. Muheim-Lenz R, Buterin T, Marra G, Naegeli H, (2004) Short-patch correction of C/C mismatches in human cells. Nucleic Acids Res 32: 6696–6705.
17. Guo X, Jinks-Robertson S, (2013) Removal of N-6-methyladenine by the nucleotide excision repair pathway triggers the repair of mismatches in yeast gap-repair intermediates. DNA Repair (Amst) 12: 1053–1061.
18. Radford SJ, McMahan S, Blanton HL, Sekelsky J, (2007) Heteroduplex DNA in meiotic recombination in Drosophila mei-9 mutants. Genetics 176: 63–72.
19. Tomkinson AE, Bardwell AJ, Bardwell L, Tappe NJ, Friedberg EC, (1993) Yeast DNA repair and recombination proteins Rad1 and Rad10 constitute a single-stranded-DNA endonuclease. Nature 263: 860–862.
20. Bardwell AJ, Bardwell L, Tomkinson AE, Friedberg EC, (1994) Specific cleavage of model recombination and repair intermediates by the yeast Rad1-Rad10 DNA endonuclease. Science 265: 2082–2085.
21. Park CH, Bessho T, Matsunaga T, Sancar A, (1995) Purification and characterization of the XPF-ERCC1 complex of human DNA repair excision nuclease. J Biol Chem 270: 22657–22660.
22. Sekelsky JJ, McKim KS, Chin GM, Hawley RS, (1995) The Drosophila meiotic recombination gene mei-9 encodes a homologue of the yeast excision repair protein Rad1. Genetics 141: 619–627.
23. Baker BS, Carpenter ATC, (1972) Genetic analysis of sex chromosomal meiotic mutants in Drosophila melanogaster. Genetics 71: 255–286.
24. Goosen N, (2010) Scanning the DNA for damage by the nucleotide excision repair machinery. DNA Repair (Amst) 9: 593–596.
25. Chovnick A, Ballantyne GH, Baillie DL, Holm DG, (1970) Gene conversion in higher organisms: half-tetrad analysis of recombination within the rosy cistron of Drosophila melanogaster. Genetics 66: 315–329.
26. Blanton HL, Radford SJ, McMahan S, Kearney HM, Ibrahim JG, et al. (2005) REC, Drosophila MCM8, drives formation of meiotic crossovers. PLoS Genet 1: e40.
27. Huang JC, Svoboda DL, Reardon JT, Sancar A, (1992) Human nucleotide excision nuclease removes thymine dimers from DNA by incising the 22nd phosphodiester bond 5′ and the 6th phosphodiester bond 3′ to the photodimer. Proc Natl Acad Sci U S A 89: 3664–3668.
28. Sekelsky JJ, Hollis KJ, Eimerl AI, Burtis KC, Hawley RS, (2000) Nucleotide excision repair endonuclease genes in Drosophila melanogaster. Mutat Res 459: 219–228.
29. Hilliker AJ, Clark SH, Chovnick A, (1991) The effect of DNA sequence polymorphisms on intragenic recombination in the rosy locus of Drosophila melanogaster. Genetics 129: 779–781.
30. Carpenter ATC, (1982) Mismatch repair, gene conversion, and crossing-over in two recombination-defective mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A 79: 5961–5965.
31. Mitchel K, Lehner K, Jinks-Robertson S, (2013) Heteroduplex DNA position defines the roles of the Sgs1, Srs2, and Mph1 helicases in promoting distinct recombination outcomes. PLoS Genet 9: e1003340.
32. Gilbertson LA, Stahl FW, (1996) A test of the double-strand break repair model for meiotic recombination in Saccharomyces cerevisiae. Genetics 144: 27–41.
33. Jessop L, Allers T, Lichten M, (2005) Infrequent co-conversion of markers flanking a meiotic recombination initiation site in Saccharomyces cerevisiae. Genetics 169: 1353–1367.
34. Baker MD, Birmingham EC, (2001) Evidence for biased Holliday junction cleavage and mismatch repair directed by junction cuts during double-strand-break repair in mammalian cells. Mol Cell Biol 21: 3425–3435.
35. Foss HM, Hillers KJ, Stahl FW, (1999) The conversion gradients at HIS4 of Saccharomyces cerevisiae. II. A role for mismatch repair directed by biased resolution of the recombinational intermediate. Genetics 153: 573–583.
