Meiotic crossover patterns: Obligatory crossover, interference and homeostasis in a single process

Cell Cycle

Volumn 14, Issue 3, 2015, Pages 305-314

  Wang, Shunxin ^a   Zickler, Denise ^b   Kleckner, Nancy ^a   Zhang, Liangran ^a  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Beam film model; Crossover; Crossover homeostasis; Crossover interference; Meiosis; Obligatory crossover; Recombination

Indexed keywords

DNA; DNA TOPOISOMERASE (ATP HYDROLYSING);

CHROMOSOME ARM; CHROMOSOME SIZE; CROSSING OVER; GENETIC DISTANCE; HOMEOSTASIS; MECHANICAL STRESS; MEIOSIS; MEIOTIC RECOMBINATION; NONHUMAN; REVIEW; SISTER CHROMATID; SUMOYLATION; TRANSPOSON; BIOLOGICAL MODEL; CHROMOSOME; GENETICS; METABOLISM;

CHROMOSOMES; CROSSING OVER, GENETIC; HOMEOSTASIS; MEIOSIS; MODELS, BIOLOGICAL;

EID: 84923203447     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/15384101.2014.991185     Document Type: Review

References (76)

1. Kleckner N, Zhang L, Weiner B, Zickler D. Meiotic chromosome dynamics. In: Rippe, ed. Genome Organization and Function in the Mammalian Cell Nucleus. New York: John Wiley and Sons, 2011: 487-534.
2. Zickler D, Kleckner N. Recombination, pairing and synapsis of homologs in meiosis. In: Kowalczykowski S, Hunter N, Heyer WD. DNA Replication. Cold Spring Harbor: Cold Spring Harbor Press, 2015; in press.
3. Berchowitz LE, Copenhaver GP. Genetic interference: Don't stand so close to me. Curr Genomics 2010; 11 (2): 91-102; PMID: 20885817; http://dx.doi.org/10.2174/138920210790886835
4. Jones GH, Franklin FC. Meiotic crossing-over: Obligation and interference. Cell 2006; 126(2): 246-8; PMID: 16873056; http://dx.doi.org/10.1016/j.cell.2006.07.010
5. Jones GH. The control of chiasma distribution. Symp Soc Exp Biol 1984; 38: 293-320; PMID: 6545727
6. Martini E, Diaz RL, Hunter N, Keeney S. Crossover homeostasis in yeast meiosis. Cell 2006; 126(2): 285-95; PMID: 16873061; http://dx.doi.org/10.1016/j.cell.2006.05.044
7. Cole F, Kauppi L, Lange J, Roig I, Wang R, Keeney S, Jasin M. Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Biol 2012; 14(4): 424-30; PMID: 22388890; http://dx.doi.org/10.1038/ncb2451
8. Globus ST, Keeney S. The joy of six: How to control your crossovers. Cell 2012; 149(1): 11-2; PMID: 22464316; http://dx.doi.org/10.1016/j.cell.2012.03.011
9. Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, Villeneuve AM. COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 2012; 149(1): 75-87; PMID: 22464324; http://dx.doi.org/10.1016/j.cell.2012.01.052
10. Zhang L, Liang Z, Hutchinson J, Kleckner N. Crossover patterning by the beam-film model: Analysis and implications. PLoS Genet 2014; 10(1): E1004042; PMID: 24497834; http://dx.doi.org/10.1371/journal.pgen.1004042
11. Zhang L, Wang S, Yin S, Hong S, Kim KP, Kleckner N. Topoisomerase II mediatesmeiotic crossover interference. Nature 2014; 511(7511): 551-6; PMID: 25043020; http://dx.doi.org/10.1038/nature13442
12. Mehrotra S, McKim KS. Temporal analysis of meiotic DNA double-strand break formation and repair in Drosophila females. PLoS Genet 2006; 2(11): E200; PMID: 17166055; http://dx.doi.org/10.1371/journal.pgen.0020200
13. de Boer E, Stam P, Dietrich AJ, Pastink A, Heyting C. Two levels of interference in mouse meiotic recombination. Proc Natl Acad Sci U S A 2006; 103(25): 9607-12; PMID: 16766662; http://dx.doi.org/10.1073/pnas.0600418103
