Mutation of Arabidopsis SMC4 identifies condensin as a corepressor of pericentromeric transposons and conditionally expressed genes

Abstract

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 requires SMC4, a core subunit of condensins I and II, acting in conjunction with CG methylation by MET1 (DNA METHYLTRANSFERASE 1), CHG methylation by CMT3 (CHROMOMETHYLASE 3), the chromatin remodeler DDM1 (DECREASE IN DNA METHYLATION 1), and histone modifications, including histone H3 Lys 27 monomethylation (H3K27me1), imparted by ATXR5 and ATXR6. 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.

The Arabidopsis condensin CAP-D subunits arrange interphase chromatin

“…Accordingly, we observed no increased retrotransposon transcription in any of the cap-d3 mutants. Moreover, in accordance with our observations for both cap-d3 mutants, the protein-coding genes up-regulated in smc4 mutants are mainly involved in flower development, reproductive processes and DNA repair, and are distributed all over the genome (Wang et al, 2017). However, we observed in the cap-d3 mutants a differential expression of genes involved in transcription and stress response.…”

“…Moreover, condensin of fission yeast, which is similar to condensin I, binds to RNA polymerase III transcribed genes (5S rDNA and tRNA), and mediates their localization near the centromeres (Iwasaki et al, 2010). The nuclear and chromocenter phenotype which we observed in the cap-d3 mutants differs from previous reports (Moissiard et al, 2012;Sakamoto and Takagi, 2013;Tatout et al, 2014;Poulet et al, 2017;Wang et al, 2017). The chromocenters cluster and localize at the nuclear periphery, but do not decondense, the nuclear area does not change compared to that of wild-type, and the general degree of DNA and histone methylation is unaffected.…”

“…Moreover, hypomethylation, linc and morc mutants do not show transcriptional silencing of centromeric and pericentromeric repeats, and of silenced genes (Moissiard et al, 2012;Poulet et al, 2017). In contrast, CAP-D3 has little effect on silencing, because no increased transcription of transposable elements was detected in cap-d3 mutants (Wang et al, 2017). MORC, CRWN and LINC proteins localize close to the chromocenters, MORC foci adjacent to the chromocenters (Moissiard et al, 2012), CRWN1 and CRWN4 at the nuclear periphery (Sakamoto and Takagi, 2013), and the LINC complex in the nuclear envelope (Tatout et al, 2014).…”

“…Thus, chromatin structure changes as induced in the A. thaliana cap-d3 mutants seem to influence the global transcription only slightly. Wang et al (2017) showed that A. thaliana SMC4, but not CAP-D3, is important to maintain the repression of pericentromeric retrotransposons independent of DNA methylation. Accordingly, we observed no increased retrotransposon transcription in any of the cap-d3 mutants.…”

Acute condensin depletion causes genome decompaction without altering the level of global gene expression inSaccharomyces cerevisiae

“…In C. elegans and other organisms, condensins have been linked to the regulation of transcription (38,79,80). Our data indicate that the global gene expression program is largely unaffected by condensin depletion in yeast.…”