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Loss of Small-RNA-Directed DNA Methylation in the Plant Cell Cycle Promotes Germline Reprogramming and Somaclonal Variation

ABSTRACT: 5-methyl cytosine is widespread in plant genomes in both CG and non-CG contexts. During replication, hemi-methylation on parental DNA strands guides symmetric CG methylation on nascent strands, but non-CG methylation requires modified histones and small RNA guides. Here, we used immortalized Arabidopsis cell suspensions to sort replicating nuclei and determine genome-wide cytosine methylation dynamics during the plant cell cycle. We find that symmetric mCG and mCHG are selectively retained in actively dividing cells in culture, while mCHH is depleted. mCG becomes transiently asymmetric during S phase but is rapidly restored in G2, while mCHG remains asymmetric throughout the cell cycle. Hundreds of loci gain ectopic CHG methylation, as well as 24-nt small-interfering RNAs and H3K9me2, without gaining CHH methylation. This suggests that spontaneous epialelles that arise in plant cell cultures are stably maintained by small RNA independently of the canonical RNA-directed DNA methylation pathway. In contrast, loci that fail to produce siRNA are targeted for demethylation when cell cycle arrests. Comparative analysis with methylomes of various tissues and cell types suggests that loss of small RNA-directed non-CG methylation during DNA replication promotes germline reprogramming and epigenetic variation in plants propagated as clones.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE155958 | GEO | 2020/12/03

REPOSITORIES: GEO

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Loss of Small-RNA-Directed DNA Methylation in the Plant Cell Cycle Promotes Germline Reprogramming and Somaclonal Variation

Project description:5-methyl cytosine is widespread in plant genomes in both CG and non-CG contexts. During replication, hemi-methylation on parental DNA strands guides symmetric CG methylation on nascent strands, but non-CG methylation requires modified histones and small RNA guides. Here, we used immortalized Arabidopsis cell suspensions to sort replicating nuclei and determine genome-wide cytosine methylation dynamics during the plant cell cycle. We find that symmetric mCG and mCHG are selectively retained in actively dividing cells in culture, while mCHH is depleted. mCG becomes transiently asymmetric during S phase but is rapidly restored in G2, while mCHG remains asymmetric throughout the cell cycle. Hundreds of loci gain ectopic CHG methylation, as well as 24-nt small-interfering RNAs and H3K9me2, without gaining CHH methylation. This suggests that spontaneous epialelles that arise in plant cell cultures are stably maintained by small RNA independently of the canonical RNA-directed DNA methylation pathway. In contrast, loci that fail to produce siRNA are targeted for demethylation when cell cycle arrests. Comparative analysis with methylomes of various tissues and cell types suggests that loss of small RNA-directed non-CG methylation during DNA replication promotes germline reprogramming and epigenetic variation in plants propagated as clones.

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Loss of Small-RNA-Directed DNA Methylation in the Plant Cell Cycle Promotes Germline Reprogramming and Somaclonal Variation

Project description:5-methyl cytosine in plant genomes occurs in all sequence contexts, especially in heterochromatin, transposons and other repeats. During replication, nascent cytosines in symmetric contexts (CG) are guided for methylation by hemi-methyl C on the parental DNA strands of both daughter chromatids. However nascent cytosines in the asymmetric CHH context or in symmetric CHG (where H=A, T or C) use modified histones and 24-nt small interfering RNAs to restore methylation to each daughter chromatid. Here, we use fluorescent activated sorting of EdU-labeled nuclei to examine DNA methylation dynamics in dividing cell cultures of Arabidopsis thaliana. We find that CG methylation becomes transiently asymmetric during late S phase, but is rapidly restored during each cell division, while CHG methylation remains asymmetric and is substantially reduced. Levels of mCHH are extremely low in dividing cells, accompanied by a shift from 24-nt to 21-nt epigenetically activated small RNAs (easiRNAs) and a loss of histone lysine-9 methylation. When cell division arrests, RNA-directed CHH methylation is restored, but only at loci that retained 24-nt siRNAs. Comparisons with methylation patterns in pollen suggest that DNA methylation reprogramming in microspores (G2), sperm cells (S phase) and the vegetative nucleus (which is quiescent) reflect their cell cycle stage. Our results also account for the loss of non-CG methylation in plants micropropagated as clones, which undergo methylation reprogramming in the absence of fertilization.

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Loss of Small-RNA-Directed DNA Methylation in the Plant Cell Cycle Promotes Germline Reprogramming and Somaclonal Variation

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Project description:Maintenance of CG methylation (mCG) patterns is essential for chromatin-mediated epigenetic regulation of transcription in plants and mammals. Using successive generations of an Arabidopsis thaliana mutant deficient in maintaining mCG, we found that mCG loss triggered genome-wide activation of alternative epigenetic mechanisms. However, these mechanisms involving RNA-directed DNA methylation, inhibiting expression of DNA demethylases, and retargeting of histone H3K9 methylation act in a stochastic and uncoordinated fashion. As a result, new and aberrant epigenetic patterns were progressively formed over several plant generations in the absence of mCG. Interestingly, the unconventional redistribution of epigenetic marks was necessary to ‘rescue’ the loss of mCG, since mutant plants impaired in rescue activities were severely dwarfed and sterile. Our results provide evidence that mCG is a central coordinator of epigenetic memory that secures stable transgenerational inheritance in plants. Keywords: DNA methylation profiling, epigenetic inheritance, mCIP, H3K9 methylation, RdDM, demethylase expression

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Project description:Cytosine methylation is commonly targeted to symmetrical CG sites, as well as to non-CGs, such as the symmetrical-CHG and asymmetric-CHH sites in plants (H= A, C or T). Thus far, depletion of CG methylation in plants was associated with ample transcriptional activation of transposons. Here, we profiled transcription in various context specific methylation mutants in the early-diverged plant, Physcomitrella patens. We discovered that specific elimination of CG methylation is fully complemented by non-CG methylation but not vice versa. Between the symmetrically-methylated sites, CHG methylation silenced transposons stronger than CG methylation did. Finally, non-CG methylation revealed as crucial for the silencing of CG depleted transposons. Our results suggest that non-CG methylation evolved to silence transposons due to functional limitations and/or rapid mutability of methylated-CGs.

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Project description:5-methylcytosine (5mC) is a modified base often described as necessary for the proper regulation of genes and transposons and for the maintenance of genome integrity in plants. However, the extent of this dogma is limited by the current phylogenetic sampling of land plant species diversity. Here, we report that a monocot plant, Spirodela polyrhiza, has lost CG gene body methylation, genome-wide CHH methylation, and the presence or expression of several genes in the highly conserved RNA-directed DNA methylation (RdDM) pathway. It has also lost the CHH methyltransferase CHROMOMETHYLASE 2. Consequently, the transcriptome is depleted of 24-nucleotide, heterochromatic, small interfering RNAs that act as guides for the deposition of 5mC to RdDM-targeted loci in all other currently sampled angiosperm genomes. Although the genome displays low levels of genome-wide 5mC primarily at LTR retrotransposons, CG maintenance methylation is still functional. In contrast, CHG methylation is weakly maintained even though H3K9me2 is present at loci dispersed throughout the euchromatin and highly enriched at regions likely demarcating pericentromeric regions. Collectively, these results illustrate that S. polyrhiza is maintaining CG and CHG methylation mostly at repeats. S. polyrhiza reproduces rapidly through clonal propagation in aquatic environments, which we hypothesize may enable low levels of maintenance methylation to persist in large populations.

2022-08-24 | GSE161234 | GEO

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