Meiotic recombination hotspots - A comparative view

Plant Journal

Volumn 83, Issue 1, 2015, Pages 52-61

  Choi, Kyuha ^a   Henderson, Ian R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

chromatin; DNA motifs; hotspots; meiosis; recombination

Indexed keywords

CROPS; GENES;

CHROMATIN; DNA MOTIF; HOTSPOTS; MEIOSIS; RECOMBINATION;

DNA;

EUKARYOTA;

SINGLE STRANDED DNA;

CROSSING OVER; DOUBLE STRANDED DNA BREAK; FUNGUS; GENETIC EPIGENESIS; GENETIC PROCEDURES; GENETICS; GENOME; HOMOLOGOUS RECOMBINATION; MEIOSIS; METABOLISM; PLANT;

CROSSING OVER, GENETIC; DNA BREAKS, DOUBLE-STRANDED; DNA, SINGLE-STRANDED; EPIGENESIS, GENETIC; FUNGI; GENETIC TECHNIQUES; GENOME; HOMOLOGOUS RECOMBINATION; MEIOSIS; PLANTS;

EID: 84932193560     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12870     Document Type: Article

References (151)

1. Acquaviva, L., Székvölgyi, L., Dichtl, B., Dichtl, B.S., de La Roche Saint André, C., Nicolas, A., and, Géli, V., (2013) The COMPASS subunit Spp1 links histone methylation to initiation of meiotic recombination. Science, 339, 215-218.
2. Allers, T., and, Lichten, M., (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell, 106, 47-57.
3. Auton, A., Fledel-Alon, A., Pfeifer, S., et al. (2012) A fine-scale chimpanzee genetic map from population sequencing. Science, 336, 193-198.
4. Auton, A., and, McVean, G., (2012) Estimating recombination rates from genetic variation in humans. Methods Mol. Biol. 856, 217-237.
5. Auton, A., and, McVean, G., (2007) Recombination rate estimation in the presence of hotspots. Genome Res. 17, 1219-1227.
6. Auton, A., Rui Li, Y., Kidd, J., et al. (2013) Genetic recombination is targeted towards gene promoter regions in dogs. PLoS Genet. 9, e1003984.
7. Baker, C.L., Walker, M., Kajita, S., Petkov, P.M., and, Paigen, K., (2014) PRDM9 binding organizes hotspot nucleosomes and limits Holliday junction migration. Genome Res. 24, 724-732.
8. Baudat, F., Buard, J., Grey, C., Fledel-Alon, A., Ober, C., Przeworski, M., Coop, G., and, de Massy, B., (2010) PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science, 327, 836-840.
9. Baudat, F., and, de Massy, B., (2007) Cis- and trans-acting elements regulate the mouse Psmb9 meiotic recombination hotspot. PLoS Genet. 3, e100.
10. Baudat, F., and, de Massy, B., (2009) Parallel detection of crossovers and noncrossovers in mouse germ cells. Methods Mol. Biol. 557, 305-322.
11. Baudat, F., and, Nicolas, A., (1997) Clustering of meiotic double-strand breaks on yeast chromosome III. Proc. Natl Acad. Sci. USA, 94, 5213-5218.
12. Berchowitz, L.E., and, Copenhaver, G.P., (2008) Fluorescent Arabidopsis tetrads: a visual assay for quickly developing large crossover and crossover interference data sets. Nat. Protoc. 3, 41-50.
13. Berchowitz, L.E., Francis, K.E., Bey, A.L., and, Copenhaver, G.P., (2007) The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genet. 3, 10.
14. Berchowitz, L.E., Hanlon, S.E., Lieb, J.D., and, Copenhaver, G.P., (2009) A positive but complex association between meiotic double-strand break hotspots and open chromatin in Saccharomyces cerevisiae. Genome Res. 19, 2245-2257.
15. Berg, I.L., Neumann, R., Lam, K.-W.G., Sarbajna, S., Odenthal-Hesse, L., May, C.A., and, Jeffreys, A.J., (2010) PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nat. Genet. 42, 859-863.
