Loss of DNA methylation affects the recombination landscape in Arabidopsis
During sexual reproduction, one-half of the genetic material is deposited in gametes, and a complete set of chromosomes is restored upon fertilization. Reduction of the genetic information before gametogenesis occurs in meiosis, when cross-overs (COs) between homologous chromosomes secure an exchang...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2012-04, Vol.109 (15), p.5880-5885 |
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| creator | Mirouze, Marie Lieberman-Lazarovich, Michal Aversano, Riccardo Bucher, Etienne Nicolet, Joël Reinders, Jon Paszkowski, Jerzy |
| description | During sexual reproduction, one-half of the genetic material is deposited in gametes, and a complete set of chromosomes is restored upon fertilization. Reduction of the genetic information before gametogenesis occurs in meiosis, when cross-overs (COs) between homologous chromosomes secure an exchange of their genetic information. COs are not evenly distributed along chromosomes and are suppressed in chromosomal regions encompassing compact, hypermethylated centromeric and pericentromeric DNA. Therefore, it was postulated that DNA hypermethylation is inhibitory to COs. Here, when analyzing meiotic recombination in mutant plants with hypomethylated DNA, we observed unexpected and counterintuitive effects of DNA methylation losses on CO distribution. Recombination was further promoted in the hypomethylated chromosome arms while it was inhibited in heterochromatic regions encompassing pericentromeric DNA. Importantly, the total number of COs was not affected, implying that loss of DNA methylation led to a global redistribution of COs along chromosomes. To determine by which mechanisms altered levels of DNA methylation influence recombination—whether directly in cis or indirectly in trans by changing expression of genes encoding recombination components—we analyzed CO distribution in wild-type lines with randomly scattered and well-mapped hypomethylated chromosomal segments. The results of these experiments, supported by expression profiling data, suggest that DNA methylation affects meiotic recombination in cis. Because DNA methylation exhibits significant variation even within a single species, our results imply that it may influence the evolution of plant genomes through the control of meiotic recombination. |
| doi_str_mv | 10.1073/pnas.1120841109 |
| format | Article |
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Reduction of the genetic information before gametogenesis occurs in meiosis, when cross-overs (COs) between homologous chromosomes secure an exchange of their genetic information. COs are not evenly distributed along chromosomes and are suppressed in chromosomal regions encompassing compact, hypermethylated centromeric and pericentromeric DNA. Therefore, it was postulated that DNA hypermethylation is inhibitory to COs. Here, when analyzing meiotic recombination in mutant plants with hypomethylated DNA, we observed unexpected and counterintuitive effects of DNA methylation losses on CO distribution. Recombination was further promoted in the hypomethylated chromosome arms while it was inhibited in heterochromatic regions encompassing pericentromeric DNA. Importantly, the total number of COs was not affected, implying that loss of DNA methylation led to a global redistribution of COs along chromosomes. To determine by which mechanisms altered levels of DNA methylation influence recombination—whether directly in cis or indirectly in trans by changing expression of genes encoding recombination components—we analyzed CO distribution in wild-type lines with randomly scattered and well-mapped hypomethylated chromosomal segments. The results of these experiments, supported by expression profiling data, suggest that DNA methylation affects meiotic recombination in cis. Because DNA methylation exhibits significant variation even within a single species, our results imply that it may influence the evolution of plant genomes through the control of meiotic recombination.