Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters

Abstract

PRDM9 directs human meiotic crossover hot spots to intergenic sequence motifs, whereas budding yeast hot spots overlap regions of low nucleosome density (LND) in gene promoters. To investigate hot spots in plants, which lack PRDM9, we used coalescent analysis of genetic variation in Arabidopsis thaliana. Crossovers increased toward gene promoters and terminators, and hot spots were associated with active chromatin modifications, including H2A.Z, histone H3 Lys4 trimethylation (H3K4me3), LND and low DNA methylation. Hot spot–enriched A-rich and CTT-repeat DNA motifs occurred upstream and downstream, respectively, of transcriptional start sites. Crossovers were asymmetric around promoters and were most frequent over CTT-repeat motifs and H2A.Z nucleosomes. Pollen typing, segregation and cytogenetic analysis showed decreased numbers of crossovers in the arp6 H2A.Z deposition mutant at multiple scales. During meiosis, H2A.Z forms overlapping chromosomal foci with the DMC1 and RAD51 recombinases. As arp6 reduced the number of DMC1 or RAD51 foci, H2A.Z may promote the formation or processing of meiotic DNA double-strand breaks. We propose that gene chromatin ancestrally designates hot spots within eukaryotes and PRDM9 is a derived state within vertebrates.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Meiotic crossover frequency in the Arabidopsis genome.
Figure 2: Chromatin landscape at hot and cold promoters.
Figure 3: A-rich and CTT-repeat DNA sequence motifs at hot and cold promoters.
Figure 4: The arp6 mutant has decreased crossover frequency at the 3a and 3b hot spots.
Figure 5: The arp6 mutant has decreased crossover frequency at the domain and whole-chromosome scales.
Figure 6: Immunolocalization of H2A.Z and meiotic proteins in wild-type plants and arp6 mutants.

References

  1. Kauppi, L., Jeffreys, A.J. & Keeney, S. Where the crossovers are: recombination distributions in mammals. Nat. Rev. Genet. 5, 413–424 (2004).

    CAS  PubMed  Google Scholar 

  2. McVean, G.A.T. et al. The fine-scale structure of recombination rate variation in the human genome. Science 304, 581–584 (2004).

    CAS  PubMed  Google Scholar 

  3. Pan, J. et al. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144, 719–731 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Baudat, F. et al. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327, 836–840 (2010).

    CAS  PubMed  Google Scholar 

  5. Myers, S. et al. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327, 876–879 (2010).

    CAS  PubMed  Google Scholar 

  6. Berg, I.L. et al. 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 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Berg, I.L. et al. PRDM9 variation strongly influences recombination hot spot activity and meiotic instability in humans. Nat. Genet. 42, 859–863 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Hinch, A.G. et al. The landscape of recombination in African Americans. Nature 476, 170–175 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Kong, A. et al. Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467, 1099–1103 (2010).

    CAS  PubMed  Google Scholar 

  10. Parvanov, E.D., Petkov, P.M. & Paigen, K. Prdm9 controls activation of mammalian recombination hotspots. Science 327, 835 (2010).

    CAS  PubMed  Google Scholar 

  11. Smagulova, F. et al. Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472, 375–378 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Myers, S., Bottolo, L., Freeman, C., McVean, G. & Donnelly, P. A fine-scale map of recombination rates and hotspots across the human genome. Science 310, 321–324 (2005).

    CAS  PubMed  Google Scholar 

  13. Hayashi, K., Yoshida, K. & Matsui, Y. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438, 374–378 (2005).

    CAS  PubMed  Google Scholar 

  14. Grey, C. et al. Mouse PRDM9 DNA-binding specificity determines sites of histone H3 lysine 4 trimethylation for initiation of meiotic recombination. PLoS Biol. 9, e1001176 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Brick, K., Smagulova, F., Khil, P., Camerini-Otero, R.D. & Petukhova, G.V. Genetic recombination is directed away from functional genomic elements in mice. Nature 485, 642–645 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Ohta, K., Shibata, T. & Nicolas, A. Changes in chromatin structure at recombination initiation sites during yeast meiosis. EMBO J. 13, 5754–5763 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Wu, T.C. & Lichten, M. Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science 263, 515–518 (1994).

