Description
DNA topoisomerases release supercoils in DNA introduced during replication or transcription. How DNA topoisomerases impact transcription in the context of eukaryotic chromatin is poorly understood. In this study, using a floral stem cell model in Arabidopsis, we uncovered a role of TOP1 in Polycomb Group (PcG) protein-mediated histone lysine 27 trimethylation at, and transcriptional repression of, the stem cell maintenance gene WUSCHEL (WUS). The strong genetic interactions between a top1 mutant and mutations in PcG genes and the overwhelming enrichment of PcG targets among genes affected in expression in the top1a mutant revealed a role of TOP1 in PcG-mediated regulation. Intriguingly, not only the repression of some PcG target genes but also the expression of others requires TOP1. The mechanism that unifies the opposing effects of TOP1 on PcG target genes appears to lie in its role in decreasing nucleosome density. Genome-wide nucleosome mapping shows that TOP1 is required for the depletion of nucleosomes at regulatory regions of genes, which probably allows the binding of factors that either recruit PcG, as we show for AGAMOUS at the WUS locus, or counteract PcG-mediated regulation. This study uncovers a strong and previously unknown connection between TOP1 and PcG.