Unusual combinatorial involvement of poly-A/T tracts in organizing genes and chromatin in Dictyostelium
- Gue Su Chang1,
- Angelika A. Noegel2,
- Travis N. Mavrich1,
- Rolf Müller2,
- Lynn Tomsho1,
- Elissa Ward1,
- Marius Felder3,
- Cizhong Jiang1,6,
- Ludwig Eichinger4,
- Gernot Glöckner5,
- Stephan C. Schuster1 and
- B. Franklin Pugh1,7
- 1Center for Eukaryotic Gene Regulation and Center for Comparative Genomics and Bioinformatics, Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania 16802, USA;
- 2Institute of Biochemistry I, Medical Faculty, Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), 50931 Koeln, Germany;
- 3Genome Analysis, Fritz-Lipmann-Institute, FLI, D-07745 Jena, Germany;
- 4Center for Biochemistry, Institute of Biochemistry I, Medical Faculty, University of Cologne, 50931 Cologne, Germany;
- 5Leibniz-Institute of Freshwater Ecology and Inland Fisheries, IGB, D-12587 Berlin, Germany
Abstract
Dictyostelium discoideum is an amoebozoa that exists in both a free-living unicellular and a multicellular 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 II. Indeed, we find a strong phylogenetic relationship between the presence of the NELF pausing factor and positioning of the +1 nucleosome. Pausing and +1 nucleosome positioning may have coevolved in animals.
Footnotes
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↵7 Corresponding author.
E-mail bfp2{at}psu.edu.
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.131649.111.
- Received September 7, 2011.
- Accepted March 7, 2012.
This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 3.0 Unported License), as described at http://creativecommons.org/licenses/by-nc/3.0/.