Proc. Natl Acad. Sci. USA 133, E6895–E6902 (2016)

The epigenetic reprogramming that occurs in plant hybrids involves altered levels of small RNAs (sRNAs) and DNA methylation (mC). Trans-chromosomal methylation (TCM) and trans-chromosomal demethylation (TCdM) events were known to confer changes in mC levels, resulting in the epigenetic states of paternal and maternal alleles resembling each other. TCM/TCdM may also be important to heterosis. To gain insight into the establishment and features of TCM/TCdM events, a group of Australian researchers combined comprehensive epigenomic and mutant analyses for Arabidopsis parental lines, their F1 hybrids and the F2 generation.

The researchers identified hundreds of TCM/TCdM regions that were inherited by the F2 generation by comparing the methylomes among parental, F1 and F2 individuals. TCM events increased over time in F1 hybrids, suggesting the requirement of a build-up of inducing molecules, presumably small interfering RNAs (siRNAs). Another feature of the inherited TCM/TCdM regions is the enrichment of transposable elements.

The transgenerational stability of altered epigenetic states varies among F2 individuals and different genomic loci. Thirty-four candidate genes were found to show variable inheritance of the altered epigenetic states and associated variable expression, probably contributing to phenotypic segregation in the F2 population.

In some inherited TCM/TCdM regions, sRNA levels are significantly associated with altered mC states in hybrids. Genetic analysis showed that polymerase IV-dependent 24-nt siRNAs are required for the initiation of mC state change, as hybrids with a mutant polIV allele failed to establish TCM-mediated mC state change.

Although this study offers no evidence to suggest that TCM/TCdM affects heterosis, further studies will be needed to support or exclude this possibility.