Chromatin inheritance upon Zeste-mediated Brahma recruitment at a minimal cellular memory module

Polycomb group and trithorax group proteins maintain the memory of repressed and active chromatin states by regulating chromatin of their target genes via DNA sequences termed Polycomb- and trithorax response elements. Since these elements often overlap and are able to convey the memory of both silent and active chromatin through cell division, they were also defined as cellular memory modules (CMMs). We identify here a minimal CMM of 219 bp from the Drosophila Fab-7 region that regulates the homeotic gene Abdominal-B. This CMM conveys the inheritance of active chromatin states induced by an embryonic pulse of transcriptional activation via recruitment of the trithorax group proteins Trithorax (TRX) and Brahma (BRM), the Drosophila homologue of the SWI2/SNF2 ATPase involved in chromatin remodelling. Within this CMM, DNA-binding sites for the Zeste protein are necessary for the inheritance of active chromatin through Zeste-dependent recruitment of BRM, while TRX can bind the CMM even in their absence. Thus, epigenetic inheritance of active chromatin states involves the recruitment of multiple cooperative chromatin-modifying complexes at closely spaced but distinct sites within a CMM.