Genome-Wide Prediction of Nucleosome Occupancy in Maize Reveals Plant Chromatin Structural Features at Genes and Other Elements at Multiple Scales    

Abstract

The nucleosome is a fundamental structural and functional chromatin unit that affects nearly all DNA-templated events in eukaryotic genomes. It is also a biochemical substrate for higher order, cis-acting gene expression codes and the monomeric structural unit for chromatin packaging at multiple scales. To predict the nucleosome landscape of a model plant genome, we used a support vector machine computational algorithm trained on human chromatin to predict the nucleosome occupancy likelihood (NOL) across the maize (Zea mays) genome. Experimentally validated NOL plots provide a novel genomic annotation that highlights gene structures, repetitive elements, and chromosome-scale domains likely to reflect regional gene density. We established a new genome browser (http://www.genomaize.org) for viewing support vector machine-based NOL scores. This annotation provides sequence-based comprehensive coverage across the entire genome, including repetitive genomic regions typically excluded from experimental genomics data. We find that transposable elements often displayed family-specific NOL profiles that included distinct regions, especially near their termini, predicted to have strong affinities for nucleosomes. We examined transcription start site consensus NOL plots for maize gene sets and discovered that most maize genes display a typical +1 nucleosome positioning signal just downstream of the start site but not upstream. This overall lack of a -1 nucleosome positioning signal was also predicted by our method for Arabidopsis (Arabidopsis thaliana) genes and verified by additional analysis of previously published Arabidopsis MNase-Seq data, revealing a general feature of plant promoters. Our study advances plant chromatin research by defining the potential contribution of the DNA sequence to observed nucleosome positioning and provides an invariant baseline annotation against which other genomic data can be compared.

Determinants of nucleosome positioning and their influence on plant gene expression

“…Compared to genes with lower transcript abundance, genes with higher transcript abundance tend to have lower nucleosome occupancy in NDRs and genic regions, a well-positioned nucleosome (larger differential between the peak and surrounding trough) immediately downstream from the TSS, and a characteristic occupancy pattern surrounding the transcription termination site (TTS) (Fig. 1A), which is consistent with previous studies in A. thaliana, rice, maize, and human (Valouev et al 2011;Fincher et al 2013;Li et al 2014;Wu et al 2014). Taken together, these findings indicate our nucleosome data are of comparable quality to published studies.…”

“…The nucleosome gDNA read coverage per base-referred to as the Nucleosome OCcupancy (NOC) score (see Methods)-revealed NDRs immediately upstream of TSS and a prominent +1 peak (Supplemental Fig. S1C,D), consistent with earlier studies (Yuan et al 2005;Valouev et al 2011;Fincher et al 2013;Li et al 2014;Wu et al 2014). In contrast, the naked gDNA sample did not show these patterns (Supplemental Fig.…”

“…In plants, genome-wide nucleosome positions have been determined for Arabidopsis thaliana (Chodavarapu et al 2010;Li et al 2014), rice (Oryza sativa) (Wu et al 2014), and maize (Zea mays) (Fincher et al 2013;Vera et al 2014). These studies examined the relationship between nucleosome positions and DNA methylation, known TFBSs, and gene expression (Chodavarapu et al 2010;Fincher et al 2013;Li et al 2014;Vera et al 2014;Wu et al 2014).…”

“…These studies examined the relationship between nucleosome positions and DNA methylation, known TFBSs, and gene expression (Chodavarapu et al 2010;Fincher et al 2013;Li et al 2014;Vera et al 2014;Wu et al 2014). In particular, it was shown that the nucleosome density around TSSs and within gene bodies correlates with gene expression in A. thaliana and maize Vera et al 2014).…”

The spring-loaded genome: Nucleosome redistributions are widespread, transient, and DNA-directed

“…Specifically, we compared our observed nucleosome distributions (in vivo) to the computationally predicted nucleosome occupancy scores based on DNA sequence (in silico), using a well-characterized and tested model (Gupta et al 2008;Tanaka and Nakai 2009;Fincher et al 2013). We calculated the difference of the correlation value between 24 h with the predicted model, and the correlation between 0 h with the predicted model.…”