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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.

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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.

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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.

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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.

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Correspondence to Ian R Henderson.

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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

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