16. Berg, I.L., Neumann, R., Sarbajna, S., Odenthal-Hesse, L., Butler, N.J., and, Jeffreys, A.J., (2011) Variants of the protein PRDM9 differentially regulate a set of human meiotic recombination hotspots highly active in African populations. Proc. Natl Acad. Sci. USA, 108, 12378-12383.
17. Bergerat, A., de Massy, B., Gadelle, D., Varoutas, P.C., Nicolas, A., and, Forterre, P., (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature, 386, 414-417.
18. Bishop, D.K., Park, D., Xu, L., and, Kleckner, N., (1992) DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell, 69, 439-456.
19. de Boer, E., Jasin, M., and, Keeney, S., (2013) Analysis of recombinants in female mouse meiosis. Methods Mol. Biol. 957, 19-45.
20. Borde, V., Robine, N., Lin, W., Bonfils, S., Géli, V., and, Nicolas, A., (2009) Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J. 28, 99-111.
21. Brick, K., Smagulova, F., Khil, P., Camerini-Otero, R.D., and, Petukhova, G.V., (2012) Genetic recombination is directed away from functional genomic elements in mice. Nature, 485, 642-645.
22. Brown, J., and, Sundaresan, V., (1991) A recombination hotspot in the maize A1 intragenic region. Theor. Appl. Genet. 81, 185-188.
23. Buhler, C., Borde, V., and, Lichten, M., (2007) Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biol. 5, e324.
24. Buhler, C., Shroff, R., and, Lichten, M., (2009) Genome-wide mapping of meiotic DNA double-strand breaks in Saccharomyces cerevisiae. Methods Mol. Biol. 557, 143-164.
25. Campbell, C.L., Furlotte, N.A., Eriksson, N., Hinds, D., and, Auton, A., (2015) Escape from crossover interference increases with maternal age. Nat. Commun. 6, 6260.
26. Charlesworth, B., and, Charlesworth, D., (2010) Elements of Evolutionary Genetics. Colorado: Roberts and Company Publishers.
27. Chelysheva, L., Grandont, L., Vrielynck, N., le Guin, S., Mercier, R., and, Grelon, M., (2010) An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: immunodetection of cohesins, histones and MLH1. Cytogenet. Genome Res. 129, 143-153.
28. Chelysheva, L., Vezon, D., Chambon, A., et al. (2012) The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS Genet. 8, e1002799.
29. Chen, C., Zhang, W., Timofejeva, L., Gerardin, Y., and, Ma, H., (2005) The Arabidopsis ROCK-N-ROLLERS gene encodes a homolog of the yeast ATP-dependent DNA helicase MER3 and is required for normal meiotic crossover formation. Plant J. 43, 321-334.
30. Choi, K., Kim, S., Kim, S.Y., et al. (2005) SUPPRESSOR OF FRIGIDA3 encodes a nuclear ACTIN-RELATED PROTEIN6 required for floral repression in Arabidopsis. Plant Cell, 17, 2647-2660.
31. Choi, K., Zhao, X., Kelly, K.A., et al. (2013) Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters. Nat. Genet. 45, 1327-1336.
32. Choulet, F., Alberti, A., Theil, S., et al. (2014) Structural and functional partitioning of bread wheat chromosome 3B. Science 345, 1249721.
33. Cole, F., Baudat, F., Grey, C., Keeney, S., de Massy, B., and, Jasin, M., (2014) Mouse tetrad analysis provides insights into recombination mechanisms and hotspot evolutionary dynamics. Nat. Genet. 46, 1072-1080.
34. Cole, F., and, Jasin, M., (2011) DNA Recombination. (, Tsubouchi, H., ed.). Totowa, NJ: Humana Press.
35. Cole, F., Keeney, S., and, Jasin, M., (2010) Comprehensive, fine-scale dissection of homologous recombination outcomes at a hot spot in mouse meiosis. Mol. Cell, 39, 700-710.
36. Coleman-Derr, D., and, Zilberman, D., (2012) Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLoS Genet. 8, e1002988.