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1120841109</identifier><identifier>PMID: 22451936</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Arabidopsis ; Arabidopsis - cytology ; Arabidopsis - genetics ; Arabidopsis Proteins ; Arabidopsis Proteins - genetics ; Biological Sciences ; Chromatin ; Chromosomes ; Chromosomes, Plant ; Chromosomes, Plant - genetics ; cytology ; DNA ; DNA (Cytosine-5-)-Methyltransferases ; DNA (Cytosine-5-)-Methyltransferases - genetics ; DNA methylation ; DNA Methylation - genetics ; Epigenetics ; Euchromatin ; Euchromatin - metabolism ; evolution ; Flowers & plants ; gametogenesis ; Gene expression ; Genes ; Genetic mutation ; genetics ; Genomes ; germ cells ; Heterochromatin ; Heterochromatin - metabolism ; Histones ; Inbreeding ; meiosis ; Meiosis - genetics ; metabolism ; Methylation ; mutants ; Mutation ; Mutation - genetics ; Plants ; Recombination, Genetic ; sexual reproduction</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2012-04, Vol.109 (15), p.5880-5885</ispartof><rights>copyright © 1993-2008 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Apr 10, 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c556t-5ea8b4d9aa3039560081f922869b18fbbfb101e1604307240a22088e6a4ee3a53</citedby><cites>FETCH-LOGICAL-c556t-5ea8b4d9aa3039560081f922869b18fbbfb101e1604307240a22088e6a4ee3a53</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/109/15.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/41588259$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/41588259$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27903,27904,53769,53771,57995,58228</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22451936$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mirouze, Marie</creatorcontrib><creatorcontrib>Lieberman-Lazarovich, Michal</creatorcontrib><creatorcontrib>Aversano, Riccardo</creatorcontrib><creatorcontrib>Bucher, Etienne</creatorcontrib><creatorcontrib>Nicolet, Joël</creatorcontrib><creatorcontrib>Reinders, Jon</creatorcontrib><creatorcontrib>Paszkowski, Jerzy</creatorcontrib><title>Loss of DNA methylation affects the recombination landscape in Arabidopsis</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>During sexual reproduction, one-half of the genetic material is deposited in gametes, and a complete set of chromosomes is restored upon fertilization. Reduction of the genetic information before gametogenesis occurs in meiosis, when cross-overs (COs) between homologous chromosomes secure an exchange of their genetic information. COs are not evenly distributed along chromosomes and are suppressed in chromosomal regions encompassing compact, hypermethylated centromeric and pericentromeric DNA. Therefore, it was postulated that DNA hypermethylation is inhibitory to COs. Here, when analyzing meiotic recombination in mutant plants with hypomethylated DNA, we observed unexpected and counterintuitive effects of DNA methylation losses on CO distribution. Recombination was further promoted in the hypomethylated chromosome arms while it was inhibited in heterochromatic regions encompassing pericentromeric DNA. Importantly, the total number of COs was not affected, implying that loss of DNA methylation led to a global redistribution of COs along chromosomes. To determine by which mechanisms altered levels of DNA methylation influence recombination—whether directly in cis or indirectly in trans by changing expression of genes encoding recombination components—we analyzed CO distribution in wild-type lines with randomly scattered and well-mapped hypomethylated chromosomal segments. The results of these experiments, supported by expression profiling data, suggest that DNA methylation affects meiotic recombination in cis. Because DNA methylation exhibits significant variation even within a single species, our results imply that it may influence the evolution of plant genomes through the control of meiotic recombination.</description><subject>Arabidopsis</subject><subject>Arabidopsis - cytology</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis Proteins</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Biological Sciences</subject><subject>Chromatin</subject><subject>Chromosomes</subject><subject>Chromosomes, Plant</subject><subject>Chromosomes, Plant - genetics</subject><subject>cytology</subject><subject>DNA</subject><subject>DNA (Cytosine-5-)-Methyltransferases</subject><subject>DNA (Cytosine-5-)-Methyltransferases - genetics</subject><subject>DNA methylation</subject><subject>DNA Methylation - genetics</subject><subject>Epigenetics</subject><subject>Euchromatin</subject><subject>Euchromatin - metabolism</subject><subject>evolution</subject><subject>Flowers & plants</subject><subject>gametogenesis</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genetic mutation</subject><subject>genetics</subject><subject>Genomes</subject><subject>germ cells</subject><subject>Heterochromatin</subject><subject>Heterochromatin - metabolism</subject><subject>Histones</subject><subject>Inbreeding</subject><subject>meiosis</subject><subject>Meiosis - genetics</subject><subject>metabolism</subject><subject>Methylation</subject><subject>mutants</subject><subject>Mutation</subject><subject>Mutation - genetics</subject><subject>Plants</subject><subject>Recombination, Genetic</subject><subject>sexual reproduction</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUtvEzEUhS1ERUNgzQoYsWIz7fVz7A1SVB4timABXVt3Jp7G0cx4sCdI_fc4SkiADd3Yi_PdY597CHlB4YJCxS_HAdMFpQy0oBTMIzLLJy2VMPCYzABYVWrBxDl5mtIGAIzU8IScMyYkNVzNyOdlSKkIbfH-y6Lo3bS-73DyYSiwbV0zpWJauyK6JvS1H_ZKh8MqNTi6wg_FImLtV2FMPj0jZy12yT0_3HNy-_HD96vrcvn1083VYlk2UqqplA51LVYGkQM3UgFo2hrGtDI11W1dtzUF6qgCwaFiApDleNopFM5xlHxO3u19x23du1XjhiliZ8foe4z3NqC3fyuDX9u78NNyzpTMrnPy9mAQw4-tS5PtfWpcl4O5sE2WSm6E5JWg_0ch_40rA_IBKIAAaXJtc_LmH3QTtnHIS7PG5OpUpVmGLvdQE3NF0bXHhBTsrny7K9-eys8Tr_5czJH_3XYGXh-A3eTJzuTIVmoNmXi5JzZpCvGICJpVJs3JocVg8S76ZG-_MaAih1NG5Vd-AXClxdk</recordid><startdate>20120410</startdate><enddate>20120410</enddate><creator>Mirouze, Marie</creator><creator>Lieberman-Lazarovich, Michal</creator><creator>Aversano, Riccardo</creator><creator>Bucher, Etienne</creator><creator>Nicolet, Joël</creator><creator>Reinders, Jon</creator><creator>Paszkowski, Jerzy</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20120410</creationdate><title>Loss of DNA methylation affects the recombination landscape in Arabidopsis</title><author>Mirouze, Marie ; 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Reduction of the genetic information before gametogenesis occurs in meiosis, when cross-overs (COs) between homologous chromosomes secure an exchange of their genetic information. COs are not evenly distributed along chromosomes and are suppressed in chromosomal regions encompassing compact, hypermethylated centromeric and pericentromeric DNA. Therefore, it was postulated that DNA hypermethylation is inhibitory to COs. Here, when analyzing meiotic recombination in mutant plants with hypomethylated DNA, we observed unexpected and counterintuitive effects of DNA methylation losses on CO distribution. Recombination was further promoted in the hypomethylated chromosome arms while it was inhibited in heterochromatic regions encompassing pericentromeric DNA. Importantly, the total number of COs was not affected, implying that loss of DNA methylation led to a global redistribution of COs along chromosomes. To determine by which mechanisms altered levels of DNA methylation influence recombination—whether directly in cis or indirectly in trans by changing expression of genes encoding recombination components—we analyzed CO distribution in wild-type lines with randomly scattered and well-mapped hypomethylated chromosomal segments. The results of these experiments, supported by expression profiling data, suggest that DNA methylation affects meiotic recombination in cis. Because DNA methylation exhibits significant variation even within a single species, our results imply that it may influence the evolution of plant genomes through the control of meiotic recombination.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>22451936</pmid><doi>10.1073/pnas.1120841109</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Arabidopsis Arabidopsis - cytology Arabidopsis - genetics Arabidopsis Proteins Arabidopsis Proteins - genetics Biological Sciences Chromatin Chromosomes Chromosomes, Plant Chromosomes, Plant - genetics cytology DNA DNA (Cytosine-5-)-Methyltransferases DNA (Cytosine-5-)-Methyltransferases - genetics DNA methylation DNA Methylation - genetics Epigenetics Euchromatin Euchromatin - metabolism evolution Flowers & plants gametogenesis Gene expression Genes Genetic mutation genetics Genomes germ cells Heterochromatin Heterochromatin - metabolism Histones Inbreeding meiosis Meiosis - genetics metabolism Methylation mutants Mutation Mutation - genetics Plants Recombination, Genetic sexual reproduction |
| title | Loss of DNA methylation affects the recombination landscape in Arabidopsis |
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