Abstract
BackgroundIn plants, the existence and possible role of epigenetic reprogramming has been questioned because of the occurrence of stably inherited epialleles. Evidence suggests that epigenetic reprogramming does occur during land plant reproduction, but there is little consensus on the generality and extent of epigenetic reprogramming in plants. We studied DNA methylation dynamics during the life cycle of the liverwort Marchantia polymorpha. We isolated thalli and meristems from male and female gametophytes, archegonia, antherozoids, as well as sporophytes at early and late developmental stages, and compared their DNA methylation profiles.ResultsOf all cytosines tested for differential DNA methylation, 42% vary significantly in their methylation pattern throughout the life cycle. However, the differences are limited to few comparisons between specific stages of the life cycle and suggest four major epigenetic states specific to sporophytes, vegetative gametophytes, antherozoids, and archegonia. Further analyses indicated clear differences in the mechanisms underlying reprogramming in the gametophytic and sporophytic generations, which are paralleled by differences in the expression of genes involved in DNA methylation. Differentially methylated cytosines with a gain in methylation in antherozoids and archegonia are enriched in the CG and CHG contexts, as well as in gene bodies and gene flanking regions. In contrast, gain of DNA methylation during sporophyte development is mostly limited to the CHH context, LTR retrotransposons, DNA transposons, and repeats.ConclusionWe conclude that epigenetic reprogramming occurs at least twice during the life cycle of M. polymorpha and that the underlying mechanisms are likely different between the two events.
Highlights
In plants, the existence and possible role of epigenetic reprogramming has been questioned because of the occurrence of stably inherited epialleles
We first characterized the DNA methylation patterns of the individual tissue types separately (Fig. 2) and focused on the identification of Differentially methylated cytosine (DMC) to characterize the extent of DNA methylation dynamics during the M. polymorpha life cycle
DNA methylation was generally low in the gametophytes and DNA methylation dynamics during the life cycle were largely driven by a gain of DNA methylation in antherozoids and archegonia, a loss in the sporophyte compared to the antherozoids and the archegonia before fertilization, and another gain during sporophyte development
Summary
The existence and possible role of epigenetic reprogramming has been questioned because of the occurrence of stably inherited epialleles. Land plants do not have a predefined germline and follow a more complex life cycle with an alternation between two heteromorphic and multicellular generations: the diploid sporophyte and the haploid gametophyte [7]. Distinct cells undergo meiosis and produce spores These give rise to multicellular gametophytes, which produce the male and female gametes through mitotic divisions. Epigenetic reprogramming does occur in plants, at least to a certain extent [2, 10, 17, 18] These studies focused on either male or female gametogenesis or embryogenesis of flowering plants and do not provide a comprehensive view on the entire life cycle. Considering the different modes of sexual reproduction and different overall patterns of DNA methylation across the plant kingdom [19], it is likely that there are differences in epigenetic reprogramming between species
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