Epigenome confrontation triggers immediate reprogramming of DNA methylation and transposon silencing in Arabidopsis epihybrids

Genes and transposons can exist in variable DNA methylation states with potentially differential transcription. However, how these epialleles emerge is poorly understood. Here we show that crossing a hypomethylated plant with its normally methylated wild-type counterpart results already in the F1 generation in widespread changes in DNA methylation and transcription patterns. Novel non-parental and heritable epialleles arise at many genic loci, including a locus that itself controls DNA methylation patterns, but with most of the changes affecting pericentromeric transposons. While a subset of transposons show immediate resilencing, a large number displays decreased DNA methylation, which is associated with de novo or enhanced transcriptional activation. This can translate into transposon mobilization in the progeny. Our findings reveal that the combination of distinct epigenomes can be viewed as an epigenomic shock, which is characterized by a round of epigenetic variation creating novel patterns of gene and TE regulation.