Abstract
Cytosine methylation within CG dinucleotides (mCG) can be epigenetically inherited over many generations. Such inheritance is thought to be mediated by a semiconservative mechanism that produces binary present/absent methylation patterns. However, we show here that, in Arabidopsis thaliana h1ddm1 mutants, intermediate heterochromatic mCG is stably inherited across many generations and is quantitatively associated with transposon expression. We develop a mathematical model that estimates the rates of semiconservative maintenance failure and de novo methylation at each transposon, demonstrating that mCG can be stably inherited at any level via a dynamic balance of these activities. We find that DRM2—the core methyltransferase of the RNA-directed DNA methylation pathway—catalyzes most of the heterochromatic de novo mCG, with de novo rates orders of magnitude higher than previously thought, whereas chromomethylases make smaller contributions. Our results demonstrate that stable epigenetic inheritance of mCG in plant heterochromatin is enabled by extensive de novo methylation.
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•Stable epigenetic inheritance of intermediate CG methylation in heterochromatin•Quantitative association of CG methylation with expression of transposable elements•Mathematical modeling reveals extensive heterochromatic de novo CG methylation•Heterochromatic de novo CG methylation mainly mediated by the RdDM pathway
By inbreeding DNA methylation-deficient Arabidopsis thaliana plants for many generations, Lyons et al. find that epigenetic inheritance of heterochromatic CG methylation relies on multiple methyltransferases and, using mathematical modeling, demonstrate that the inheritance process is much more dynamic and flexible than previously thought.