Paternal DNA methylation is remodeled to maternal levels in rice zygote

Abstract

Epigenetic reprogramming occurs during reproduction to reset the genome for early development. In flowering plants, mechanistic details of parental methylation remodeling in zygote remain elusive. Here we analyze allele-specific DNA methylation in rice hybrid zygotes and during early embryo development and show that paternal DNA methylation is predominantly remodeled to match maternal allelic levels upon fertilization, which persists after the first zygotic division. The DNA methylation remodeling pattern supports the predominantly maternal-biased gene expression during zygotic genome activation (ZGA) in rice. However, parental allelic-specific methylations are reestablished at the globular embryo stage and associate with allelic-specific histone modification patterns in hybrids. These results reveal that paternal DNA methylation is remodeled to match the maternal pattern during zygotic genome reprogramming and suggest existence of a chromatin memory allowing parental allelic-specific methylation to be maintained in the hybrid.

DNA methylation remodeling and the functional implication during male gametogenesis in rice

“…Previous results showed that DNA methylation in plants is partially remodeled or reconfigured in male and female gametes [ 12 – 17 , 19 ]. In this work, we provided evidence that non-CG (mainly CHG) methylations are dynamically remodeled during rice male gametogenesis with the highest levels observed in microspore and the lowest levels in sperm.…”

“…The generative cell is further divided to produce two sperm cells in the mature pollen grain, the male gametophyte. Previous studies showed that plant sperm DNA methylation is remodeled and shows variation relative to somatic tissues [ 12 , 14 , 16 – 19 ]. However, it remains unclear whether the remodeling process is initiated in male meiocytes before meiosis or at the subsequent steps after meiosis and whether DNA methylation remodeling is required for male gametogenesis.…”

Comparative transcriptomic analysis reveals the molecular mechanism underlying seedling heterosis and its relationship with hybrid contemporary seeds DNA methylation in soybean

“…Previous studies in rice have demonstrated that DNA methylation in hybrid contemporary seeds or embryos can affect the expression levels of hybrid seedlings ( Zhou et al., 2021 ; Liu et al., 2023 ). We speculate that a similar situation exists in soybean hybrids.…”

“…The significant correlation between methylation levels in gene regions and seedling expression levels, along with the similarity of reprogramming patterns ( Figures 5A, B , Supplementary Figures S11A, C ), which typically occur in plant hybrids of the same growth period ( Orantes-Bonilla et al., 2023 ; Rao et al., 2023 ). It has been observed that DNA methylation patterns in soybean seed development can be partially inherited during the early stages of seedling growth ( Lin et al., 2017 ), and research on rice F 1 zygote has shown that DNA methylation is transmitted through cell division following reprogramming completion and is linked to histone modification in seedlings ( Liu et al., 2023 ). Additionally, the DNA methylation status of rice hybrid shoots was discovered to persist during the emergence of young spikes, indicating lasting methylation at specific loci ( Ma et al., 2021 ).…”

“…In Arabidopsis and pigeonpea, the pattern of DNA methylation changes is similar to that of gene expression in F 1 seedlings, both of which are dominated by non-additive types and involve very similar biological pathways ( Shen et al., 2012 ; Sinha et al., 2020 ). On the other hand, DNA methylation recombination profiles of contemporary seeds in rice hybrids are associated with non-additive expression of several rhythmic and yield-related genes ( Zhou et al., 2021 ), and the methylation sites formed during the zygote period can be transferred to subsequent life processes ( Liu et al., 2023 ). A fact that the rhythmic expression of the AtCCA1 ( Circadian clock associated 1 ) gene formed 10 days after cross-pollination can be maintained until late plant development and demethylation of the gene in hybrid seedlings results in the loss of biomass heterosis ( Ng et al., 2014 ).…”