Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation

Maintenance of CG methylation (m CG) patterns is essential for chromatin-mediated epigenetic regulation of transcription in plants and mammals. However, functional links between m CG and other epigenetic mechanisms in vivo remain obscure. Using successive generations of an Arabidopsis thaliana mutant deficient in maintaining m CG, we find that m CG 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 m CG. Interestingly, the unconventional redistribution of epigenetic marks is necessary to "rescue'' the loss of m CG, since mutant plants impaired in rescue activities are severely dwarfed and sterile. Our results provide evidence that m CG is a central coordinator of epigenetic memory that secures stable transgenerational inheritance in plants.