    CAS  PubMed  Google Scholar 

  18. Fan, Q.Q. & Petes, T.D. Relationship between nuclease-hypersensitive sites and meiotic recombination hot spot activity at the HIS4 locus of Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 2037–2043 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Nicolas, A., Treco, D., Schultes, N.P. & Szostak, J.W. An initiation site for meiotic gene conversion in the yeast Saccharomyces cerevisiae. Nature 338, 35–39 (1989).

    CAS  PubMed  Google Scholar 

  20. Baudat, F. & Nicolas, A. Clustering of meiotic double-strand breaks on yeast chromosome III. Proc. Natl. Acad. Sci. USA 94, 5213–5218 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Berchowitz, L.E., Hanlon, S.E., Lieb, J.D. & Copenhaver, G.P. A positive but complex association between meiotic double-strand break hotspots and open chromatin in Saccharomyces cerevisiae. Genome Res. 19, 2245–2257 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Borde, V. et al. Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J. 28, 99–111 (2009).

    CAS  PubMed  Google Scholar 

  23. Sommermeyer, V., Béneut, C., Chaplais, E., Serrentino, M.E. & Borde, V. 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 (2013).

    CAS  PubMed  Google Scholar 

  24. Sollier, J. et al. Set1 is required for meiotic S-phase onset, double-strand break formation and middle gene expression. EMBO J. 23, 1957–1967 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Acquaviva, L. et al. The COMPASS subunit Spp1 links histone methylation to initiation of meiotic recombination. Science 339, 215–218 (2013).

    CAS  PubMed  Google Scholar 

  26. Tischfield, S.E. & Keeney, S. 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 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Copenhaver, G.P. et al. Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286, 2468–2474 (1999).

    CAS  PubMed  Google Scholar 

  28. Dooner, H.K. Genetic fine structure of the BRONZE locus in maize. Genetics 113, 1021–1036 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Giraut, L. et al. Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLoS Genet. 7, e1002354 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Gore, M.A. et al. A first-generation haplotype map of maize. Science 326, 1115–1117 (2009).

    CAS  PubMed  Google Scholar 

  31. Mayer, K.F.X. et al. A physical, genetic and functional sequence assembly of the barley genome. Nature 491, 711–716 (2012).

    CAS  PubMed  Google Scholar 

  32. Saintenac, C. et al. Detailed recombination studies along chromosome 3B provide new insights on crossover distribution in wheat (Triticum aestivum L.). Genetics 181, 393–403 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Salomé, P.A. et al. The recombination landscape in Arabidopsis thaliana F2 populations. Heredity 108, 447–455 (2012).

    PubMed  Google Scholar 

  34. Cao, J. et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet. 43, 956–963 (2011).

    CAS  PubMed  Google Scholar 

  35. Yelina, N.E. et al. Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLoS Genet. 8, e1002844 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Loudet, O., Chaillou, S., Camilleri, C., Bouchez, D. & Daniel-Vedele, F. Bay-0 × Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in. Arabidopsis. Theor. Appl. Genet. 104, 1173–1184 (2002).

    CAS  PubMed  Google Scholar 

  37. Fransz, P.F. et al. Integrated cytogenetic map of chromosome arm 4S of A. thaliana: structural organization of heterochromatic knob and centromere region. Cell 100, 367–376 (2000).

    Article  CAS  PubMed  Google Scholar 

  38. Horton, M.W. et al. Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nat. Genet. 44, 212–216 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Auton, A. et al. A fine-scale chimpanzee genetic map from population sequencing. Science 336, 193–198 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Fearnhead, P. SequenceLDhot: detecting recombination hotspots. Bioinformatics 22, 3061–3066 (2006).

