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Nucleosome positioning in yeasts: methods, maps, and mechanisms

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Abstract

Eukaryotic nuclear DNA is packaged into nucleosomes. During the past decade, genome-wide nucleosome mapping across species revealed the high degree of order in nucleosome positioning. There is a conserved stereotypical nucleosome organization around transcription start sites (TSSs) with a nucleosome-depleted region (NDR) upstream of the TSS and a TSS-aligned regular array of evenly spaced nucleosomes downstream over the gene body. As nucleosomes largely impede access to DNA and thereby provide an important level of genome regulation, it is of general interest to understand the mechanisms generating nucleosome positioning and especially the stereotypical NDR-array pattern. We focus here on the most advanced models, unicellular yeasts, and review the progress in mapping nucleosomes and which nucleosome positioning mechanisms are discussed. There are four mechanistic aspects: How are NDRs generated? How are individual nucleosomes positioned, especially those flanking the NDRs? How are nucleosomes evenly spaced leading to regular arrays? How are regular arrays aligned at TSSs? The main candidates for nucleosome positioning determinants are intrinsic DNA binding preferences of the histone octamer, specific DNA binding factors, nucleosome remodeling enzymes, transcription, and statistical positioning. We summarize the state of the art in an integrative model where nucleosomes are positioned by a combination of all these candidate determinants. We highlight the predominance of active mechanisms involving nucleosome remodeling enzymes which may be recruited by DNA binding factors and the transcription machinery. While this mechanistic framework emerged clearly during recent years, the involved factors and their mechanisms are still poorly understood and require future efforts combining in vivo and in vitro approaches.

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Notes

  1. While the average +1 nucleosome position relative to the TSS is conserved across yeasts, it differs in other eukaryotes. For example, the Drosophila TSSs are often upstream of the +1 nucleosome within the NDR (Mavrich et al. 2008b).

  2. Alternative nomenclatures: canonical versus noncanonical (Jiang and Pugh 2009b), open versus covered (Cairns 2009), depleted versus occupied proximal nucleosome (DPN vs. OPN; Tirosh and Barkai 2008), and much earlier in the context of Drosophila promoters: preset versus remodeling promoters (Lu et al. 1994).

  3. The comparison of nucleosome occupancy between different data sets may be problematic (see “Comparison of different methods and the problem of nucleosome occupancy”).

  4. There is the formal possibility of species-specific intrinsic sequence preferences. However, we think this unlikely given the high conservation of the histone octamer and physiological biophysical conditions.

  5. While yeast cells show constant spacing throughout the genome, human cells vary the NRL inversely with transcription rate (Valouev et al. 2011).

  6. Alternatively, “organizing centers” (Zhang et al. 2011b) or “focal points” (Yen et al. 2012).

  7. It is quite striking that one of the oldest observations in the chromatin field, regular nucleosome spacing seen in MNase ladders, is still not explained mechanistically.

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Acknowledgments

We apologize to all colleagues whose work we could not cite because of space restrictions. This work was funded by the German Research Community (DFG) through the Collaborative Research Cluster SFB1064 and by the Bavarian State Ministry of Education and Culture, Science and the Arts through the Bavarian Research Network for Molecular Biosystems (BioSysNet).

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  1. Adolf-Butenandt-Institut, University of Munich, Schillerstr. 44, 80336, Munich, Germany

    Corinna Lieleg, Nils Krietenstein, Maria Walker & Philipp Korber

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  1. Corinna Lieleg
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Correspondence to Philipp Korber.

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Lieleg, C., Krietenstein, N., Walker, M. et al. Nucleosome positioning in yeasts: methods, maps, and mechanisms. Chromosoma 124, 131–151 (2015). https://doi.org/10.1007/s00412-014-0501-x

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