37. Colomé-Tatché, M., Cortijo, S., Wardenaar, R., et al. (2012) Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. Proc. Natl Acad. Sci. USA, 109, 16240-16245.
38. Copenhaver, G.P., Browne, W.E., and, Preuss, D., (1998) Assaying genome-wide recombination and centromere functions with Arabidopsis tetrads. Proc. Natl Acad. Sci. USA, 95, 247-252.
39. Copenhaver, G.P., Nickel, K., Kuromori, T., et al. (1999) Genetic definition and sequence analysis of Arabidopsis centromeres. Science, 286, 2468-2474.
40. Crawford, D.C., Bhangale, T., Li, N., Hellenthal, G., Rieder, M.J., Nickerson, D.A., and, Stephens, M., (2004) Evidence for substantial fine-scale variation in recombination rates across the human genome. Nat. Genet. 36, 700-706.
41. Crismani, W., Girard, C., Froger, N., Pradillo, M., Santos, J.L., Chelysheva, L., Copenhaver, G.P., Horlow, C., and, Mercier, R., (2012) FANCM limits meiotic crossovers. Science, 336, 1588-1590.
42. Cromie, G.A., Hyppa, R.W., Cam, H.P., Farah, J.A., Grewal, S.I.S., and, Smith, G.R., (2007) A discrete class of intergenic DNA dictates meiotic DNA break hotspots in fission yeast. PLoS Genet. 3, e141.
43. Deal, R.B., and, Henikoff, S., (2011) Histone variants and modifications in plant gene regulation. Curr. Opin. Plant Biol. 14, 116-122.
44. Dooner, H.K., (1986) Genetic fine structure of the BRONZE locus in maize. Genetics, 113, 1021-1036.
45. Drouaud, J., Khademian, H., Giraut, L., Zanni, V., Bellalou, S., Henderson, I.R., Falque, M., and, Mézard, C., (2013) Contrasted patterns of crossover and non-crossover at Arabidopsis thaliana meiotic recombination hotspots. PLoS Genet. 9, e1003922.
46. Drouaud, J., and, Mézard, C., (2011) Characterization of meiotic crossovers in pollen from Arabidopsis thaliana. Methods Mol. Biol. 745, 223-249.
47. Fearnhead, P., (2006) SequenceLDhot: detecting recombination hotspots. Bioinformatics, 22, 3061-3066.
48. Ferdous, M., Higgins, J.D., Osman, K., et al. (2012) Inter-homolog crossing-over and synapsis in Arabidopsis meiosis are dependent on the chromosome axis protein AtASY3. PLoS Genet. 8, e1002507.
49. Fowler, K.R., Sasaki, M., Milman, N., Keeney, S., and, Smith, G.R., (2014) Evolutionarily diverse determinants of meiotic DNA break and recombination landscapes across the genome. Genome Res. 24, 1650-1664.
50. Francis, K.E., Lam, S.Y., and, Copenhaver, G.P., (2006) Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiol. 142, 1004-1013.
51. Francis, K.E., Lam, S.Y., Harrison, B.D., Bey, A.L., Berchowitz, L.E., and, Copenhaver, G.P., (2007) Pollen tetrad-based visual assay for meiotic recombination in Arabidopsis. Proc. Natl Acad. Sci. USA, 104, 3913-3918.
52. Fu, H., Park, W., Yan, X., Zheng, Z., Shen, B., and, Dooner, H.K., (2001) The highly recombinogenic bz locus lies in an unusually gene-rich region of the maize genome. Proc. Natl Acad. Sci. USA, 98, 8903-8908.
53. Fu, H., Zheng, Z., and, Dooner, H.K., (2002) Recombination rates between adjacent genic and retrotransposon regions in maize vary by two orders of magnitude. Proc. Natl Acad. Sci. USA, 99, 1082-1087.
54. Garcia, V., Bruchet, H., Camescasse, D., Granier, F., Bouchez, D., and, Tissier, A., (2003) AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell, 15, 119-132.
55. Garcia, V., Gray, S., Allison, R.M., Cooper, T.J., and, Neale, M.J., (2015) Tel1(ATM)-mediated interference suppresses clustered meiotic double-strand-break formation. Nature, 520, 114-118.