14. Broman KW, Weber JL. Characterization of human crossover interference. Am J Hum Genet 2000; 66 (6): 1911-26; PMID: 10801387; http://dx.doi.org/10.1086/302923
15. McPeek MS, Speed TP. Modeling interference in genetic recombination. Genetics 1995; 139(2): 1031-44; PMID: 7713406
16. Falque M, Anderson LK, Stack SM, Gauthier F, Martin OC. Two types of meiotic crossovers coexist in maize. Plant Cell 2009; 21(12): 3915-25; PMID: 20040539; http://dx.doi.org/10.1105/tpc.109.071514
17. Muller HJ. The Mechanism of Crossing Over. Am Nat 1916; 50: 193-434; http://dx.doi.org/10.1086/279534
18. Sturtevant AH. The behavior of the chromosomes as studied through linkage. Z Indukt Abstamm-u VererbLehre 1915; 13: 234-87.
19. Charles DR. The spatial distribution of cross-overs in X-chromosome tetrads of Drosophila melanogaster. J Genetics 1938; 36: 103-26; http://dx.doi.org/10.1007/BF02982376
20. Kleckner N, Zickler D, Jones GH, Dekker J, Padmore R, Henle J, Hutchinson J. A mechanical basis for chromosome function. Proc Natl Acad Sci U S A 2004; 101(34): 12592-7; PMID: 15299144; http://dx.doi.org/10.1073/pnas.0402724101
21. Lebofsky R, Heilig R, Sonnleitner M, Weissenbach J, Bensimon A. DNA replication origin interference increases the spacing between initiation events in human cells. Mol Biol Cell 2006; 17(12): 5337-45; PMID: 17005913; http://dx.doi.org/10.1091/mbc. E06-04-0298
22. Maeshima K, Eltsov M, Laemmli UK. Chromosome structure: Improved immunolabeling for electron microscopy. Chromosoma 2005; 114(5): 365-75; PMID: 16175370; http://dx.doi.org/10.1007/s00412-005-0023-7
23. Kleckner N. Mesoscale spatial patterning in the Escherichia coli Min system: Reaction-diffusion versus mechanical communication. Proc Natl Acad Sci U S A 2010; 107(18): 8053-4; PMID: 20421460; http://dx.doi.org/10.1073/pnas.1002477107
24. Vecchiarelli AG, Hwang LC, Mizuuchi K. Cell-free study of F plasmid partition provides evidence for cargo transport by a diffusion-ratchet mechanism. Proc Natl Acad Sci USA 2013; 110(15): E1390-7; PMID: 23479605; http://dx.doi.org/10.1073/pnas.1302745110
25. Ivanov V, Mizuuchi K. Multiple modes of interconverting dynamic pattern formation by bacterial cell division proteins. Proc Natl Acad Sci USA 2010; 107(18): 8071-8; PMID: 20212106; http://dx.doi.org/10.1073/pnas.0911036107
26. Lao JP, Cloud V, Huang CC, Grubb J, Thacker D, Lee CY, Dresser ME, Hunter N, Bishop DK. Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLoS Genet 2013; 9(12): E1003978; PMID: 24367271; http://dx.doi.org/10.1371/journal.pgen.1003978
27. Hillers KJ, Villeneuve AM. Chromosome-wide control of meiotic crossing over in C. elegans. Curr Biol 2003; 13(18): 1641-7; PMID: 13678597; http://dx.doi.org/10.1016/j.cub.2003.08.026
28. Keeney S. Spo11 and the formation of DNA double-strand breaks in meiosis. Genome Dyn Stab 2008; 2: 81-123; PMID: 21927624; http://dx.doi.org/10.1007/7050-2007-026
29. Kleckner N. Chiasma formation: Chromatin/axis interplay and the role(s) of the synaptonemal complex. Chromosoma 2006; 115(3): 175-94; PMID: 16555016; http://dx.doi.org/10.1007/s00412-006-0055-7
30. Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, Shirahige K, Klein F. Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 2011; 146(3): 372-83; PMID: 21816273; http://dx.doi.org/10.1016/j.cell.2011.07.003
