Chromatin states in Drosophila have been profiled by multiple groups over the last decade. Surprisingly, these studies do not agree on the fundamental organisation of chromatin, with protein-based DamID studies identifying very different active forms of chromatin to histone-mark ChIP-seq studies. While DamID studies have identified developmental states associated with Trithorax-group (TrxG) complexes and house-keeping states associated with MRG15, ChIP-seq modelling has focussed upon gene transcriptional elements that do not separate by gene ontology.
Here, combining DamID, ChIP-seq, RNA-seq and 3D genome datasets across multiple cell types, we unify protein and histone-mark data and demonstrate that fly chromatin is organised into eight principle chromatin types. We show that active states are divided by a refractory relationship between the Swi/Snf chromatin remodelling complex and MRG15/H3K36me3 into a Swi/Snf state associated with developmental genes, and a Yellow state associated with housekeeping and metabolic genes. We demonstrate the existence of a previously-undocumented form of chromatin that silences housekeeping and metabolic genes cell-type specifically. We show that the Black chromatin silent state of DamID studies, associated with Histone H1 and Lamin enrichment, is directly equivalent to the “low signal” states of ChIP-seq data, and represses the majority of developmental genes in non-terminally-differentiated cell types.
We show that through eight chromatin states, the genome is fundamentally divided along developmental and housekeeping/metabolic lines, and that this division covers not only gene bodies but enhancers, core promoters and regulatory transcription factor motifs. Our results suggest a more complex organisation of the chromatin landscape than has been previously recognised and show that at every level the genome is divided by gene function along developmental and housekeeping/metabolic roles.