56. Garcia, V., Phelps, S.E.L., Gray, S., and, Neale, M.J., (2011) Bidirectional resection of DNA double-strand breaks by Mre11 and Exo1. Nature, 479, 241-244.
57. Girard, C., Crismani, W., Froger, N., Mazel, J., Lemhemdi, A., Horlow, C., and, Mercier, R., (2014) FANCM-associated proteins MHF1 and MHF2, but not the other Fanconi anemia factors, limit meiotic crossovers. Nucleic Acids Res. 42, 9087-9095.
58. Giraut, L., Falque, M., Drouaud, J., Pereira, L., Martin, O.C., and, Mézard, C., (2011) Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLoS Genet. 7, e1002354.
59. Gore, M.A., Chia, J.-M., Elshire, R.J., et al. (2009) A first-generation haplotype map of maize. Science, 326, 1115-1117.
60. Grey, C., Barthès, P., Chauveau-Le Friec, G., Langa, F., Baudat, F., and, de Massy, B., (2011) Mouse PRDM9 DNA-binding specificity determines sites of histone H3 lysine 4 trimethylation for initiation of meiotic recombination. PLoS Biol. 9, e1001176.
61. He, Y., Sidhu, G., and, Pawlowski, W.P., (2013) Chromatin immunoprecipitation for studying chromosomal localization of meiotic proteins in maize. Methods Mol. Biol. 990, 191-201.
62. Hellsten, U., Wright, K.M., Jenkins, J., Shu, S., Yuan, Y., Wessler, S.R., Schmutz, J., Willis, J.H., and, Rokhsar, D.S., (2013) Fine-scale variation in meiotic recombination in Mimulus inferred from population shotgun sequencing. Proc. Natl Acad. Sci. USA, 110, 19478-19482.
63. Higgins, J.D., Armstrong, S.J., Franklin, F.C.H., and, Jones, G.H., (2004) The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev. 18, 2557-2570.
64. Higgins, J.D., Buckling, E.F., Franklin, F.C.H., and, Jones, G.H., (2008a) Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. Plant J. 54, 152-162.
65. Higgins, J.D., Vignard, J., Mercier, R., Pugh, A.G., Franklin, F.C.H., and, Jones, G.H., (2008b) AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. Plant J. 55, 28-39.
66. Hinch, A.G., Tandon, A., Patterson, N., et al. (2011) The landscape of recombination in African Americans. Nature, 476, 170-175.
67. Hou, Y., Fan, W., Yan, L., et al. (2013) Genome analyses of single human oocytes. Cell, 155, 1492-1506.
68. Hudson, R.R., and, Kaplan, N.L., (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics, 111, 147-164.
69. Hunt Morgan, T., (1916) A Critique of the Theory of Evolution. Princeton: Princeton University Press.
70. Hyppa, R.W., and, Smith, G.R., (2010) Crossover invariance determined by partner choice for meiotic DNA break repair. Cell, 142, 243-255.
71. Ines, O.Da., Degroote, F., Goubely, C., Amiard, S., Gallego, M.E., and, White, C.I., (2013) Meiotic recombination in Arabidopsis is catalysed by DMC1, with RAD51 playing a supporting role. F. C. H. Franklin, ed. PLoS Genet. 9, e1003787.
72. Iyer, V., and, Struhl, K., (1995) Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure. EMBO J. 14, 2570-2579.
73. Jeffreys, A.J., Kauppi, L., and, Neumann, R., (2001) Intensely punctate meiotic recombination in the class II region of the major histocompatibility complex. Nat. Genet. 29, 217-222.
74. Joshi, N., Brown, M.S., Bishop, D.K., and, Börner, G.V., (2015) Gradual implementation of the meiotic recombination program via checkpoint pathways controlled by global DSB Levels. Mol. Cell, 57, 797-811.
75. Kauppi, L., Jeffreys, A.J., and, Keeney, S., (2004) Where the crossovers are: recombination distributions in mammals. Nat. Rev. Genet. 5, 413-424.