31. Lichten M, de Massy B. The impressionistic landscape of meiotic recombination. Cell 2011; 147(2): 267-70; PMID: 22000007; http://dx.doi.org/10.1016/j.cell.2011.09.038
32. Borde V, de Massy B. Programmed induction of DNA double strand breaks during meiosis: Setting up communication between DNA and the chromosome structure. Curr Opin Genet Dev 2013; 23(2): 147-55; PMID: 23313097; http://dx.doi.org/10.1016/j.gde.2012.12.002
33. de Massy B. Initiation of meiotic recombination: How and where? Conservation and specificities among eukaryotes. Annu Rev Genet 2013; 47: 563-99; PMID: 24050176; http://dx.doi.org/10.1146/annurevgenet-110711-155423
34. Blat Y, Protacio RU, Hunter N, Kleckner N. Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 2002; 111: 791-802; http://dx.doi.org/10.1016/S0092-8674(02)01167-4
35. Storlazzi A, Gargano S, Ruprich-Robert G, Falque M, David M, Kleckner N, Zickler D. Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 2010; 141(1): 94-106; PMID: 20371348; http://dx.doi.org/10.1016/j.cell.2010.02.041
36. Zhang L, Espagne E, de Muyt A, Zickler D, Kleckner NE. Interference-mediated synaptonemal complex formation with embedded crossover designation. Proc Natl Acad Sci U S A 2014: Pii: 201416411. [Epub ahead of print]; PMID: 25380597
37. Zickler D, Kleckner N. Meiotic chromosomes: Integrating structure and function. Annu Rev Genet 1999; 33: 603-754; PMID: 10690419; http://dx.doi.org/10.1146/annurev.genet.33.1.603
38. De Muyt A, Zhang L, Piolot T, Kleckner N, Espagne E, Zickler D. E3 ligaseHei10: A multifaceted structure-based signaling molecule with roles within and beyond meiosis. Genes Dev 2014; 28(10): 1111-23; PMID: 24831702; http://dx.doi.org/10.1101/gad.240408.114
39. Fraune J, Schramm S, Alsheimer M, Benavente R. The mammalian synaptonemal complex: Protein components, assembly and role in meiotic recombination. Exp Cell Res 2012; 318(12): 1340-6; PMID: 22394509; http://dx.doi.org/10.1016/j.yexcr.2012.02.018
40. Espagne E, Vasnier C, Storlazzi A, Kleckner NE, Silar P, Zickler D, Malagnac F. Sme4 coiled-coil protein mediates synaptonemal complex assembly, recombinosome relocalization, and spindle pole body morphogenesis. Proc Natl Acad Sci U S A 2011; 108(26): 10614-9; PMID: 21666097; http://dx.doi.org/10.1073/pnas.1107272108
41. Bishop DK, Zickler D. Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 2004; 117(1): 9-15; PMID: 15066278; http://dx.doi.org/10.1016/S0092-8674(04)00297-1
42. Börner GV, Kleckner N, Hunter N. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 2004; 117(1): 29-45; PMID: 15066280; http://dx.doi.org/10.1016/S0092-8674(04)00292-2
43. Fung JC, Rockmill B, Odell M, Roeder GS. Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 2004; 116 (6): 795-802; PMID: 15035982; http://dx.doi.org/10.1016/S0092-8674(04)00249-1
44. Reynolds A, Qiao H, Yang Y, Chen JK, Jackson N, Biswas K, Holloway JK, Baudat F, de Massy B, Wang J, et al. RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat Genet 2013; 45(3): 269-78; http://dx.doi.org/10.1038/ng.2541
45. Hunter N. Meiotic recombination. In: Aguilera A, Rothstein R, eds. Molecular Genetics of Recombination. Heidelberg: Springer Berlin, 2006: 381-442.
