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


Crossing-over is a central feature of meiosis. Meiotic crossover (CO) sites are spatially patterned along chromosomes. CO-designation at one position disfavors subsequent CO-designation(s) nearby, as described by the classical phenomenon of CO interference. If multiple designations occur, COs tend to be evenly spaced. We have previously proposed a mechanical model by which CO patterning could occur. The central feature of a mechanical mechanism is that communication along the chromosomes, as required for CO interference, can occur by redistribution of mechanical stress. Here we further explore the nature of the beam-film model, its ability to quantitatively explain CO patterns in detail in several organisms, and its implications for three important patterning-related phenomena: CO homeostasis, the fact that the level of zero-CO bivalents can be low (the “obligatory CO”), and the occurrence of non-interfering COs. Relationships to other models are discussed.


Vyšlo v časopise: Crossover Patterning by the Beam-Film Model: Analysis and Implications. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1004042
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004042

Souhrn

Crossing-over is a central feature of meiosis. Meiotic crossover (CO) sites are spatially patterned along chromosomes. CO-designation at one position disfavors subsequent CO-designation(s) nearby, as described by the classical phenomenon of CO interference. If multiple designations occur, COs tend to be evenly spaced. We have previously proposed a mechanical model by which CO patterning could occur. The central feature of a mechanical mechanism is that communication along the chromosomes, as required for CO interference, can occur by redistribution of mechanical stress. Here we further explore the nature of the beam-film model, its ability to quantitatively explain CO patterns in detail in several organisms, and its implications for three important patterning-related phenomena: CO homeostasis, the fact that the level of zero-CO bivalents can be low (the “obligatory CO”), and the occurrence of non-interfering COs. Relationships to other models are discussed.


Zdroje

1. MullerHJ (1916) The Mechanism of Crossing Over. Am Nat 50: 193–434.

2. SturtevantAH (1915) The behavior of the chromosomes as studied through linkage. Z indukt Abstamm-u VererbLehre 13: 234–287.

3. KlecknerN, ZicklerD, JonesGH, DekkerJ, PadmoreR, et al. (2004) A mechanical basis for chromosome function. Proc Natl Acad Sci U S A 101: 12592–12597.

4. BornerGV, KlecknerN, HunterN (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. DrouaudJ, MercierR, ChelyshevaL, BerardA, FalqueM, et al. (2007) Sex-specific crossover distributions and variations in interference level along Arabidopsis thaliana chromosome 4. PLoS Genet 3: e106.

7. PetkovPM, BromanKW, SzatkiewiczJP, PaigenK (2007) Crossover interference underlies sex differences in recombination rates. Trends Genet 23: 539–542.

8. BillingsT, SargentEE, SzatkiewiczJP, LeahyN, KwakIY, et al. (2010) Patterns of recombination activity on mouse chromosome 11 revealed by high resolution mapping. PLoS One 5: e15340.

9. HillersKJ, VilleneuveAM (2003) Chromosome-wide control of meiotic crossing over in C. elegans. Curr Biol 13: 1641–1647.

10. Oliver-BonetM, CampilloM, TurekPJ, KoE, MartinRH (2007) Analysis of replication protein A (RPA) in human spermatogenesis. Mol Human Reprod 13: 837–844.

11. de BoerE, StamP, DietrichAJ, PastinkA, HeytingC (2006) Two levels of interference in mouse meiotic recombination. Proc Natl Acad Sci U S A 103: 9607–9612.

12. StorlazziA, GarganoS, Ruprich-RobertG, FalqueM, DavidM, et al. (2010) Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141: 94–106.

13. ZhangL, KimKP, KlecknerNE, StorlazziA (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. BerchowitzLE, CopenhaverGP (2010) Genetic interference: don't stand so close to me. Curr Genomics 11: 91–102.

15. ColeF, KauppiL, LangeJ, RoigI, WangR, et al. (2012) Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Biol 14: 424–430.

16. MetsDG, MeyerBJ (2009) Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139: 73–86.

17. McPeekS, SpeedTP, MorH (1995) Modeling Interference in Genetic Recombination. Genetics 1044: 1031–1044.

18. FalqueM, AndersonLK, StackSM, GauthierF, MartinOC (2009) Two types of meiotic crossovers coexist in maize. Plant Cell 21: 3915–3925.