76. Kauppi, L., May, C.A., and, Jeffreys, A.J., (2009) Meiosis. (, Keeney, S., ed.). Totowa, NJ: Humana Press.
77. Keeney, S., Giroux, C.N., and, Kleckner, N., (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell, 88, 375-384.
78. Khil, P.P., and, Camerini-Otero, R.D., (2010) Genetic crossovers are predicted accurately by the computed human recombination map. PLoS Genet. 6, e1000831.
79. Khil, P.P., Smagulova, F., Brick, K.M., Camerini-Otero, R.D., and, Petukhova, G.V., (2012) Sensitive mapping of recombination hotspots using sequencing-based detection of ssDNA. Genome Res. 22, 957-965.
80. Kleckner, N., Zickler, D., Jones, G.H., Dekker, J., Padmore, R., Henle, J., and, Hutchinson, J., (2004) A mechanical basis for chromosome function. Proc. Natl Acad. Sci. USA, 101, 12592-12597.
81. Knoll, A., Higgins, J.D., Seeliger, K., Reha, S.J., Dangel, N.J., Bauknecht, M., Schröpfer, S., Franklin, F.C.H., and, Puchta, H., (2012) The Fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic cells in Arabidopsis. Plant Cell, 24, 1448-1464.
82. Kurzbauer, M.-T., Uanschou, C., Chen, D., and, Schlögelhofer, P., (2012) The recombinases DMC1 and RAD51 are functionally and spatially separated during meiosis in Arabidopsis. Plant Cell, 24, 2058-2070.
83. Lam, I., and, Keeney, S., (2014) Mechanism and regulation of meiotic recombination initiation. Cold Spring Harb. Perspect. Biol. 7, a016634.
84. Lange, J., Pan, J., Cole, F., Thelen, M.P., Jasin, M., and, Keeney, S., (2011) ATM controls meiotic double-strand-break formation. Nature, 479, 237-240.
85. Lenormand, T., and, Dutheil, J., (2005) Recombination difference between sexes: a role for haploid selection. PLoS Biol. 3, e63.
86. Li, X., Li, L., and, Yan, J., (2015) Dissecting meiotic recombination based on tetrad analysis by single-microspore sequencing in maize. Nat. Commun. 6, 6648.
87. Lichten, M., (2014) Tetrad, random spore, and molecular analysis of meiotic segregation and recombination. Methods Mol. Biol. 1205, 13-28.
88. Lichten, M., and, Goldman, A.S., (1995) Meiotic recombination hotspots. Annu. Rev. Genet. 29, 423-444.
89. Liu, S., Yeh, C.-T., Ji, T., Ying, K., Wu, H., Tang, H.M., Fu, Y., Nettleton, D., and, Schnable, P.S., (2009) Mu transposon insertion sites and meiotic recombination events co-localize with epigenetic marks for open chromatin across the maize genome. PLoS Genet. 5, 13.
90. Lu, S., Zong, C., Fan, W., et al. (2012) Probing meiotic recombination and aneuploidy of single sperm cells by whole-genome sequencing. Science, 338, 1627-1630.
91. Lynn, A., Soucek, R., and, Börner, G.V., (2007) ZMM proteins during meiosis: crossover artists at work. Chromosome Res. 15, 591-605.
92. Macaisne, N., Novatchkova, M., Peirera, L., Vezon, D., Jolivet, S., Froger, N., Chelysheva, L., Grelon, M., and, Mercier, R., (2008) SHOC1, an XPF endonuclease-related protein, is essential for the formation of class I meiotic crossovers. Curr. Biol. 18, 1432-1437.
93. Martini, E., Borde, V., Legendre, M., Audic, S., Regnault, B., Soubigou, G., Dujon, B., and, Llorente, B., (2011) Genome-wide analysis of heteroduplex DNA in mismatch repair-deficient yeast cells reveals novel properties of meiotic recombination pathways. PLoS Genet. 7, e1002305.
94. de Massy, B., (2013) Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu. Rev. Genet. 47, 563-599.
95. Mayer, K.F.X., Waugh, R., Brown, J.W.S., et al. (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature, 491, 711-716.
