Compromised stability of DNA methylation and transposon immobilization in mosaic <i>Arabidopsis</i> epigenomes

TLDR

Transgenerational epigenetic inheritance has been largely characterized at a limited number of loci. The authors recommend that future epigenomic analyses account for genetic instabilities and use alternative mapping strategies. The study examined recombinant inbred lines with mosaic chromosomes containing wild‑type and CG‑methylation–depleted segments. In epiRILs, transposons that were immobile in parents became mobile in 28 % of lines, and after eight generations recombined segments displayed high nonparental methylation polymorphism, revealing long‑lasting epi‑allelic interactions that violate Mendelian expectations and complicate linkage‑based mapping.

Abstract

Transgenerational epigenetic inheritance has been defined by the study of relatively few loci. We examined a population of recombinant inbred lines with epigenetically mosaic chromosomes consisting of wild-type and CG methylation-depleted segments (epiRILs). Surprisingly, transposons that were immobile in the parental lines displayed stochastic movement in 28% of the epiRILs. Although analysis after eight generations of inbreeding, supported by genome-wide DNA methylation profiling, identified recombined parental chromosomal segments, these were interspersed with unexpectedly high frequencies of nonparental methylation polymorphism. Hence, epigenetic inheritance in hybrids derived from parents with divergent epigenomes permits long-lasting epi-allelic interactions that violate Mendelian expectations. Such persistently “unstable” epigenetic states complicate linkage-based epigenomic mapping. Thus, future epigenomic analyses should consider possible genetic instabilities and alternative mapping strategies.