DNA methylation dynamics during early plant life

Abstract

BackgroundCytosine 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.ResultsUsing 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.ConclusionOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-017-1313-0) contains supplementary material, which is available to authorized users.

Epigenetic dynamics during flowering plant reproduction: evidence for reprogramming?

“…In mature Arabidopsis embryos, CHH methylation approaches 100% at individual cytosines, whereas in other tissues, including younger embryos, individual CHH sites are c . 20% methylated (Bouyer et al ., ). Methylation decreases upon seed germination, likely through a passive mechanism (Bouyer et al ., ; Kawakatsu et al ., ; Lin et al ., ; Narsai et al ., ).…”

“…Recent studies from soybean and Arabidopsis have shown that CHH methylation increases during embryogenesis (Kawakatsu et al, 2017;Lin et al, 2017;Narsai et al, 2017). In mature Arabidopsis embryos, CHH methylation approaches 100% at individual cytosines, whereas in other tissues, including younger embryos, individual CHH sites are c. 20% methylated (Bouyer et al, 2017). Methylation decreases upon seed germination, likely through a passive mechanism (Bouyer et al, 2017;Kawakatsu et al, 2017;Lin et al, 2017;Narsai et al, 2017).…”

“…In mature Arabidopsis embryos, CHH methylation approaches 100% at individual cytosines, whereas in other tissues, including younger embryos, individual CHH sites are c. 20% methylated (Bouyer et al, 2017). Methylation decreases upon seed germination, likely through a passive mechanism (Bouyer et al, 2017;Kawakatsu et al, 2017;Lin et al, 2017;Narsai et al, 2017). It is unknown whether the increased CHH methylation in developing embryos is functional: mutation of the de novo methyltransferases DRM2 and CMT2 prevents CHH methylation but without obvious effects on seed development or germination, although it is unclear how comprehensively phenotypes have been assessed.…”

Azacitidine (5-AzaC)-treatment and mutations in DNA methylase genes affect embryogenic response and expression of the genes that are involved in somatic embryogenesis in Arabidopsis

“…Since, DNA methylation is accompanied by active DNA demethylation and the balance between these antagonistic processes is believed to control the pattern of DNA methylation in plant development including the early stages of embryogenesis (Penterman et al 2007;Lei et al 2015;Bouyer et al 2017), we also analysed the expression of the genes encoding DNA demethylases during SE induction and a distinct down-regulation of ROS1, DME and DML2 genes in the SE-induced explants was observed. Thus, the reduction of the global DNA methylation level that was found in the embryogenic culture (present results) appears not to directly result from the transcriptional activity of the genes encoding DNA methylases and demethylases.…”

“…During the life cycle of Arabidopsis, the global level of DNA methylation undergoes dynamic changes and the content of 5 mC decreases in gametogenesis and increases after fertilisation and during embryo development (Jullien et al 2012;Bouyer et al 2017). In adult plants, variations in the level and pattern of methylation have been observed between the plant organs but the overall trend is that the 5 mC content increases during the aging and maturation of a plant (RuizGarcía et al 2005;Widman et al 2014).…”