DNA methylation-free Arabidopsis reveals crucial roles of DNA methylation in regulating gene expression and development

Abstract

A contribution of DNA methylation to defense against invading nucleic acids and maintenance of genome integrity is uncontested; however, our understanding of the extent of involvement of this epigenetic mark in genome-wide gene regulation and plant developmental control is incomplete. Here, we knock out all five known DNA methyltransferases in Arabidopsis, generating DNA methylation-free plants. This quintuple mutant exhibits a suite of developmental defects, unequivocally demonstrating that DNA methylation is essential for multiple aspects of plant development. We show that CG methylation and non-CG methylation are required for a plethora of biological processes, including pavement cell shape, endoreduplication, cell death, flowering, trichome morphology, vasculature and meristem development, and root cell fate determination. Moreover, we find that DNA methylation has a strong dose-dependent effect on gene expression and repression of transposable elements. Taken together, our results demonstrate that DNA methylation is dispensable for Arabidopsis survival but essential for the proper regulation of multiple biological processes.

DNA methylation underpins the epigenomic landscape regulating genome transcription in Arabidopsis

“…To completely eliminate DNA methylation, we recently generated the quintuple mutant mddcc ( met1 drm1 drm2 cmt2 cmt3 ), in which all reported DNA methyltransferases were mutated [ 28 ]. As expected, almost all CG and non-CG methylation is eliminated in met1 and ddcc , respectively, revealed by examinations of both two- [ 28 ] and five-week-old mutant plants (Additional file 1 : Fig. S1) used in this study; DNA methylation in all contexts is completely eliminated in mddcc mutant, which grew extremely slowly and failed to flower [ 28 ] (Fig.…”

“…DNA methylation is involved in the control of TE activity; consistent with this, mutants lacking DNA methylation displayed a reactivation of TEs [ 8 ]. A higher number of TEs were derepressed in met1 than in ddcc , suggesting that CG methylation plays a larger role than non-CG methylation in TE silencing [ 28 ] (Fig. 7 a).…”

Zebularine, a DNA Methylation Inhibitor, Activates Anthocyanin Accumulation in Grapevine Cells

“…In most cases, a high methylation level at the promoter in all sequence contexts is associated with a reduced gene expression [ 35 ], although in a few cases the reverse situation was demonstrated, as for example for the Arabidopsis ROS1 gene [ 36 , 37 ]. Moreover, transcriptional regulation through DNA methylation has been shown to play important roles during plant development and in response to environmental changes [ 38 , 39 , 40 , 41 ]. Interestingly, the genes whose expression regulation involves DNA methylation include a number of genes related to plant metabolism and in particular to plant secondary metabolism.…”

Accurate simultaneous sequencing of genetic and epigenetic bases in DNA

“…Genetic sequencing of the DNA bases G, C, T and A has been transformed by high throughput sequencing approaches in the past two decades. Epigenetic information in DNA provides insights into dynamic changes in biology that is closely associated with transcriptional programmes 1 and cell fate 2 . The combination of genetic and epigenetic information provides a more comprehensive view of biology.…”