Mutation of Arabidopsis SMC4 identifies condensin as a co-repressor of pericentromeric transposons, flowering, and DNA repair genes

In eukaryotes, transcriptionally inactive loci are enriched within highly condensed heterochromatin. In plants, as in mammals, the DNA of heterochromatin is densely methylated and wrapped by histones displaying a characteristic subset of post-translational modifications. Growing evidence indicates that these chromatin modifications are not sufficient for silencing. Instead, they are prerequisites for further assembly of higher-order chromatin structures that are refractory to transcription, but not fully understood. We show that silencing of transposons in the pericentromeric heterochromatin of Arabidopsis thaliana requires SMC4, a core subunit of condensins I and II, acting downstream of CG methylation by MET1 (DNA METHYLTRANSFERASE 1) and CHG methylation by CMT3 (CHROMOMETHYLASE 3), enabled by the chromatin remodeler DDM1 (DECREASE IN DNA METHYLATION 1). SMC4/condensin also acts within the mostly euchromatic chromosome arms to suppress conditionally-expressed genes involved in flowering or DNA repair, including the DNA glycosylase ROS1, which facilitates DNA demethylation. Collectively, our genome-wide analyses implicate condensin in the suppression of hundreds of loci, acting in both DNA methylation-dependent and methylation-independent pathways.