19. GauthierF, MartinOC, FalqueM (2011) CODA (crossover distribution analyzer): quantitative characterization of crossover position patterns along chromosomes. BMC Bioinformatics 12: 27.

20. FossE, LandeR, StahlFW, SteinbergCM (1993) Chiasma interference as a function of genetic distance. Genetics 133: 681–691.

21. PanJ, SasakiM, KniewelR, MurakamiH, BlitzblauHG, et al. (2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144: 719–731.

22. ChenSY, TsubouchiT, RockmillB, SandlerJS, RichardsDR, et al. (2008) Global analysis of the meiotic crossover landscape. Dev Cell 15: 401–415.

23. BordeV, LinW, NovikovE, PetriniJH, LichtenM, et al. (2004) Association of Mre11p with double-strand break sites during yeast meiosis. Mol Cell 13: 389–401.

24. GertonJL, DerisiJ, ShroffR, LichtenM, BrownPO, 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. BlatY, ProtacioRU, HunterN, KlecknerN (2002) Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111: 791–802.

26. BuhlerC, BordeV, LichtenM (2007) Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biol 5: e324.

27. KauppiL, BarchiM, LangeJ, BaudatF, JasinM, et al. (2013) Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev 27: 873–886.

28. JoyceEF, McKimKS (2010) Chromosome axis defects induce a checkpoint-mediated delay and interchromosomal effect on crossing over during Drosophila meiosis. PLoS Genet 6: e1001059.

29. JoyceEF, McKimKS (2011) Meiotic checkpoints and the interchromosomal effect on crossing over in Drosophila females. Fly (Austin) 5: 134–140.

30. HigginsJD, PerryRM, BarakateA, RamsayL, WaughR, 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. FungJC, RockmillB, OdellM, RoederGS (2004) Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116: 795–802.

32. MalkovaA, SwansonJ, GermanM, McCuskerJH, HousworthEA, et al. (2004) Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII. Genetics 168: 49–63.

33. CharlesDR (1938) The spatial distribution of cross-overs in X-chromosome tetrads of Drosophila melanogaster. J Genetics 36: 103–126.

34. MehrotraS, McKimKS (2006) Temporal analysis of meiotic DNA double-strand break formation and repair in Drosophila females. PLoS Genet 2: e200.

35. LandeR, StahlFW (1993) Chiasma interference and the distribution of exchanges in Drosophila melanogaster. Cold Spring Harb Symp Quant Biol 58: 543–552.

36. LaurieDA, JonesGH (1981) Inter-individual variation in chiasma distribution in Chorthippus brunneus (Orthoptera: Acrididae). Heredity 47: 409–416.

37. JonesGH (1984) The control of chiasma distribution. Symp Soc Exp Biol 38: 293–320.

38. LhuissierFG, OffenbergHH, WittichPE, VischerNO, HeytingC (2007) The mismatch repair protein MLH1 marks a subset of strongly interfering crossovers in tomato. Plant Cell 19: 862–876.

39. ColomboPC, JonesGH (1997) Chiasma interference is blind to centromeres. Heredity (Edinb) 79(Pt 2): 214–227.

40. SaintenacC, FalqueM, MartinOC, PauxE, FeuilletC, 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. LianJ, YinY, Oliver-BonetM, LiehrT, KoE, et al. (2008) Variation in crossover interference levels on individual chromosomes from human males. Hum Mol Genet 17: 2583–2594.

42. BromanKW, RoweLB, ChurchillGA, PaigenK (2002) Crossover interference in the mouse. Genetics 160: 1123–1131.

43. MartiniE, DiazRL, HunterN, KeeneyS (2006) Crossover homeostasis in yeast meiosis. Cell 126: 285–295.

44. RosuS, LibudaDE, VilleneuveAM (2011) Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science 334: 1286–1289.

45. YokooR, ZawadzkiKA, NabeshimaK, DrakeM, ArurS, et al. (2012) COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149: 75–87.

