DNA methylation dynamics during early plant life
Abstract Background Cytosine methylation is crucial for gene regulation and silencing of transposable elements in mammals and plants. While this epigenetic mark is extensively reprogrammed in the germline and early embryos of mammals, the extent to which DNA methylation is reset between generations...
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| Format: | Article |
| Language: | English |
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BMC
2017-09-01
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| Series: | Genome Biology |
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| Online Access: | http://link.springer.com/article/10.1186/s13059-017-1313-0 |
| _version_ | 1818333691708964864 |
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| author | Daniel Bouyer Amira Kramdi Mohamed Kassam Maren Heese Arp Schnittger François Roudier Vincent Colot |
| author_facet | Daniel Bouyer Amira Kramdi Mohamed Kassam Maren Heese Arp Schnittger François Roudier Vincent Colot |
| author_sort | Daniel Bouyer |
| collection | DOAJ |
| description | Abstract Background Cytosine methylation is crucial for gene regulation and silencing of transposable elements in mammals and plants. While this epigenetic mark is extensively reprogrammed in the germline and early embryos of mammals, the extent to which DNA methylation is reset between generations in plants remains largely unknown. Results Using Arabidopsis as a model, we uncovered distinct DNA methylation dynamics over transposable element sequences during the early stages of plant development. Specifically, transposable elements and their relics show invariably high methylation at CG sites but increasing methylation at CHG and CHH sites. This non-CG methylation culminates in mature embryos, where it reaches saturation for a large fraction of methylated CHH sites, compared to the typical 10–20% methylation level observed in seedlings or adult plants. Moreover, the increase in CHH methylation during embryogenesis matches the hypomethylated state in the early endosperm. Finally, we show that interfering with the embryo-to-seedling transition results in the persistence of high CHH methylation levels after germination, specifically over sequences that are targeted by the RNA-directed DNA methylation (RdDM) machinery. Conclusion Our findings indicate the absence of extensive resetting of DNA methylation patterns during early plant life and point instead to an important role of RdDM in reinforcing DNA methylation of transposable element sequences in every cell of the mature embryo. Furthermore, we provide evidence that this elevated RdDM activity is a specific property of embryogenesis. |
| first_indexed | 2024-12-13T13:55:40Z |
| format | Article |
| id | doaj.art-3712273eb44d4d23a501c4e15a357266 |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-12-13T13:55:40Z |
| publishDate | 2017-09-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-3712273eb44d4d23a501c4e15a3572662022-12-21T23:42:55ZengBMCGenome Biology1474-760X2017-09-0118111210.1186/s13059-017-1313-0DNA methylation dynamics during early plant lifeDaniel Bouyer0Amira Kramdi1Mohamed Kassam2Maren Heese3Arp Schnittger4François Roudier5Vincent Colot6Institut de Biologie Moléculaire des Plantes du CNRS - UPR2357, Université de StrasbourgInstitut de Biologie de l’Ecole Normale Supérieure, CNRS UMR 8197–INSERM U 1024Institut de Biologie de l’Ecole Normale Supérieure, CNRS UMR 8197–INSERM U 1024Institut de Biologie Moléculaire des Plantes du CNRS - UPR2357, Université de StrasbourgInstitut de Biologie Moléculaire des Plantes du CNRS - UPR2357, Université de StrasbourgInstitut de Biologie de l’Ecole Normale Supérieure, CNRS UMR 8197–INSERM U 1024Institut de Biologie de l’Ecole Normale Supérieure, CNRS UMR 8197–INSERM U 1024Abstract Background Cytosine methylation is crucial for gene regulation and silencing of transposable elements in mammals and plants. While this epigenetic mark is extensively reprogrammed in the germline and early embryos of mammals, the extent to which DNA methylation is reset between generations in plants remains largely unknown. Results Using Arabidopsis as a model, we uncovered distinct DNA methylation dynamics over transposable element sequences during the early stages of plant development. Specifically, transposable elements and their relics show invariably high methylation at CG sites but increasing methylation at CHG and CHH sites. This non-CG methylation culminates in mature embryos, where it reaches saturation for a large fraction of methylated CHH sites, compared to the typical 10–20% methylation level observed in seedlings or adult plants. Moreover, the increase in CHH methylation during embryogenesis matches the hypomethylated state in the early endosperm. Finally, we show that interfering with the embryo-to-seedling transition results in the persistence of high CHH methylation levels after germination, specifically over sequences that are targeted by the RNA-directed DNA methylation (RdDM) machinery. Conclusion Our findings indicate the absence of extensive resetting of DNA methylation patterns during early plant life and point instead to an important role of RdDM in reinforcing DNA methylation of transposable element sequences in every cell of the mature embryo. Furthermore, we provide evidence that this elevated RdDM activity is a specific property of embryogenesis.http://link.springer.com/article/10.1186/s13059-017-1313-0DNA methylationRdDMTransposable elementsEmbryogenesisEmbryo-seedling transition |
| spellingShingle | Daniel Bouyer Amira Kramdi Mohamed Kassam Maren Heese Arp Schnittger François Roudier Vincent Colot DNA methylation dynamics during early plant life Genome Biology DNA methylation RdDM Transposable elements Embryogenesis Embryo-seedling transition |
| title | DNA methylation dynamics during early plant life |
| title_full | DNA methylation dynamics during early plant life |
| title_fullStr | DNA methylation dynamics during early plant life |
| title_full_unstemmed | DNA methylation dynamics during early plant life |
| title_short | DNA methylation dynamics during early plant life |
| title_sort | dna methylation dynamics during early plant life |
| topic | DNA methylation RdDM Transposable elements Embryogenesis Embryo-seedling transition |
| url | http://link.springer.com/article/10.1186/s13059-017-1313-0 |
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