96. McMahill, M.S., Sham, C.W., and, Bishop, D.K., (2007) Synthesis-dependent strand annealing in meiosis. PLoS Biol. 5, e299.
97. McVean, G.A.T., Myers, S.R., Hunt, S., Deloukas, P., Bentley, D.R., and, Donnelly, P., (2004) The fine-scale structure of recombination rate variation in the human genome. Science, 304, 581-584.
98. Melamed-Bessudo, C., and, Levy, A.A., (2012) Deficiency in DNA methylation increases meiotic crossover rates in euchromatic but not in heterochromatic regions in Arabidopsis. Proc. Natl Acad. Sci. USA, 109, E981-E988.
99. Mercier, R., Jolivet, S., Vezon, D., et al. (2005) Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3, whereas the other one is not. Curr. Biol. 15, 692-701.
100. Mercier, R., Mézard, C., Jenczewski, E., Macaisne, N., and, Grelon, M., (2014) The Molecular biology of meiosis in plants. Annu. Rev. Plant Biol. 66, 297-327.
101. Mihola, O., Trachtulec, Z., Vlcek, C., Schimenti, J.C., and, Forejt, J., (2009) A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science, 323, 373-375.
102. Mirouze, M., Lieberman-Lazarovich, M., Aversano, R., Bucher, E., Nicolet, J., Reinders, J., and, Paszkowski, J., (2012) Loss of DNA methylation affects the recombination landscape in Arabidopsis. Proc. Natl Acad. Sci. USA, 109, 5880-5885.
103. Myers, S., Bottolo, L., Freeman, C., McVean, G., and, Donnelly, P., (2005) A fine-scale map of recombination rates and hotspots across the human genome. Science, 310, 321-324.
104. Myers, S., Bowden, R., Tumian, A., Bontrop, R.E., Freeman, C., MacFie, T.S., McVean, G., and, Donnelly, P., (2010) Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science, 327, 876-879.
105. Myers, S., Freeman, C., Auton, A., Donnelly, P., and, McVean, G., (2008) A common sequence motif associated with recombination hot spots and genome instability in humans. Nat. Genet. 40, 1124-1129.
106. Neale, M.J., Pan, J., and, Keeney, S., (2005) Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature, 436, 1053-1057.
107. Nicolas, A., Treco, D., Schultes, N.P., and, Szostak, J.W., (1989) An initiation site for meiotic gene conversion in the yeast Saccharomyces cerevisiae. Nature, 338, 35-39.
108. Oliver, P.L., Goodstadt, L., Bayes, J.J., et al. (2009) Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet. 5, e1000753.
109. Page, S.L., and, Hawley, R.S., (2003) Chromosome choreography: the meiotic ballet. Science, 301, 785-789.
110. Pan, J., Sasaki, M., Kniewel, R., et al. (2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell, 144, 719-731.
111. Panizza, S., Mendoza, M.A., Berlinger, M., Huang, L., Nicolas, A., Shirahige, K., and, Klein, F., (2011) Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell, 146, 372-383.
112. Parvanov, E.D., Petkov, P.M., and, Paigen, K., (2010) Prdm9 controls activation of mammalian recombination hotspots. Science, 327, 835.
113. Patterson, G.I., Kubo, K.M., Shroyer, T., and, Chandler, V.L., (1995) Sequences required for paramutation of the maize b gene map to a region containing the promoter and upstream sequences. Genetics, 140, 1389-1406.
114. Pratto, F., Brick, K., Khil, P., Smagulova, F., Petukhova, G.V., and, Camerini-Otero, R.D., (2014) Recombination initiation maps of individual human genomes. Science, 346, 1256442.
115. Qi, J., Chen, Y., Copenhaver, G.P., and, Ma, H., (2014) Detection of genomic variations and DNA polymorphisms and impact on analysis of meiotic recombination and genetic mapping. Proc. Natl Acad. Sci. USA, 111, 10007-10012.