46. GlobusST, KeeneyS (2012) The joy of six: how to control your crossovers. Cell 149: 11–12.

47. JonesGH, FranklinFC (2006) Meiotic crossing-over: obligation and interference. Cell 126: 246–248.

48. HawleyRS, TheurkaufWE (1993) Requiem for distributive segregation: achiasmate segregation in Drosophila females. Trends Genet 9: 310–317.

49. ArguesoJL, KijasAW, SarinS, HeckJ, WaaseM, 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. ArguesoJL, WanatJ, GemiciZ, AlaniE (2004) Competing crossover pathways act during meiosis in Saccharomyces cerevisiae. Genetics 168: 1805–1816.

51. ZakharyevichK, TangS, MaY, HunterN (2012) Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149: 334–347.

52. ManceraE, BourgonR, BrozziA, HuberW, SteinmetzLM (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454: 479–485.

53. FranklinWS, FossHM (2010) A two-pathway analysis of meiotic crossing over and gene conversion in Saccharomyces cerevisiae. Genetics 186: 515–536.

54. BzymekM, ThayerNH, OhSD, KlecknerN, HunterN (2010) Double holliday junctions are intermediates of DNA break repair. Nature 464: 937–941.

55. KingJS, MortimerRK (1990) A polymerization model of chiasma interference and corresponding computer simulation. Genetics 126: 1127–1138.

56. FujitaniY, MoriS, KobayashiI (2002) A reaction-diffusion model for interference in meiotic crossing over. Genetics 161: 365–372.

57. HanYW, MizuuchiK (2010) Phage Mu transposition immunity: protein pattern formation along DNA by a diffusion-ratchet mechanism. Mol Cell 39: 48–58.

58. VecchiarelliAG, HwangLC, MizuuchiK (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. HultenMA (2011) On the origin of crossover interference: A chromosome oscillatory movement (COM) model. Mol Cytogenet 4: 10.

60. GetzTJ, BanseSA, YoungLS, BanseAV, SwansonJ, et al. (2008) Reduced mismatch repair of heteroduplexes reveals “non”-interfering crossing over in wild-type Saccharomyces cerevisiae. Genetics 178: 1251–1269.

61. StraightAF, Belmont AS, RobinettCC, MurrayAW (1996) GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr Biol 6: 1599–1608.

62. HollingsworthNM, PonteL, HalseyC (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. AgarwalS, RoederGS (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245–255.

64. ChuaPR, RoederGS (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349–359.

65. CherryJM, BallC, WengS, JuvikG, SchmidtR, et al. (1997) Genetic and physical maps of Saccharomyces cerevisiae. Nature 387: 67–73.

66. KoszulR, KlecknerN (2009) Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends Cell Biol 19: 716–724.

67. LoidlJ, KleinF, EngebrechtJ (1998) Genetic and morphological approaches for the analysis of meiotic chromosomes in yeast. Methods Cell Biol 53: 257–285.

68. KimPK, WeinerBM, ZhangL, JordanA, DekkerJ, et al. (2010) Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143: 924–937.

69. QiaoH, LohmillerLD, AndersonLK (2011) Cohesin proteins load sequentially during prophase I in tomato primary microsporocytes. Chromosome Res 19: 193–207.

70. DolezelJ, BartosJ, VoglmayrH, GreilhuberJ (2003) Nuclear DNA content and genome size of trout and human. Cytometry A 51: 127–128.

71. SantosJ, del CerroA, DíezM (1993) Spreading synaptonemal complexes from the grasshopper Chorthippus jacobsi: pachytene and zygotene observations. Hereditas 118: 235–241 Hereditas 118: 235–241.

72. PageSL, HawleyRS (2001) c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev 15: 3130–3143.

73. CarpenterAT (1979) Recombination nodules and synaptonemal complex in recombination-defective females of Drosophila melanogaster. Chromosoma 75: 259–292.

74. PetersonDG, StackSM, PriceJH, JohnstonJS DNA content of heterochromatin and euchromatin in tomato (Lycopersicon esculentum) pachytene chromosomes. Genome 39: 77–82.

75. ShermanJD, StackSM (1995) Two-dimensional spreads of synaptonemal complexes from solanaceous plants. VI. High-resolution recombination nodule map for tomato (Lycopersicon esculentum). Genetics 141: 683–708.

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Genetika Reprodukčná medicína

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