DNA methylation and histone H1 jointly repress transposable elements and aberrant intragenic transcripts

DNA methylation and histone H1 mediate transcriptional silencing of genes and transposable elements, but how they interact is unclear. In plants and animals with mosaic genomic methylation, functionally mysterious methylation is also common within constitutively active housekeeping genes. Here we show that H1 is enriched in methylated sequences, including genes, of Arabidopsis thaliana, yet this enrichment is independent of DNA methylation. Loss of H1 disperses heterochromatin, globally alters nucleosome organization, and activates H1-bound genes, but only weakly de-represses transposable elements. However, H1 loss strongly activates transposable elements hypomethylated through mutation of DNA methyltransferase MET1. Hypomethylation of genes also activates antisense transcription, which is enhanced by H1 loss. Our results demonstrate that H1 and DNA methylation jointly maintain transcriptional homeostasis by silencing transposable elements and aberrant intragenic transcripts. Such functionality plausibly explains why DNA methylation, a well-known mutagen, has been maintained within coding sequences of crucial plant and animal genes. Bisulfite and RNA sequencing was performed using wt, h1, met1, h1met1, h1;met1 +/- plants (5-6 replicates, one sample for h1;met1 +/-) to examine the effect of DNA methylation and histone H1 loss on RNA expression. Decap-seq was performed using wt, met1, h1met1, and h1;met1+/- plants (2-3 replicates, one sample for h1;met1+/-). H1 ChAP and H3K9me2 ChIP sequencing: pH1-H1-BLRP transgenic plants were generated in wt and met1 plants to monitor H1 distribution change. Antibody against H3K9me2 (Abcam, cat. No. AB1220) was used to enrich chromatin bound to modified histones in wt and met1 plants.