116. Qiao, H., Prasada Rao, H.B.D., Yang, Y., et al. (2014) Antagonistic roles of ubiquitin ligase HEI10 and SUMO ligase RNF212 regulate meiotic recombination. Nat. Genet. 46, 194-199.
117. Qin, J., Richardson, L.L., Jasin, M., Handel, M.A., and, Arnheim, N., (2004) Mouse strains with an active H2-Ea meiotic recombination hot spot exhibit increased levels of H2-Ea-specific DNA breaks in testicular germ cells. Mol. Cell. Biol. 24, 1655-1666.
118. Qin, Y., Zhao, L., Skaggs, M.I., et al. (2014) ACTIN-RELATED PROTEIN6 regulates female meiosis by modulating meiotic gene expression in Arabidopsis. Plant Cell, 26, 1612-1628.
119. Reynolds, A., Qiao, H., Yang, Y., et al. (2013) RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat. Genet. 45, 269-278.
120. Rodgers-Melnick, E., Bradbury, P.J., Elshire, R.J., Glaubitz, J.C., Acharya, C.B., Mitchell, S.E., Li, C., Li, Y., and, Buckler, E.S., (2015) Recombination in diverse maize is stable, predictable, and associated with genetic load. Proc. Natl Acad. Sci. USA, 112, 3823-3828.
121. Roitinger, E., Hofer, M., Köcher, T., Pichler, P., Novatchkova, M., Yang, J., Schlögelhofer, P., and, Mechtler, K., (2015) Quantitative phosphoproteomics of the ataxia telangiectasia-mutated (ATM) and ataxia telangiectasia-mutated and Rad3-related (ATR) dependent DNA damage response in Arabidopsis thaliana. Mol. Cell Proteomics, 14, 556-571.
122. Rowan, B.A., Patel, V., Weigel, D., and, Schneeberger, K., (2015) Rapid and inexpensive whole-genome genotyping-by-sequencing for crossover localization and fine-scale genetic mapping. G3: Genes-Genomes-Genetics, 5, 385-398.
123. Saintenac, C., Falque, M., Martin, O.C., Paux, E., Feuillet, C., and, Sourdille, P., (2009) Detailed recombination studies along chromosome 3B provide new insights on crossover distribution in wheat (Triticum aestivum L.). Genetics, 181, 393-403.
124. Salomé, P.A., Bomblies, K., Fitz, J., Laitinen, R.A.E., Warthmann, N., Yant, L., and, Weigel, D., (2012) The recombination landscape in Arabidopsis thaliana F2 populations. Heredity (Edinb), 108, 447-455.
125. Schwacha, A., and, Kleckner, N., (1995) Identification of double Holliday junctions as intermediates in meiotic recombination. Cell, 83, 783-791.
126. Segal, E., and, Widom, J., (2009) Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr. Opin. Struct. Biol. 19, 65-71.
127. Séguéla-Arnaud, M., Crismani, W., Larchevêque, C., et al. (2015) Multiple mechanisms limit meiotic crossovers: TOP3α and two BLM homologs antagonize crossovers in parallel to FANCM. Proc. Natl Acad. Sci. USA 112, 4713-4718.
128. Serrentino, M.-E., Chaplais, E., Sommermeyer, V., and, Borde, V., (2013) Differential association of the conserved SUMO ligase Zip3 with meiotic double-strand break sites reveals regional variations in the outcome of meiotic recombination. PLoS Genet. 9, e1003416.
129. Shinohara, A., Ogawa, H., and, Ogawa, T., (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell, 69, 457-470.
130. Smagulova, F., Gregoretti, I.V., Brick, K., Khil, P., Camerini-Otero, R.D., and, Petukhova, G.V., (2011) Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature, 472, 375-378.
131. Sommermeyer, V., Béneut, C., Chaplais, E., Serrentino, M.E., and, Borde, V., (2013) Spp1, a member of the Set1 complex, promotes meiotic DSB formation in promoters by tethering histone H3K4 methylation sites to chromosome axes. Mol. Cell, 49, 43-54.