    CAS  PubMed  Google Scholar 

  41. Drouaud, J. & Mézard, C. Characterization of meiotic crossovers in pollen from Arabidopsis thaliana. Methods Mol. Biol. 745, 223–249 (2011).

    CAS  PubMed  Google Scholar 

  42. Bickel, P.J., Boley, N., Brown, J.B., Huang, H. & Zhang, N.R. Subsampling methods for genomic inference. Ann. Appl. Stat. 4, 1660–1697 (2010).

    Google Scholar 

  43. Venters, B.J. & Pugh, B.F. How eukaryotic genes are transcribed. Crit. Rev. Biochem. Mol. Biol. 44, 117–141 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Zhang, X., Bernatavichute, Y.V., Cokus, S., Pellegrini, M. & Jacobsen, S.E. Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 10, R62 (2009).

    PubMed  PubMed Central  Google Scholar 

  45. Coleman-Derr, D. & Zilberman, D. Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLoS Genet. 8, e1002988 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Deal, R.B. & Henikoff, S. Histone variants and modifications in plant gene regulation. Curr. Opin. Plant Biol. 14, 116–122 (2011).

    CAS  PubMed  Google Scholar 

  47. Zhang, X. et al. Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 5, e129 (2007).

    PubMed  PubMed Central  Google Scholar 

  48. Cokus, S.J. et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215–219 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Maloisel, L. & Rossignol, J.L. Suppression of crossing-over by DNA methylation in Ascobolus. Genes Dev. 12, 1381–1389 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Bailey, T.L. et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202–W208 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Bembom, O., Keles, S. & van der Laan, M.J. Supervised detection of conserved motifs in DNA sequences with cosmo. Stat. Appl. Genet. Mol. Biol. 6, Article8 (2007).

    PubMed  Google Scholar 

  52. Mahony, S., Golden, A., Smith, T.J. & Benos, P.V. Improved detection of DNA motifs using a self-organized clustering of familial binding profiles. Bioinformatics 21 (suppl. 1), i283–i291 (2005).

    CAS  PubMed  Google Scholar 

  53. Pavesi, G., Mauri, G. & Pesole, G. An algorithm for finding signals of unknown length in DNA sequences. Bioinformatics 17 (suppl. 1), S207–S214 (2001).

    PubMed  Google Scholar 

  54. Field, Y. et al. Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLOS Comput. Biol. 4, e1000216 (2008).

    PubMed  PubMed Central  Google Scholar 

  55. Baudat, F. & de Massy, B. Cis- and trans-acting elements regulate the mouse Psmb9 meiotic recombination hotspot. PLoS Genet. 3, e100 (2007).

    PubMed  PubMed Central  Google Scholar 

  56. Cole, F., Keeney, S. & Jasin, M. Comprehensive, fine-scale dissection of homologous recombination outcomes at a hot spot in mouse meiosis. Mol. Cell 39, 700–710 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Jeffreys, A.J. & Neumann, R. Factors influencing recombination frequency and distribution in a human meiotic crossover hotspot. Hum. Mol. Genet. 14, 2277–2287 (2005).

    CAS  PubMed  Google Scholar 

  58. Choi, K. et al. SUPPRESSOR OF FRIGIDA3 encodes a nuclear ACTIN-RELATED PROTEIN6 required for floral repression in Arabidopsis. Plant Cell 17, 2647–2660 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Deal, R.B., Topp, C.N., McKinney, E.C. & Meagher, R.B. Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z. Plant Cell 19, 74–83 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Kumar, S.V. & Wigge, P.A. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140, 136–147 (2010).

    CAS  PubMed  Google Scholar 

  61. Zilberman, D., Coleman-Derr, D., Ballinger, T. & Henikoff, S. Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456, 125–129 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Martin-Trillo, M. et al. EARLY IN SHORT DAYS 1 (ESD1) encodes ACTIN-RELATED PROTEIN 6 (AtARP6), a putative component of chromatin remodelling complexes that positively regulates FLC accumulation in Arabidopsis. Development 133, 1241–1252 (2006).

