Genome-wide Nucleosome Specificity and Directionality of Chromatin Remodelers

How chromatin remodelers cooperate to organize nucleosomes around the start and end of genes is not known. We determined the genome-wide binding of remodeler complexes SWI/SNF, RSC, ISW1a, ISW1b, ISW2, and INO80 to individual nucleosomes in Saccharomyces, and determined their functional contributions to nucleosome positioning through deletion analysis. We applied ultra-high-resolution ChIP-exo mapping to Isw2 to determine its subnucleosomal orientation and organization on a genomic scale. Remodelers interacted with selected nucleosome positions relative to the start and end of genes and produced net directionality in moving nucleosomes either away or toward nucleosome-free regions at the 5′ and 3′ ends of genes. Isw2 possessed a subnucleosomal organization in accord with biochemical and crystallographic-based models that place its linker binding region within promoters and abutted against Reb1-bound locations. Together, these findings reveal a coordinated position-specific approach taken by remodelers to organize genic nucleosomes into arrays. [Display omitted] ► Nucleosome-free regions organize the directional packing of nucleosomal arrays ► ISWI and SWI/SNF remodelers engage in a positional tug-of-war with nucleosome arrays ► ISW1a and ISW2 move nucleosomes toward NFRs, others move nucleosomes away The nucleosome binding preferences of six chromatin remodeling complexes in yeast suggests they work in concert at subsets of genes, targeting specific nucleosomes positioned near the starts and ends of the genes. The findings also indicate that nucleosome-free regions at transcription start sites act as focal points for directional packing of nucleosomes.