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Nataliya E. Yelina1#, Kyuha Choi1#, Liudmila Chelysheva2, Malcolm Macaulay3, Bastiaan de Snoo4, Erik Wijnker5, Nigel Miller6, Jan Drouaud2, Mathilde Grelon2, Gregory P. Copenhaver7,8, Christine Mezard2, Krystyna A. Kelly1, Ian R. Henderson1*
1Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom, 2Institut Jean-Pierre Bourgin, INRA Centre de Versailles-Grignon, Versailles, France, 3The James Hutton Institute, Invergowrie, Dundee, United Kingdom, 4Rijk Zwaan Breeding, De Lier, The Netherlands, 5Wageningen University, Wageningen, The Netherlands, 6Department of Pathology, University of Cambridge, Cambridge, United Kingdom, 7Department of Biology and The Carolina Center for Genome Sciences, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America, 8Lineberger Comprehensive Cancer Center, The University of North Carolina School of Medicine, Chapel Hill, North Carolina, United States of America
#These authors contributed equally to this work.
*Corresponding author.
Abstract
Meiosis is a specialized eukaryotic cell division that generates haploid gametes required for sexual reproduction. During meiosis, homologous chromosomes pair and undergo reciprocal genetic exchange, termed crossover (CO). Meiotic CO frequency varies along the physical length of chromosomes and is determined by hierarchical mechanisms, including epigenetic organization, for example methylation of the DNA and histones. Here we investigate the role of DNA methylation in determining patterns of CO frequency along Arabidopsis thaliana chromosomes. In A. thaliana the pericentromeric regions are repetitive, densely DNA methylated, and suppressed for both RNA polymerase-II transcription and CO frequency. DNA hypomethylated methyltransferase1 (met1) mutants show transcriptional reactivation of repetitive sequences in the pericentromeres, which we demonstrate is coupled to extensive remodeling of CO frequency. We observe elevated centromere-proximal COs in met1, coincident with pericentromeric decreases and distal increases. Importantly, total numbers of CO events are similar between wild type and met1, suggesting a role for interference and homeostasis in CO remodeling. To understand recombination distributions at a finer scale we generated CO frequency maps close to the telomere of chromosome 3 in wild type and demonstrate an elevated recombination topology in met1. Using a pollen-typing strategy we have identified an intergenic nucleosome-free CO hotspot 3a, and we demonstrate that it undergoes increased recombination activity in met1. We hypothesize that modulation of 3a activity is caused by CO remodeling driven by elevated centromeric COs. These data demonstrate how regional epigenetic organization can pattern recombination frequency along eukaryotic chromosomes.
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