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.
Subjects: organism description > plant > Arabidopsis
bioinformatics
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification > DNA methylation
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification
bioinformatics > genomics and proteomics > genetics & nucleic acid processing
bioinformatics > genomics and proteomics
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > protein structure, function, modification
organs, tissues, organelles, cell types and functions > cell types and functions > cell functions > cell cycle
organs, tissues, organelles, cell types and functions > cell types and functions > cell functions
organs, tissues, organelles, cell types and functions > cell types and functions
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > protein structure, function, modification > protein types > enzymes
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > protein structure, function, modification > protein types > histone
organs, tissues, organelles, cell types and functions
organism description > plant
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > protein structure, function, modification > protein types
CSHL Authors:
Communities: CSHL Cancer Center Program
CSHL Cancer Center Program > Gene Regulation and Inheritance Program
CSHL Cancer Center Shared Resources
CSHL labs > Martienssen lab
School of Biological Sciences > Publications
Depositing User: Matthew Dunn
Date: 27 November 2020
Date Deposited: 19 Apr 2021 17:39
Last Modified: 29 Feb 2024 19:31
PMCID: PMC9019819
Related URLs:
URI: https://repository.cshl.edu/id/eprint/39847

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