132. Sun, H., Treco, D., and, Szostak, J.W., (1991) Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site. Cell, 64, 1155-1161.
133. Sun, Y., Ambrose, J.H., Haughey, B.S., et al. (2012) Deep genome-wide measurement of meiotic gene conversion using tetrad analysis in Arabidopsis thaliana. PLoS Genet. 8, e1002968.
134. Szostak, J.W., Orr-Weaver, T.L., Rothstein, R.J., and, Stahl, F.W., (1983) The double-strand-break repair model for recombination. Cell, 33, 25-35.
135. Thacker, D., Lam, I., Knop, M., and, Keeney, S., (2011) Exploiting spore-autonomous fluorescent protein expression to quantify meiotic chromosome behaviors in Saccharomyces cerevisiae. Genetics, 189, 423-439.
136. The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 485, 635-641.
137. Tiemann-Boege, I., Calabrese, P., Cochran, D.M., Sokol, R., and, Arnheim, N., (2006) High-resolution recombination patterns in a region of human chromosome 21 measured by sperm typing. PLoS Genet. 2, e70.
138. Tischfield, S.E., and, Keeney, S., (2012) Scale matters: the spatial correlation of yeast meiotic DNA breaks with histone H3 trimethylation is driven largely by independent colocalization at promoters. Cell Cycle, 11, 1496-1503.
139. Uanschou, C., Siwiec, T., Pedrosa-Harand, A., et al. (2007) A novel plant gene essential for meiosis is related to the human CtIP and the yeast COM1/SAE2 gene. EMBO J. 26, 5061-5070.
140. Venters, B.J., and, Pugh, B.F., (2009) How eukaryotic genes are transcribed. Crit. Rev. Biochem. Mol. Biol. 44, 117-141.
141. Villeneuve, A.M., and, Hillers, K.J., (2001) Whence meiosis? Cell, 106, 647-650.
142. Wei, F., Zhang, J., Zhou, S., et al. (2009) The physical and genetic framework of the maize B73 genome. PLoS Genet. 5, 9.
143. Wijeratne, A.J., Chen, C., Zhang, W., Timofejeva, L., and, Ma, H., (2006) The Arabidopsis thaliana PARTING DANCERS gene encoding a novel protein is required for normal meiotic homologous recombination. Mol. Biol. Cell, 17, 1331-1343.
144. Wijnker, E., Velikkakam James, G., Ding, J., et al. (2013) The genomic landscape of meiotic crossovers and gene conversions in Arabidopsis thaliana. Elife, 2, e01426.
145. Wu, T.C., and, Lichten, M., (1994) Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science, 263, 515-518.
146. Xu, X., Hsia, A.P., Zhang, L., Nikolau, B.J., and, Schnable, P.S., (1995) Meiotic recombination break points resolve at high rates at the 5′ end of a maize coding sequence. Plant Cell, 7, 2151-2161.
147. Yao, H., and, Schnable, P.S., (2005) Cis-effects on meiotic recombination across distinct a1-sh2 intervals in a common Zea genetic background. Genetics, 170, 1929-1944.
148. Yelina, N.E., Choi, K., Chelysheva, L., et al. (2012) Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLoS Genet. 8, e1002844.
149. Yelina, N.E., Ziolkowski, P.A., Miller, N., Zhao, X., Kelly, K.A., Muñoz, D.F., Mann, D.J., Copenhaver, G.P., and, Henderson, I.R., (2013) High-throughput analysis of meiotic crossover frequency and interference via flow cytometry of fluorescent pollen in Arabidopsis thaliana. Nat. Protoc. 8, 2119-2134.
150. Young, J.A., Schreckhise, R.W., Steiner, W.W., and, Smith, G.R., (2002) Meiotic recombination remote from prominent DNA break sites in S. pombe. Mol. Cell, 9, 253-263.
151. Zhang, X., Bernatavichute, Y.V., Cokus, S., Pellegrini, M., and, Jacobsen, S.E., (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 10, R62.