    CAS  PubMed  Google Scholar 

  63. Francis, K.E. et al. Pollen tetrad-based visual assay for meiotic recombination in Arabidopsis. Proc. Natl. Acad. Sci. USA 104, 3913–3918 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Barth, S., Melchinger, A.E., Devezi-Savula, B. & Lübberstedt, T. A high-throughput system for genome-wide measurement of genetic recombination in Arabidopsis thaliana based on transgenic markers. Funct. Integr. Genomics 1, 200–206 (2000).

    CAS  PubMed  Google Scholar 

  65. Jones, G.H. & Franklin, F.C.H. Meiotic crossing-over: obligation and interference. Cell 126, 246–248 (2006).

    CAS  PubMed  Google Scholar 

  66. Melamed-Bessudo, C., Yehuda, E., Stuitje, A.R. & Levy, A.A. A new seed-based assay for meiotic recombination in Arabidopsis thaliana. Plant J. 43, 458–466 (2005).

    CAS  PubMed  Google Scholar 

  67. Bishop, D.K., Park, D., Xu, L. & Kleckner, N. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69, 439–456 (1992).

    CAS  PubMed  Google Scholar 

  68. Shinohara, A., Ogawa, H. & Ogawa, T. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69, 457–470 (1992).

    CAS  PubMed  Google Scholar 

  69. Sanchez-Moran, E., Santos, J.-L., Jones, G.H. & Franklin, F.C.H. ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev. 21, 2220–2233 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Copenhaver, G.P., Browne, W.E. & Preuss, D. Assaying genome-wide recombination and centromere functions with Arabidopsis tetrads. Proc. Natl. Acad. Sci. USA 95, 247–252 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Sanchez-Moran, E., Armstrong, S.J., Santos, J.L., Franklin, F.C.H. & Jones, G.H. Variation in chiasma frequency among eight accessions of Arabidopsis thaliana. Genetics 162, 1415–1422 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Francis, R.A. et al. Characterizing the performance of the Conway-Maxwell Poisson generalized linear model. Risk Anal. 32, 167–183 (2012).

    PubMed  Google Scholar 

  73. Jackson, N. et al. Reduced meiotic crossovers and delayed prophase I progression in AtMLH3-deficient Arabidopsis. EMBO J. 25, 1315–1323 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Blat, Y., Protacio, R.U., Hunter, N. & Kleckner, N. Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111, 791–802 (2002).

    CAS  PubMed  Google Scholar 

  75. Panizza, S. et al. Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 146, 372–383 (2011).

    CAS  PubMed  Google Scholar 

  76. Gerton, J.L. et al. Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 97, 11383–11390 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Morillo-Huesca, M., Clemente-Ruiz, M., Andújar, E. & Prado, F. The SWR1 histone replacement complex causes genetic instability and genome-wide transcription misregulation in the absence of H2A.Z. PLoS ONE 5, e12143 (2010).

    PubMed  PubMed Central  Google Scholar 

  78. Papamichos-Chronakis, M., Watanabe, S., Rando, O.J. & Peterson, C.L. Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity. Cell 144, 200–213 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Iacovoni, J.S. et al. High-resolution profiling of γH2AX around DNA double strand breaks in the mammalian genome. EMBO J. 29, 1446–1457 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Savic, V. et al. Formation of dynamic γ-H2AX domains along broken DNA strands is distinctly regulated by ATM and MDC1 and dependent upon H2AX densities in chromatin. Mol. Cell 34, 298–310 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Meier, A. et al. Spreading of mammalian DNA-damage response factors studied by ChIP-chip at damaged telomeres. EMBO J. 26, 2707–2718 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Kleckner, N. Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex. Chromosoma 115, 175–194 (2006).

    PubMed  Google Scholar 

  83. Oliver, P.L. et al. Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet. 5, e1000753 (2009).

    PubMed  PubMed Central  Google Scholar 

  84. Wu, Y., Close, T.J. & Lonardi, S. On the accurate construction of consensus genetic maps. Comput. Syst. Bioinformatics Conf. 7, 285–296 (2008).

