Crossover Patterning by the Beam-Film Model: Analysis and Implications

PLoS Genetics

Volumn 10, Issue 1, 2014, Pages

  Zhang, Liangran ^a   Liang, Zhangyi ^a   Hutchinson, John ^b   Kleckner, Nancy ^a  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BEAM FILM MODEL; CAELIFERA; CHORTHIPPUS BRUNEUS; CHROMOSOME; CHROMOSOME ANALYSIS; CHROMOSOME SIZE; COEFFICIENT OF COINCIDENCE RELATIONSHIP; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; DROSOPHILA MELANOGASTER; EVENT DISTRIBUTION; HOMEOSTASIS; MATHEMATICAL PARAMETERS; MECHANICAL STRESS; MEIOSIS; MEIOTIC CROSSOVER; MEIOTIC CROSSOVER INTERFERENCE; MOLECULAR MODEL; NONHUMAN; OBLIGATORY MEIOTIC CROSSOVER; PHENOTYPE; PROBABILITY; SACCHAROMYCES CEREVISIAE; SIMULATION; TOMATO;

ANIMALS; CAENORHABDITIS ELEGANS; CHROMOSOMES; CROSSING OVER, GENETIC; MEIOSIS; MODELS, GENETIC; SYNAPTONEMAL COMPLEX;

EID: 84896712493     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004042     Document Type: Article

References (75)

1. Muller HJ, (1916) The Mechanism of Crossing Over. Am Nat 50: 193-434.
2. Sturtevant AH, (1915) The behavior of the chromosomes as studied through linkage. Z indukt Abstamm-u VererbLehre 13: 234-287.
3. Kleckner N, Zickler D, Jones GH, Dekker J, Padmore R, et al. (2004) A mechanical basis for chromosome function. Proc Natl Acad Sci U S A 101: 12592-12597.
4. Borner 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.
5. Hunter N (2006) Meiotic recombination. In: Aguilera A, Rothstein R editors. Molecular Genetics of Recombination. pp 381-442.
6. Drouaud J, Mercier R, Chelysheva L, Berard A, Falque M, et al. (2007) Sex-specific crossover distributions and variations in interference level along Arabidopsis thaliana chromosome 4. PLoS Genet 3: e106.
7. Petkov PM, Broman KW, Szatkiewicz JP, Paigen K, (2007) Crossover interference underlies sex differences in recombination rates. Trends Genet 23: 539-542.
8. Billings T, Sargent EE, Szatkiewicz JP, Leahy N, Kwak IY, et al. (2010) Patterns of recombination activity on mouse chromosome 11 revealed by high resolution mapping. PLoS One 5: e15340.
9. Hillers KJ, Villeneuve AM, (2003) Chromosome-wide control of meiotic crossing over in C. elegans. Curr Biol 13: 1641-1647.
10. Oliver-Bonet M, Campillo M, Turek PJ, Ko E, Martin RH, (2007) Analysis of replication protein A (RPA) in human spermatogenesis. Mol Human Reprod 13: 837-844.
11. de Boer E, Stam P, Dietrich AJ, Pastink A, Heyting C, (2006) Two levels of interference in mouse meiotic recombination. Proc Natl Acad Sci U S A 103: 9607-9612.
12. Storlazzi A, Gargano S, Ruprich-Robert G, Falque M, David M, et al. (2010) Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141: 94-106.
13. Zhang L, Kim KP, Kleckner NE, Storlazzi A, (2011) Meiotic double-strand breaks occur once per pair of (sister) chromatids and, via Mec1/ATR and Tel1/ATM, once per quartet of chromatids. Proc Natl Acad Sci U S A 108: 20036-41.
14. Berchowitz LE, Copenhaver GP, (2010) Genetic interference: don't stand so close to me. Curr Genomics 11: 91-102.
15. 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.
16. Mets DG, Meyer BJ, (2009) Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139: 73-86.
17. McPeek S, Speed TP, Mor H, (1995) Modeling Interference in Genetic Recombination. Genetics 1044: 1031-1044.
18. Falque M, Anderson LK, Stack SM, Gauthier F, Martin OC, (2009) Two types of meiotic crossovers coexist in maize. Plant Cell 21: 3915-3925.
19. Gauthier F, Martin OC, Falque M, (2011) CODA (crossover distribution analyzer): quantitative characterization of crossover position patterns along chromosomes. BMC Bioinformatics 12: 27.
20. Foss E, Lande R, Stahl FW, Steinberg CM, (1993) Chiasma interference as a function of genetic distance. Genetics 133: 681-691.
21. Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG, et al. (2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144: 719-731.
22. Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR, et al. (2008) Global analysis of the meiotic crossover landscape. Dev Cell 15: 401-415.
23. Borde V, Lin W, Novikov E, Petrini JH, Lichten M, et al. (2004) Association of Mre11p with double-strand break sites during yeast meiosis. Mol Cell 13: 389-401.
24. Gerton JL, Derisi J, Shroff R, Lichten M, Brown PO, et al. (2000) Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 97: 11383-11390.
25. Blat Y, Protacio RU, Hunter N, Kleckner N, (2002) Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111: 791-802.
26. Buhler C, Borde V, Lichten M, (2007) Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biol 5: e324.
27. Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, et al. (2013) Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev 27: 873-886.
28. Joyce EF, McKim KS, (2010) Chromosome axis defects induce a checkpoint-mediated delay and interchromosomal effect on crossing over during Drosophila meiosis. PLoS Genet 6: e1001059.
29. Joyce EF, McKim KS, (2011) Meiotic checkpoints and the interchromosomal effect on crossing over in Drosophila females. Fly (Austin) 5: 134-140.
30. Higgins JD, Perry RM, Barakate A, Ramsay L, Waugh R, et al. (2012) Spatiotemporal asymmetry of the meiotic program underlies the predominantly distal distribution of meiotic crossovers in barley. Plant Cell 24: 4096-4109.
31. Fung JC, Rockmill B, Odell M, Roeder GS, (2004) Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116: 795-802.
32. Malkova A, Swanson J, German M, McCusker JH, Housworth EA, et al. (2004) Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII. Genetics 168: 49-63.
33. Charles DR, (1938) The spatial distribution of cross-overs in X-chromosome tetrads of Drosophila melanogaster. J Genetics 36: 103-126.
34. Mehrotra S, McKim KS, (2006) Temporal analysis of meiotic DNA double-strand break formation and repair in Drosophila females. PLoS Genet 2: e200.
35. Lande R, Stahl FW, (1993) Chiasma interference and the distribution of exchanges in Drosophila melanogaster. Cold Spring Harb Symp Quant Biol 58: 543-552.
36. Laurie DA, Jones GH, (1981) Inter-individual variation in chiasma distribution in Chorthippus brunneus (Orthoptera: Acrididae). Heredity 47: 409-416.
37. Jones GH, (1984) The control of chiasma distribution. Symp Soc Exp Biol 38: 293-320.
38. Lhuissier FG, Offenberg HH, Wittich PE, Vischer NO, Heyting C, (2007) The mismatch repair protein MLH1 marks a subset of strongly interfering crossovers in tomato. Plant Cell 19: 862-876.
