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

Borges, F., Donoghue, M. T. A., LeBlanc, C., Wear, E. E., Tanurdžić, M., Berube, B., Brooks, A., Thompson, W. F., Hanley-Bowdoin, L., Martienssen, R. A. (November 2020) Loss of Small-RNA-Directed DNA Methylation in the Plant Cell Cycle Promotes Germline Reprogramming and Somaclonal Variation. Curr Biol, 31 (3). pp. 591-600. ISSN 0960-9822

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, whereas mCHH is depleted. mCG becomes transiently asymmetric during S phase but is rapidly restored in G2, whereas mCHG remains asymmetric throughout the cell cycle. Hundreds of loci gain ectopic CHG methylation, as well as 24-nt small interfering RNAs (siRNAs) and histone H3 lysine dimethylation (H3K9me2), without gaining CHH methylation. This suggests that spontaneous epialleles that arise in plant cell cultures are stably maintained by siRNA and H3K9me2 independent of the canonical RNA-directed DNA methylation (RdDM) pathway. In contrast, loci that fail to produce siRNA may be targeted for demethylation when the 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.

Item Type:	Paper
Additional Information:	1879-0445 Borges, Filipe Donoghue, Mark T A LeBlanc, Chantal Wear, Emily E Tanurdžić, Milos Berube, Benjamin Brooks, Ashley Thompson, William F Hanley-Bowdoin, Linda Martienssen, Robert A Journal Article England Curr Biol. 2020 Nov 27:S0960-9822(20)31675-4. doi: 10.1016/j.cub.2020.10.098.
CSHL Authors:	Martienssen, Robert A. Donoghue, Mark LeBlanc, Chantal Tanurdzic, Milos Berube, Benjamin
Communities:	CSHL labs > Martienssen lab
Depositing User:	Matthew Dunn
Date:	27 November 2020
Date Deposited:	19 Apr 2021 17:39
Last Modified:	22 Apr 2022 13:47
PMCID:	PMC9019819
Related URLs:	Publisher
URI:	https://repository.cshl.edu/id/eprint/39847

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