Unusual combinatorial involvement of poly-A/T tracts in organizing genes and chromatin in Dictyostelium

Abstract

Dictyostelium discoideum is a member of the amoebozoa that exists in both a free-living unicellular and a multi-cellular form. It is situated in a deep branch in the evolutionary tree, and is particularly noteworthy in having a very A/T-rich genome. Dictyostelium provides an ideal system to examine the extreme to which nucleotide bias may be employed in organizing promoters, genes, and nucleosomes across a genome. We find that Dictyostelium genes are demarcated precisely at their 5' ends by poly-T tracts and precisely at their 3' ends by poly-A tracts. These tracts are also associated with nucleosome-free regions, and are embedded with precisely positioned TATA boxes. Homo- and heteropolymeric tracts of A and T demarcate nucleosome border regions. Together these findings reveal the presence of a variety of functionally distinct polymeric A/T elements. Strikingly, Dictyostelium chromatin may be organized in di-nucleosome units, but is otherwise organized as in animals. This includes a +1 nucleosome in a position, that predicts the presence of a paused RNA polymerase. Indeed, we find a strong phylogenetic relationship between the presence of the NELF pausing factor and positioning of the +1 nucleosome. Pausing and nucleosome positioning may have co-evolved with animal multi-cellularity.