Extensive epigenetic reprogramming during the life cycle of Marchantia polymorpha

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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-017-1383-z) contains supplementary material, which is available to authorized users.

Evidence for rapid evolution in a grassland biodiversity experiment

“…DNA methylation data were processed and filtered as described above. Variation in DNA methylation at each individual cytosine was then analysed with a linear model in r with the package DSS (version 2.24.0; Park & Wu, ), according to a design with a single factor comprising all different experimental treatment combinations as separate levels and using contrasts to compare levels of interest; similar to the approach described for RNA‐Seq in Schmid () and the testing procedure described in Schmid, Giraldo‐Fonseca, et al (). Specific groups were compared with linear contrasts and p ‐values for each contrast were adjusted for multiple testing to reflect FDRs (Benjamini & Hochberg, ).…”

“…the testing procedure described in Schmid, Giraldo-Fonseca, et al (2018). Specific groups were compared with linear contrasts and pvalues for each contrast were adjusted for multiple testing to reflect FDRs (Benjamini & Hochberg, 1995).…”

Characterization of evolutionarily conserved key players affecting eukaryotic flagellar motility and fertility using a moss model

“…In P. patens, methylated gene bodies usually are associated with lower gene expression (Lang et al 2018) and loss of the DNA methyltransferase PpMET1, which is involved in CG DNA methylation of gene bodies, inhibits sporophyte development (Yaari et al 2015). Recently, it has been shown, that the male reproductive organs undergo severe changes in DNA methylation in the liverwort M. polymorpha during sexual reproduction (Schmid et al 2018). Hence, we expected DNA methylation to play a role during regulation of sexual reproduction in moss.…”

DNA methylation in Marchantia polymorpha

“…Additionally, there are two AGO‐LIKE members named MpPIWIa and MpPIWIb that are missing the PAZ domain but with a distinctive PIWI domain and show an increased expression in the antheridiophores (Fig. (7)) (Schmid et al ., ). Marchantia contains two de novo DNA methyltransferases, two CMT‐like methyltransferases (that do not reside in a clade with CMT2 or CMT3 clades) and two members of the ROS1 DNA glycosylase family.…”

“…Mp CMTb is highly enriched in young sporophytes (Fig. (13)) (Bowman et al ., ; Schmid et al ., ). This opens the possibility of diversified RdDM modules acting with temporal or tissue specificity.…”