DNA Topoisomerase I Affects Polycomb Group Protein-Mediated Epigenetic Regulation and Plant Development by Altering Nucleosome Distribution in Arabidopsis

It has been perplexing that DNA topoisomerases, enzymes that release DNA supercoils, play specific roles in development. In this study, using a floral stem cell model in Arabidopsis thaliana, we uncovered a role for TOPOISOMERASE1 alpha (TOP1 alpha) in Polycomb Group (PcG) protein-mediated histone 3 lysine 27 trimethylation (H3K27me3) at, and transcriptional repression of, the stem cell maintenance gene WUSCHEL (WUS). We demonstrated that H3K27me3 deposition at other PcG targets also requires TOP1 alpha. Intriguingly, the repression of some, as well as the expression of many, PcG target genes requires TOP1 alpha. The mechanism that unifies the opposing effects of TOP1 alpha appears to lie in its role in decreasing nucleosome density, which probably allows the binding of factors that either recruit PcG, as we demonstrated for AGAMOUS at the WUS locus, or counteract PcG-mediated regulation. Although TOP1 alpha reduces nucleosome density at all genes, the lack of a 5' nucleosomefree region is a feature that distinguishes PcG targets from nontargets and may condition the requirement for TOP1 alpha for their expression. This study uncovers a connection between TOP1 alpha and PcG, which explains the specific developmental functions of TOP1 alpha.