The ancestral chromatin landscape of land plants

Abstract

SummaryIn mammals and flowering plants chromatin is modified by DNA methylation (5mC) and methylation of lysine residues of the N-terminal tail of histone H3 that reflect transcriptional activity in three chromosomal domains: euchromatin comprising transcribed genes, facultative heterochromatin comprising repressed genes, and constitutive heterochromatin comprising transposons. Yet recent studies have shown that the correlation between chromatin modifications and transcriptional regulation of transposons and genes vary among different lineages of eukaryotes including the bryophytes that diverged from vascular plants 510-480 mya. The monophyletic bryophytes comprise mosses, liverworts and hornworts. The chromatin landscapes of mosses and liverworts are different, leaving open the question regarding the identity of the chromatin landscape of all bryophytes.Here we assembled the chromatin landscape of the model hornwortAnthoceros agrestis. By comparing chromatin landscapes between mosses, liverworts and hornworts we define the common chromatin landscape of the ancestor of extant bryophytes. The constitutive heterochromatin of bryophytes is characterized by the absence of gene body DNA methylation, low levels of non-CG DNA methylation and the absence of segregation of transposons in a few well defined chromosomal compartments. In addition, whereas histone modifications of euchromatin and facultative heterochromatin are primarily associated with genes in angiosperms and mosses, nearly half of the hornwort transposons are associated with facultative heterochromatin and euchromatin. Hence the ancestral genome of bryophytes was likely a patchwork of interspersed small units of euchromatin, facultative and constitutive heterochromatin. Each unit contained a few transposons and genes that share the same chromatin state. We propose that in bryophytes, this specific type of genome organization prevented the recruitment of transposons to form constitutive heterochromatin around point centromeres observed in the genomes of angiosperms.

Transposons repressed by H3K27me3 were co-opted as cis-regulatory elements of H3K27me3 controlled protein coding genes during evolution of plants

“…This enrichment of LTR TE families was also observed in TEs longer than 500 bp (total 26,070 TEs including 923 intact TEs) (Figure S1E) and thus we analyzed separately longer TEs and shorter TEs. Using chromatin immunoprecipitation coupled with DNA sequencing (ChIP-seq), we obtained genomic profiles of five histone post translational modifications (PTMs) (H3K4me3, H3K36me3, H3K9me1, H3K27me1 and H3K27me3) and H3 from four week old vegetative tissue of A. agrestis (see 23 for a general overview of the chromatin of A. agrestis ). We performed k-means clustering of chromatin marks over TEs, and defined five major clusters of TEs showing different chromatin environments (Figure 2A).…”

“…Details for preparation for ChIP-seq libraries of A. agrestis are in 23 . Chip-seq data of C. merolae were downloaded from the Gene expression omnibus of NCBI under the series GSE93913.…”