DNA Methylation Dynamics during Sexual Reproduction in Arabidopsis thaliana

Abstract

DNA methylation maintains genome stability and regulates gene expression [1]. In mammals, DNA methylation is reprogrammed in the germline from one generation to the next [2]. In plants, it was considered that patterns of DNA methylation are stably maintained through sexual reproduction [3-6]. However, a recent report showed discrete variations of DNA methylation profiles from mother to daughter plants [7]. The mechanisms that explain these variations have remained unknown. Here, we report that maintenance DNA methyltransferases are barely expressed during Arabidopsis female gametogenesis. In contrast, after fertilization both maintenance and de novo DNA methyltransferases are expressed strongly in the embryo. Embryogenesis is marked by increased de novo DNA methylation, reaching levels that are further maintained in the adult plant. The accumulation of these epigenetic marks after fertilization silences a methylation-sensitive fluorescent reporter. De novo DNA methylation in the embryo provides a mechanism that could account for the gradual remethylation of experimentally demethylated genomes [8, 9]. In conclusion, we uncover that DNA methylation activity fluctuates during sexual reproduction. This cycle likely explains variations of genome-wide patterns of DNA methylation across generations in Arabidopsis [7, 10] and enables a limited degree of reprogramming of the epigenome.

Genomic DNA methylation analyses reveal the distinct profiles in castor bean seeds with persistent endosperms

“…Similarly, among the CMT genes, responsible for mediating CHG methylation, RcCMT1 was highly expressed in leaf, stem apex, pollen, and early embryo but lowly expressed in ovule and developing endosperms (including the early and late stages), while RcCMT2 was expressed mainly in the developing embryo and early endosperm tissues. The substantial reduction of transcript levels of both RcMET1 and RcCMT genes in castor bean endosperm compared with embryo was consistent with a report on Arabidopsis (Jullien et al, 2012). Within the DRM genes, responsible for guiding CHH methylation, RcDRM1 was expressed specifically in ovule, similar to DRM1 expression in Arabidopsis (Jullien et al, 2012), while RcDRM2 and RcDRM3 were expressed mainly in developing embryo and endosperm tissues, distinctly different from their expression in Arabidopsis.…”

“…The substantial reduction of transcript levels of both RcMET1 and RcCMT genes in castor bean endosperm compared with embryo was consistent with a report on Arabidopsis (Jullien et al, 2012). Within the DRM genes, responsible for guiding CHH methylation, RcDRM1 was expressed specifically in ovule, similar to DRM1 expression in Arabidopsis (Jullien et al, 2012), while RcDRM2 and RcDRM3 were expressed mainly in developing embryo and endosperm tissues, distinctly different from their expression in Arabidopsis. In Arabidopsis, DRM2 was strongly transcribed in the embryo tissue but not detected in endosperm (Jullien et al, 2012).…”

“…Within the DRM genes, responsible for guiding CHH methylation, RcDRM1 was expressed specifically in ovule, similar to DRM1 expression in Arabidopsis (Jullien et al, 2012), while RcDRM2 and RcDRM3 were expressed mainly in developing embryo and endosperm tissues, distinctly different from their expression in Arabidopsis. In Arabidopsis, DRM2 was strongly transcribed in the embryo tissue but not detected in endosperm (Jullien et al, 2012). In addition, the RcDnmt2 gene, in spite of its functional uncertainty, was broadly expressed in diverse tissues.…”

A transcriptional view on somatic embryogenesis

“…Chromatin‐modifying factors regulate epigenome reprogramming to change the chromatin states of genes, and are important in particular to guide global transcriptome shifts during phase transitions. In the plant's life cycle, epigenome reprogramming is required for all developmental transitions: from seed to seedling (Molitor, Bu, Yu, & Shen, 2014; Zanten et al., 2014); from vegetative growth to flowering (Hepworth & Dean, 2015); from somatic to reproductive cell during sporogenesis and gametogenesis (Borg & Berger, 2015; Houben, Kumke, Nagaki, & Hause, 2011; She et al., 2013); and after fertilization from gamete to zygotic embryo (Ingouff et al., 2010; Jullien, Susaki, Yelagandula, Higashiyama, & Berger, 2012). …”

Networks controlling seed size in Arabidopsis

“…255 Of particular importance is the balance of methylation 256 between maternal and paternal alleles in the central cell. 257 Removal of DNA methylation relies on the enzymatic 258 activity of DEMETER (DME) (Kinoshita et al 2004;259 Gehring et al 2006), and DNA methylation depends on the 260 enzyme DNA methyltransferase 1 (MET1) (Hsieh et al 261 2011;Jullien et al 2012). DME is expressed in the central 262 cell in the embryo sac (Choi et al 2002) and in the vege-263 tative cell of the pollen grain (Schoft et al 2011).…”