Heritable changes of epialleles in maize can be triggered in the absence of DNA methylation

Abstract

Trans-chromosomal interactions resulting in changes in DNA methylation during hybridization have been observed in several plant species. However, very little is known about the causes or consequences of these interactions, many of which result in changes in methylation of transposable elements. Here, we compared DNA methylomes of F1 hybrids that are mutant for two small RNA biogenesis genes,Mop1(mediator of paramutation1) andLbl1(leafbladeless1) with that of their parents, wild type siblings, and backcrossed progeny in maize. Our data show that hybridization triggers global changes in bothtrans-chromosomal methylation (TCM) andtrans-chromosomal demethylation (TCdM). Despite changes in CHH methylation in F1 hybrids, no significant changes in the quantity or distribution of small RNAs were observed. The methylation at the CHH TCM differentially methylated regions (DMRs) was largely removed in themop1mutant, although the effects of this mutant vary depending on the location of the CHH sites. Interestingly, an increase in CHH at TCM DMRs was associated with enhanced expression of a subset of highly expressed genes and suppressed expression of a small number of lowly expressed genes. Examination of the methylation levels in backcrossed plants demonstrates that the newly triggered methylation can be maintained to the subsequent generation, but that TCdM is maintained more stable than is TCM. Surprisingly, although increase CHH methylation in F1 plants did requireMop1, heritability of TCM or TCdMs did not require a functional copy of this gene, suggesting that initiation of these heritable changes in epigenetic state are not dependent on RdDM.

The Genomic Shock Hypothesis: Genetic and Epigenetic Alterations of Transposable Elements after Interspecific Hybridization in Plants

“…Barber et al (2012) [ 56 ] analyzed how siRNA populations vary between two maize inbred lines (B73 and Mo17) and their hybrid in the shoot apex and the developing ear (high percentages of these siRNAs derive from retrotransposons) and found that the small RNA levels are altered in the hybrids. In the same hybrid, Liu et al (2023) [ 57 ] found that there are regions where methylation decreases after hybridization despite the production of small RNAs.…”

“…The DNA demethylation can activate the TE transposition [ 140 ]. The methylation status of TEs returns to near parental levels in a relatively short time (a few generations), and siRNAs play an important role in this process [ 57 ]. If the active TE content of both genomes is different, the small RNA sequences derived from one parent differ from the other, resulting in an enhanced TE activity depending on which parent contains more active TEs.…”