46. Osman K, Higgins JD, Sanchez-Moran E, Armstrong SJ, Franklin FC. Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 2011; 190(3): 523 44; PMID: 21366595; http://dx.doi.org/10.1111/j.1469-8137.2011.03665.x
47. Baudat F, de Massy B. Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res 2007; 15(5): 565-77; PMID: 17674146; http://dx.doi.org/10.1007/s10577-007-1140-3
48. Tesse S, Storlazzi A, Kleckner N, Gargano S, Zickler D. Localization and roles of Ski8p protein in Sordaria meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition. Proc Natl Acad Sci U S A 2003; 100: 12865-70; http://dx.doi.org/10.1073/pnas.2034282100
49. Rog O, Dernburg AF. Chromosome pairing and synapsis during Caenorhabditis elegans meiosis. Curr Opin Cell Biol 2013; 25(3): 349-56; PMID: 23578368; http://dx.doi.org/10.1016/j.ceb.2013.03.003
50. Lui DY, Colaiácovo MP. Meiotic development in Caenorhabditis elegans. Adv Exp Med Biol 2013; 757: 133-70; PMID: 22872477; http://dx.doi.org/10.1007/978-1-4614-4015-4-6
51. Libuda DE, Uzawa S, Meyer BJ, Villeneuve AM. Meiotic chromosome structures constrain and respond to designation of crossover sites. Nature 2013; 502 (7473): 703-6; PMID: 24107990; http://dx.doi.org/10.1038/nature12577
52. Drouaud J, Mercier R, Chelysheva L, Bérard A, Falque M, Martin O, Zanni V, Brunel D, Mézard C. Sex-specific crossover distributions and variations in interference level along Arabidopsis thaliana chromosome 4. PLoS Genet 2007; 3(6): E106; PMID: 17604455
53. Petkov PM, Broman KW, Szatkiewicz JP, Paigen K. Crossover interference underlies sex differences in recombination rates. Trends Genet 2007; 23(11): 539-42; PMID: 17964681; http://dx.doi.org/10.1016/j.tig.2007.08.015
54. Hou Y, Fan W, Yan L, Li R, Lian Y, Huang J, Li J, Xu L, Tang F, Xie XS, et al. Genome analyses of single human oocytes. Cell 2013; 155(7): 1492-506; PMID: 24360273; http://dx.doi.org/10.1016/j.cell.2013.11.040
55. Shinohara M, Oh SD, Hunter N, Shinohara A. Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat Genet 2008; 40(3): 299-309; PMID: 18297071; http://dx.doi.org/10.1038/ng.83
56. King JS, Mortimer RK. A polymerization model of chiasma interference and corresponding computer simulation. Genetics 1990; 126(4): 1127-38; PMID: 2127577
57. Lande R, Stahl FW. Chiasma interference and the distribution of exchanges in Drosophila melanogaster. Cold Spring Harb Symp Quant Biol 1993; 58: 543-52; PMID: 7956068; http://dx.doi.org/10.1101/SQB.1993.058.01.061
58. Getz TJ, Banse SA, Young LS, Banse AV, Swanson J, Wang GM, Browne BL, Foss HM, Stahl FW. Reduced mismatch repair of heteroduplexes reveals "non"-interfering crossing over in wild-type Saccharomyces cerevisiae. Genetics 2008 178(3): 1251-69; PMID: 18385111; http://dx.doi.org/10.1534/genetics.106.067603
59. Fujitani Y, Kawai J, Kobayashi I. Random-walk mechanism in the genetic recombination. Adv Exp Med Biol 2010; 680: 275-82; PMID: 20865510; http://dx.doi.org/10.1007/978-1-4419-5913-3-31
60. Hulten MA. On the origin of crossover interference: A chromosome oscillatory movement (COM) model. Mol Cytogenet 2011; 4: 10; http://dx.doi.org/10.1186/1755-8166-4-10
61. Zickler D, Moreau PJ, Huynh AD, Slezec AM. Correlation between pairing initiation sites, recombination nodules and meiotic recombination in Sordaria macrospora. Genetics 1992; 132(1): 135-48; PMID: 1398050
