title: Determinants of nucleosome positioning and their influence on plant gene expression.
abstract: Nucleosome positioning influences the access of transcription factors (TFs) to their binding sites and gene expression. Studies in plant, animal, and fungal models demonstrate similar nucleosome positioning patterns along genes and correlations between occupancy and expression. However, the relationships among nucleosome positioning, cis-regulatory element accessibility, and gene expression in plants remain undefined. Here we showed that plant nucleosome depletion occurs on specific 6-mer motifs and this sequence-specific nucleosome depletion is predictive of expression levels. Nucleosome-depleted regions in Arabidopsis thaliana tend to have higher G/C content, unlike yeast, and are centered on specific G/C-rich 6-mers, suggesting that intrinsic sequence properties, such as G/C content, cannot fully explain plant nucleosome positioning. These 6-mer motif sites showed higher DNase I hypersensitivity and are flanked by strongly phased nucleosomes, consistent with known TF binding sites. Intriguingly, this 6-mer-specific nucleosome depletion pattern occurs not only in promoter but also in genic regions and is significantly correlated with higher gene expression level, a phenomenon also found in rice but not in yeast. Among the 6-mer motifs enriched in genes responsive to treatment with the defense hormone jasmonate, there are no significant changes in nucleosome occupancy, suggesting that these sites are potentially preconditioned to enable rapid response without changing chromatin state significantly. Our study provides a global assessment of the joint contribution of nucleosome occupancy and motif sequences that are likely cis-elements to the control of gene expression in plants. Our findings pave the way for further understanding the impact of chromatin state on plant transcriptional regulatory circuits.
authors.affiliation: Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824, USA;
authors.forename: Ming-Jung
authors.initials: MJ
authors.lastname: Liu
authors.affiliation: Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824, USA;
authors.forename: Alexander E
authors.initials: AE
authors.lastname: Seddon
authors.affiliation: Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824, USA;
authors.forename: Zing Tsung-Yeh
authors.initials: ZT
authors.lastname: Tsai
authors.affiliation: DOE-Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, USA;
authors.forename: Ian T
authors.initials: IT
authors.lastname: Major
authors.affiliation: Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824, USA.
authors.forename: Monique
authors.initials: M
authors.lastname: Floer
authors.affiliation: DOE-Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, USA; Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824, USA.
authors.forename: Gregg A
authors.initials: GA
authors.lastname: Howe
authors.affiliation: Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824, USA;
authors.forename: Shin-Han
authors.initials: SH
authors.lastname: Shiu
mesh_terms: D017360:Arabidopsis / Q000187:drug effects / Q000235:genetics* / Q000378:metabolism; D001482:Base Composition; D001665:Binding Sites / Q000187:drug effects; D003517:Cyclopentanes / Q000494:pharmacology; D018744:DNA, Plant / Q000737:chemistry / Q000378:metabolism*; D020869:Gene Expression Profiling / Q000379:methods; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D009707:Nucleosomes / Q000737:chemistry / Q000187:drug effects / Q000378:metabolism*; D054883:Oxylipins / Q000494:pharmacology; D050436:Regulatory Elements, Transcriptional / Q000187:drug effects
chemical_list: D003517:Cyclopentanes; D018744:DNA, Plant; D009707:Nucleosomes; D054883:Oxylipins; C011006:jasmonic acid