Extensive allele‐level remodeling of histone methylation modification in reciprocal F1 hybrids of rice subspecies

Epigenetic mechanisms play a major role in heterosis, partly as a result of the remodeling of epigenetic modifications in F₁ hybrids. Based on chromatin immunoprecipitation‐sequencing (ChIP‐Seq) analyses, we show that at the allele level extensive histone methylation remodeling occurred for a subset of genomic loci in reciprocal F₁ hybrids of Oryza sativa (rice) cultivars Nipponbare and 93‐11, representing the two subspecies japonica and indica. Globally, the allele modification‐altered loci in leaf or root of the reciprocal F₁ hybrids involved ?12–43% or more of the genomic regions carrying either of two typical histone methylation markers, H3K4me3 (>21 000 genomic regions) and H3K27me3 (>11 000 genomic regions). Nevertheless, at the total modification level, the majority (from ?43 to >90%) of the modification‐altered alleles lay within the range of parental additivity in the hybrids because of concerted alteration in opposite directions, consistent with an overall attenuation of allelic differences in the modifications. Importantly, of the genomic regions that did show non‐additivity in total modification level by either marker in the two tissues of hybrids, >80% manifested transgressivity, which involved genes enriched in specific functional categories. Extensive allele‐level alteration of H3K4me3 alone was positively correlated with genome‐wide changes in allele‐level gene expression, whereas at the total level, both H3K4me3 and H3K27me3 remodeling, although affecting just a small number of genes, contributes to the overall non‐additive gene expression to variable extents, depending on tissue/marker combinations. Our results emphasize the importance of allele‐level analysis in hybrids to assess the remodeling of epigenetic modifications and their relation to changes in gene expression.