    PubMed  Google Scholar 

  85. Borevitz, J.O. et al. Genome-wide patterns of single-feature polymorphism in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104, 12057–12062 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Clark, R.M. et al. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317, 338–342 (2007).

    CAS  PubMed  Google Scholar 

  87. Benson, G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573–580 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Warburton, P.E., Giordano, J., Cheung, F., Gelfand, Y. & Benson, G. Inverted repeat structure of the human genome: the X-chromosome contains a preponderance of large, highly homologous inverted repeats that contain testes genes. Genome Res. 14, 1861–1869 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Auton, A. & McVean, G. Recombination rate estimation in the presence of hotspots. Genome Res. 17, 1219–1227 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Achim, Z. & Grothendieck, G. zoo: S3 infrastructure for regular and irregular time series. J. Stat. Softw. 14, 1–27 (2005).

    Google Scholar 

  91. Berchowitz, L.E. & Copenhaver, G.P. Fluorescent Arabidopsis tetrads: a visual assay for quickly developing large crossover and crossover interference data sets. Nat. Protoc. 3, 41–50 (2008).

    CAS  PubMed  Google Scholar 

  92. Gan, X. et al. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419–423 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Arends, D., Prins, P., Jansen, R.C. & Broman, K.W. R/qtl: high-throughput multiple QTL mapping. Bioinformatics 26, 2990–2992 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Higgins, J.D., Armstrong, S.J., Franklin, F.C.H. & Jones, G.H. 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 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Ferdous, M. et al. Inter-homolog crossing-over and synapsis in Arabidopsis meiosis are dependent on the chromosome axis protein AtASY3. PLoS Genet. 8, e1002507 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank S. Jacobsen (University of California, Los Angeles) and D. Zilberman (University of California, Berkeley) for chromatin data, D. Weigel (Max Plank Institute for Developmental Biology, Tübingen) for genetic polymorphism data, P. Fearnhead (University of Lancaster, Lancaster) for helpful advice in running SequenceLDhot, P. Wigge (The Sainsbury Laboratory, University of Cambridge) for the HTA11-GFP hta11 hta9 line and for comments and P. Shaw (John Innes Centre, Norwich) for the HTA11-GFP arp6 line. Work in the Henderson laboratory is supported by a Royal Society University Research Fellowship, Gatsby Charitable Foundation Grant 2962, the Isaac Newton Trust and Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/K007882/1. K.C. was supported by an EMBO Long Term Fellowship, EMBO LTF-807,2009. P.A.Z. is supported by grant 605/MOB/2011/0 from the Polish Ministry of Science and Higher Education. G.M. is supported by Wellcome Trust Core Award 090532/Z/09/Z, and O.V. is supported by the Wellcome Trust studentship 086786/Z/08/Z. Work in the Franklin laboratory is supported by the BBSRC. G.P.C. is supported by grant MCB-1121563 from the National Science Foundation. This paper is dedicated to Simon Chan.

Author information

Authors and Affiliations

Authors

Contributions

K.C., J.D.H., N.E.Y. and P.A.Z. performed experiments. K.C., J.D.H., N.E.Y., P.A.Z., G.P.C., F.C.H.F. and I.R.H. designed experiments. X.Z., K.A.K., O.V., T.J.H., G.M. and I.R.H. designed and performed computational and statistical analyses. K.C., X.Z., K.A.K., O.V., J.D.H., N.E.Y., T.J.H., P.A.Z., G.P.C., F.C.H.F., G.M. and I.R.H. wrote the paper.

Corresponding author

Correspondence to Ian R Henderson.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–11, Supplementary Tables 1–24 and Supplementary Note (PDF 44267 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Choi, K., Zhao, X., Kelly, K. et al. Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters. Nat Genet 45, 1327–1336 (2013). https://doi.org/10.1038/ng.2766

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng.2766

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing