Active DNA Demethylation in Plant Companion Cells Reinforces Transposon Methylation in Gametes

Abstract

The Arabidopsis thaliana central cell, the companion cell of the egg, undergoes DNA demethylation before fertilization, but the targeting preferences, mechanism, and biological significance of this process remain unclear. Here, we show that active DNA demethylation mediated by the DEMETER DNA glycosylase accounts for all of the demethylation in the central cell and preferentially targets small, AT-rich, and nucleosome-depleted euchromatic transposable elements. The vegetative cell, the companion cell of sperm, also undergoes DEMETER-dependent demethylation of similar sequences, and lack of DEMETER in vegetative cells causes reduced small RNA–directed DNA methylation of transposons in sperm. Our results demonstrate that demethylation in companion cells reinforces transposon methylation in plant gametes and likely contributes to stable silencing of transposable elements across generations.

Hypomethylated Pollen Bypasses the Interploidy Hybridization Barrier inArabidopsis

“…Consistent with these data, we found strong enrichment of H3K27m3 on genes showing increased expression levels in triploid seeds compared with diploid seeds ( Figure 7A). Loss of FIS-PRC2 function in the endosperm causes strikingly similar changes of DNA methylation, as we report in this study: reduced levels of CHG and CHH methylation and increased levels of CG methylation (Ibarra et al, 2012). Previous studies revealed that hypomethylated pollen derived from a MET1 antisense plant can bypass maternal FIS-PRC2 requirement (Luo et al, 2000;Vinkenoog et al, 2000).…”

Epigenetic trigger for tomato ripening

“…These findings are consistent with studies of mammalian genes, where hypomethylation of gene-regulatory regions is commonly observed at sites of DNA-protein interaction 8 . Interestingly, the authors observe very little change in DNA methylation state on transposable elements during fruit maturation, in stark contrast to the novel developmental demethylation events recently reported in the endosperm and pollen of Arabidopsis, which occur mainly on transposable elements 9,10 .…”

Pollen-Specific Activation of Arabidopsis Retrogenes Is Associated with Global Transcriptional Reprogramming

“…The second model proposes spermatocyte-specific transcriptional reprogramming by global chromatin changes and transcriptional activation of retrogenes and their subsequent functionalization specific to spermatocytes (Marques et al, 2005;Potrzebowski et al, 2008). In plants, pollen has been identified as the hotspot of chromatin reprogramming (Slotkin et al, 2009;Ibarra et al, 2012;Hoffmann and Palmgren, 2013), and we have shown that pollen upregulated genes are depleted from transcription-permissive chromatin marks in somatic tissues. Furthermore, we found several retrogenes that are associated with pollen growth and development and the PCR11 retrogene, which is transcribed in pollen, contrary to its parent.…”

“…More likely, many retrogenes are part of global cellular reprogramming in male gametes. So far, chromatin changes in male gametes have been associated mainly with DNA methylation changes (Slotkin et al, 2009;Ibarra et al, 2012), but there is emerging evidence that histone modifications may also contribute to pollen-specific gene reprogramming (Hoffmann and Palmgren, 2013). In order to identify possible causes of the observed pollen-specific transcription, we explored available data on tissue-and mutant-specific transcription and the distribution of chromatin modifications.…”

“…In contrast, transcriptionally repressed genes and repetitive elements are typically labeled by histone H3 Lysine 27 trimethylation (H3K27me3), histone H3 Lysine 9 dimethylation (H3K9me2), and/or high-density DNA methylation in all cytosine sequence contexts in plants Stroud et al, 2013). While H3K27me3 ensures tissue-specific developmental transcription (Lafos et al, 2011), the role of H3K9me2 and promoter DNA methylation is to minimize the activities of repetitive elements, which frequently include retrotransposons (Mosher et al, 2009;Slotkin et al, 2009;Ibarra et al, 2012). Retrogenes are generated by retrotransposon reverse transcriptases and represent duplicated copies.…”