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.
Mathieu
Olivier
O
Laboratory of Plant Genetics, University of Geneva, Sciences III, 30 Quai Ernest-Ansermet, CH-1211 Geneva 4, Switzerland. olivier.mathieu@univ-bpclermont.fr
Reinders
Jon
J
Caikovski
Marian
M
Smathajitt
Chotika
C
Paszkowski
Jerzy
J
D017360:Arabidopsis / Q000201:enzymology / Q000235:genetics* / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D001482:Base Composition; D002467:Cell Nucleus / Q000201:enzymology / Q000378:metabolism*; D042002:Chromatin Assembly and Disassembly; D004248:DNA (Cytosine-5-)-Methyltransferases / Q000235:genetics / Q000378:metabolism; D019175:DNA Methylation; D018744:DNA, Plant; D004275:DNA, Ribosomal / Q000378:metabolism; D004268:DNA-Binding Proteins / Q000378:metabolism; D044127:Epigenesis, Genetic; D019143:Evolution, Molecular; D018507:Gene Expression Regulation, Developmental; D018506:Gene Expression Regulation, Plant; D018745:Genome, Plant; D042822:Genomic Instability; D005838:Genotype; D006570:Heterochromatin / Q000378:metabolism; D006657:Histones / Q000378:metabolism; D008745:Methylation; D008780:Methyltransferases / Q000378:metabolism; D009154:Mutation; D009687:Nuclear Proteins / Q000378:metabolism; D010641:Phenotype; D034622:RNA Interference; D034741:RNA, Small Interfering / Q000378:metabolism; D014157:Transcription Factors / Q000378:metabolism; D014158:Transcription, Genetic