36. Schwartz EK, Heyer WD, (2011) Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma 120: 109–127.
37. Kohl KP, Jones CD, Sekelsky J, (2012) Evolution of an MCM complex in flies that promotes meiotic crossovers by blocking BLM helicase. Science 338: 1363–1365.
38. Rockmill B, Lefrancois P, Voelkel-Meiman K, Oke A, Roeder GS, et al. (2013) High throughput sequencing reveals alterations in the recombination signatures with diminishing spo11 activity. PLoS Genet 9: e1003932.
39. Hilliker AJ, Harauz G, Reaume AG, Gray M, Clark SH, et al. (1994) Meiotic gene conversion tract length distribution within the rosy locus of Drosophila melanogaster. Genetics 137: 1019–1024.
40. Porter SE, White MA, Petes TD, (1993) Genetic evidence that the meiotic recombination hotspot at the HIS4 locus of Saccharomyces cerevisiae does not represent a site for a symmetrically processed double-strand break. Genetics 134: 5–19.
41. Merker JD, Dominska M, Petes TD, (2003) Patterns of heteroduplex formation associated with the initiation of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics 165: 47–63.
42. Miller DE, Takeo S, Nandanan K, Paulson A, Gogol MM, et al. (2012) A whole-chromosome analysis of meiotic recombination in Drosophila melanogaster. G3 (Bethesda) 2: 249–260.
43. Comeron JM, Ratnappan R, Bailin S, (2012) The many landscapes of recombination in Drosophila melanogaster. PLoS Genet 8: e1002905.
44. Clark SH, Hilliker AJ, Chovnick A, (1988) Recombination can initiate and terminate at a large number of sites within the rosy locus of Drosophila melanogaster. Genetics 118: 261–266.
45. Allers T, Lichten M, (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47–57.
46. De Muyt A, Jessop L, Kolar E, Sourirajan A, Chen J, et al. (2012) BLM helicase ortholog Sgs1 is a central regulator of meiotic recombination intermediate metabolism. Mol Cell 46: 43–53.
47. Chovnick A, Gelbart WM, McCarron MY, Pandey J (1993) Studies on recombination in higher organisms. In: Grell RF, editor. Mechanisms in Recombination. New York, NY: Plenum Publishing Corporation. pp. 351–364.
48. Oh SD, Lao JP, Hwang PY, Taylor AF, Smith GR, et al. (2007) BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 130: 259–272.
49. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM, (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454: 479–485.
50. Curtis D, Clark S, Chovnick A, Bender W, (1989) Molecular analysis of recombination events in Drosophila. Genetics 122: 653–661.
51. McMahan S, Kohl KP, Sekelsky J, (2013) Variation in meiotic recombination frequencies between allelic transgenes inserted at different sites in the Drosophila melanogaster genome. G3 (Bethesda) 3: 1419–1427.
52. Hunter N, (2003) Synaptonemal complexities and commonalities. Mol Cell 12: 533–535.
53. McKim KS, Green-Marroquin BL, Sekelsky JJ, Chin G, Steinberg C, et al. (1998) Meiotic synapsis in the absence of recombination. Science 279: 876–878.
54. Mehrotra S, McKim KS, (2006) Temporal analysis of meiotic DNA double-strand break formation and repair in Drosophila females. PLoS Genet 2: e200.
55. Börner GV, Kleckner N, Hunter N, (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29–45.
56. Jessop L, Rockmill B, Roeder GS, Lichten M, (2006) Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of Sgs1. PLoS Genet 2: e155.
57. Kneitz B, Cohen PE, Avdievich E, Zhu L, Kane MF, et al. (2000) MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev 14: 1085–1097.
58. Baudat F, de Massy B, (2007) Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res 15: 565–577.
59. Drouaud J, Khademian H, Giraut L, Zanni V, Bellalou S, et al. (2013) Contrasted patterns of crossover and non-crossover at Arabidopsis thaliana meiotic recombination hotspots. PLoS Genet 9: e1003922.
60. Cole F, Kauppi L, Lange J, Roig I, Wang R, et al. (2012) Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Biol 14: 424–430.
61. Hilliker AJ, Clark SH, Chovnick A (1988) Genetic analysis of intragenic recombination in Drosophila. In: Low KB, editor. The Recombination of Genetic Material. New York: Academic Press. pp. 73–90.