Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants.
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 d...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2012-01-01
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| Series: | PLoS Genetics |
| Online Access: | http://europepmc.org/articles/PMC3410864?pdf=render |
| _version_ | 1817976701771055104 |
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| author | Nataliya E Yelina Kyuha Choi Liudmila Chelysheva Malcolm Macaulay Bastiaan de Snoo Erik Wijnker Nigel Miller Jan Drouaud Mathilde Grelon Gregory P Copenhaver Christine Mezard Krystyna A Kelly Ian R Henderson |
| author_facet | Nataliya E Yelina Kyuha Choi Liudmila Chelysheva Malcolm Macaulay Bastiaan de Snoo Erik Wijnker Nigel Miller Jan Drouaud Mathilde Grelon Gregory P Copenhaver Christine Mezard Krystyna A Kelly Ian R Henderson |
| author_sort | Nataliya E Yelina |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-13T22:07:03Z |
| format | Article |
| id | doaj.art-38dfaa15370d407fb5e13f482b10a0f6 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-04-13T22:07:03Z |
| publishDate | 2012-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-38dfaa15370d407fb5e13f482b10a0f62022-12-22T02:27:54ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042012-01-0188e100284410.1371/journal.pgen.1002844Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants.Nataliya E YelinaKyuha ChoiLiudmila ChelyshevaMalcolm MacaulayBastiaan de SnooErik WijnkerNigel MillerJan DrouaudMathilde GrelonGregory P CopenhaverChristine MezardKrystyna A KellyIan R HendersonMeiosis 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.http://europepmc.org/articles/PMC3410864?pdf=render |
| spellingShingle | Nataliya E Yelina Kyuha Choi Liudmila Chelysheva Malcolm Macaulay Bastiaan de Snoo Erik Wijnker Nigel Miller Jan Drouaud Mathilde Grelon Gregory P Copenhaver Christine Mezard Krystyna A Kelly Ian R Henderson Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLoS Genetics |
| title | Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. |
| title_full | Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. |
| title_fullStr | Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. |
| title_full_unstemmed | Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. |
| title_short | Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. |
| title_sort | epigenetic remodeling of meiotic crossover frequency in arabidopsis thaliana dna methyltransferase mutants |
| url | http://europepmc.org/articles/PMC3410864?pdf=render |
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