Transgenerational Stability of the Arabidopsis Epigenome Is Coordinated by CG Methylation

SummaryMaintenance of CG methylation (mCG) patterns is essential for chromatin-mediated epigenetic regulation of transcription in plants and mammals. However, functional links between mCG and other epigenetic mechanisms in vivo remain obscure. Using successive generations of an Arabidopsis thaliana mutant deficient in maintaining mCG, we find that mCG loss triggers genome-wide activation of alternative epigenetic mechanisms. However, these mechanisms, which involve RNA-directed DNA methylation, inhibiting expression of DNA demethylases, and retargeting of histone H3K9 methylation, act in a stochastic and uncoordinated fashion. As a result, new and aberrant epigenetic patterns are progressively formed over several plant generations in the absence of mCG. Interestingly, the unconventional redistribution of epigenetic marks is necessary to “rescue” the loss of mCG, since mutant plants impaired in rescue activities are severely dwarfed and sterile. Our results provide evidence that mCG is a central coordinator of epigenetic memory that secures stable transgenerational inheritance in plants.