62. Joyce EF, McKim KS. Chromosome axis defects induce a checkpointmediated delay and interchromosomal effect on crossing over during Drosophila meiosis. PLoS Genet 2010; 6: E1001059.
63. Joyce EF, McKim KS. Meiotic checkpoints and the interchromosomal effect on crossing over in Drosophila females. Fly (Austin) 2011; 5: 134-40; http://dx.doi.org/10.4161/fly.5.2.14767
64. Gruhn JR, Rubio C, Broman KW, Hunt PA, Hassold T. Cytological studies of human meiosis: Sex-specific differences in recombination originate at, or prior to, establishment of double-strand breaks. PLoS One 2013; 8(12): E85075; PMID: 24376867; http://dx.doi.org/10.1371/journal.pone.0085075
65. Lynn A, Kashuk C, Petersen MB, Bailey JA, Cox DR, Antonarakis SE, Chakravarti A. Patterns of meiotic recombination on the long arm of human chromosome 21. Genome Res 2000; 10(9): 1319-32; PMID: 10984450; http://dx.doi.org/10.1101/gr.138100
66. Tease C, Hartshorne GM, Hultén MA. Patterns of meiotic recombination in human fetal oocytes. Am J Hum Genet 2002; 70(6): 1469-79; PMID: 11992253; http://dx.doi.org/10.1086/340734
67. Tease C, Hultén MA. Inter-sex variation in synaptonemal complex lengths largely determine the different recombination rates in male and female germ cells. Cytogenet Genome Res 2004; 107(3-4): 208-15; PMID: 15467366; http://dx.doi.org/10.1159/000080599
68. Kleckner N, Storlazzi A, Zickler D. Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length. Trends Genet 2003; 19(11): 623-8; PMID: 14585614; http://dx.doi.org/10.1016/j.tig. 2003.09.004
69. Risch N, Stein Z, Kline J, Warburton D. The relationship between maternal age and chromosome size in autosomal trisomy. Am J Hum Genet 1986; 39(1): 68-78; PMID: 3752082
70. Sun F, Mikhaail-Philips M, Oliver-Bonet M, Ko E, Rademaker A, Turek P, Martin RH. The relationship between meiotic recombination in human spermatocytes and aneuploidy in sperm. Hum Reprod 2008; 23 (8): 1691-7; PMID: 18482994; http://dx.doi.org/10.1093/humrep/den027
71. Crismani W, Girard C, Froger N, Pradillo M, Santos JL, Chelysheva L, Copenhaver GP, Horlow C, Mercier R. FANCM limits meiotic crossovers. Science 2012; 336(6088): 1588-90; PMID: 22723424; http://dx.doi.org/10.1126/science.1220381
72. Girard C, Crismani W, Froger N, Mazel J, Lemhemdi A, Horlow C, Mercier R. FANCM-associated proteins MHF1 and MHF2, but not the other Fanconi anemia factors, limit meiotic crossovers. Nucleic Acids Res 2014; 42(14): 9087-95; PMID: 25038251; http://dx.doi.org/10.1093/nar/gku614
73. Munz P. An analysis of interference in the fission yeast Schizosaccharomyces pombe. Genetics 1994; 137 (3): 701-7; PMID: 8088515
74. Strickland WN. An analysis of interference in Aspergillus nidulans. Proc R Soc Lond B Biol Sci 1958; 149 (934): 82-101; PMID: 13554433; http://dx.doi.org/10.1098/rspb.1958.0053
75. Egel-Mitani M, Olson LW, Egel R. Meiosis in Aspergillus nidulans: Another example for lacking synaptonemal complexes in the absence of crossover interference. Hereditas 1982; 97(2): 179-87; PMID: 6761318; http://dx.doi.org/10.1111/j.1601-5223.1982.tb00761.x
76. Maeshima K, Laemmli UK. A two-step scaffolding model for mitotic chromosome assembly. Dev Cell 2003; 4(4): 467-80; PMID: 12689587; http://dx.doi.org/10.1016/S1534-5807(03)00092-3