39. Colombo PC, Jones GH, (1997) Chiasma interference is blind to centromeres. Heredity (Edinb) 79 (Pt 2):: 214-227.
40. Saintenac C, Falque M, Martin OC, Paux E, Feuillet C, et al. (2009) Detailed recombination studies along chromosome 3B provide new insights on crossover distribution in wheat (Triticum aestivum L.). Genetics 181: 393-403.
41. Lian J, Yin Y, Oliver-Bonet M, Liehr T, Ko E, et al. (2008) Variation in crossover interference levels on individual chromosomes from human males. Hum Mol Genet 17: 2583-2594.
42. Broman KW, Rowe LB, Churchill GA, Paigen K, (2002) Crossover interference in the mouse. Genetics 160: 1123-1131.
43. Martini E, Diaz RL, Hunter N, Keeney S, (2006) Crossover homeostasis in yeast meiosis. Cell 126: 285-295.
44. Rosu S, Libuda DE, Villeneuve AM, (2011) Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science 334: 1286-1289.
45. Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, et al. (2012) COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149: 75-87.
46. Globus ST, Keeney S, (2012) The joy of six: how to control your crossovers. Cell 149: 11-12.
47. Jones GH, Franklin FC, (2006) Meiotic crossing-over: obligation and interference. Cell 126: 246-248.
48. Hawley RS, Theurkauf WE, (1993) Requiem for distributive segregation: achiasmate segregation in Drosophila females. Trends Genet 9: 310-317.
49. Argueso JL, Kijas AW, Sarin S, Heck J, Waase M, et al. (2003) Systematic mutagenesis of the Saccharomyces cerevisiae MLH1 gene reveals distinct roles for Mlh1p in meiotic crossing over and in vegetative and meiotic mismatch repair. Mol Cell Biol 23: 873-886.
50. Argueso JL, Wanat J, Gemici Z, Alani E, (2004) Competing crossover pathways act during meiosis in Saccharomyces cerevisiae. Genetics 168: 1805-1816.
51. Zakharyevich K, Tang S, Ma Y, Hunter N, (2012) Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149: 334-347.
52. 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.
53. Franklin WS, Foss HM, (2010) A two-pathway analysis of meiotic crossing over and gene conversion in Saccharomyces cerevisiae. Genetics 186: 515-536.
54. Bzymek M, Thayer NH, Oh SD, Kleckner N, Hunter N, (2010) Double holliday junctions are intermediates of DNA break repair. Nature 464: 937-941.
55. King JS, Mortimer RK, (1990) A polymerization model of chiasma interference and corresponding computer simulation. Genetics 126: 1127-1138.
56. Fujitani Y, Mori S, Kobayashi I, (2002) A reaction-diffusion model for interference in meiotic crossing over. Genetics 161: 365-372.
57. Han YW, Mizuuchi K, (2010) Phage Mu transposition immunity: protein pattern formation along DNA by a diffusion-ratchet mechanism. Mol Cell 39: 48-58.
58. Vecchiarelli AG, Hwang LC, Mizuuchi K, (2013) Cell-free study of F plasmid partition provides evidence for cargo transport by a diffusion-ratchet mechanism. Proc Natl Acad Sci U S A 110: E1390-1397.
59. Hulten MA, (2011) On the origin of crossover interference: A chromosome oscillatory movement (COM) model. Mol Cytogenet 4: 10.
60. Getz TJ, Banse SA, Young LS, Banse AV, Swanson J, et al. (2008) Reduced mismatch repair of heteroduplexes reveals "non"-interfering crossing over in wild-type Saccharomyces cerevisiae. Genetics 178: 1251-1269.
61. Straight AF, Belmont A S, Robinett CC, Murray AW, (1996) GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr Biol 6: 1599-1608.
62. Hollingsworth NM, Ponte L, Halsey C, (1995) MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair. Genes Dev 9: 1728-1739.
63. Agarwal S, Roeder GS, (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245-255.
64. Chua PR, Roeder GS, (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349-359.
65. Cherry JM, Ball C, Weng S, Juvik G, Schmidt R, et al. (1997) Genetic and physical maps of Saccharomyces cerevisiae. Nature 387: 67-73.
66. Koszul R, Kleckner N, (2009) Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends Cell Biol 19: 716-724.
67. Loidl J, Klein F, Engebrecht J, (1998) Genetic and morphological approaches for the analysis of meiotic chromosomes in yeast. Methods Cell Biol 53: 257-285.
68. Kim PK, Weiner BM, Zhang L, Jordan A, Dekker J, et al. (2010) Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143: 924-937.
69. Qiao H, Lohmiller LD, Anderson LK, (2011) Cohesin proteins load sequentially during prophase I in tomato primary microsporocytes. Chromosome Res 19: 193-207.
70. Dolezel J, Bartos J, Voglmayr H, Greilhuber J, (2003) Nuclear DNA content and genome size of trout and human. Cytometry A 51: 127-128.
71. Santos J, del Cerro A, Díez M, (1993) Spreading synaptonemal complexes from the grasshopper Chorthippus jacobsi: pachytene and zygotene observations. Hereditas 118: 235-241 Hereditas 118: 235-241.
72. Page SL, Hawley RS, (2001) c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev 15: 3130-3143.
73. Carpenter AT, (1979) Recombination nodules and synaptonemal complex in recombination-defective females of Drosophila melanogaster. Chromosoma 75: 259-292.
74. Peterson DG, Stack SM, Price JH, Johnston JS, DNA content of heterochromatin and euchromatin in tomato (Lycopersicon esculentum) pachytene chromosomes. Genome 39: 77-82.
75. Sherman JD, Stack SM, (1995) Two-dimensional spreads of synaptonemal complexes from solanaceous plants. VI. High-resolution recombination nodule map for tomato (Lycopersicon esculentum). Genetics 141: 683-708.