The ancestral chromatin landscape of land plants

Background In animals and flowering plants specific chromatin modifications define three chromosomal domains: euchromatin comprising transcribed genes, facultative heterochromatin comprising repressed genes, and constitutive heterochromatin comprising transposons. However, recent studies have shown that the correlation between chromatin modifications and transcription vary among different eukaryotic organisms including mosses and liverworts that differ from one another. Mosses and liverworts diverged from hornworts, altogether forming the lineage of bryophytes that shared a common ancestor with all land plants. We aimed to obtain chromatin landscapes in hornworts to establish synapomorphies across bryophytes. Results We mapped the chromatin landscape of the model hornwort Anthoceros agrestis. By comparing chromatin landscapes across bryophytes we defined the common chromatin landscape of the ancestor of extant bryophytes. In this group, constitutive heterochromatin was characterized by a scattered distribution across autosomes, which contrasted with the dense compartments of heterochromatin surrounding the centromeres in flowering plants. Topologically associated domains were primarily occupied by transposons with genes at their boundaries and nearly half of the hornwort transposons were associated with facultative heterochromatin and euchromatin. Conclusions Most of the features observed in hornworts are also present in liverworts but are distinct from flowering plants. Hence, the ancestral genome of bryophytes was likely a patchwork of units of euchromatin interspersed within facultative and constitutive heterochromatin and each unit contained both transposons and genes sharing the same chromatin state. We propose this genome organization was ancestral to land plants and prevented transposons from being segregated as constitutive heterochromatin around point centromeres as in flowering plants.