ISWI proteins participate in the genome‐wide nucleosome distribution in Arabidopsis

Abstract

SUMMARYChromatin is a highly organized structure with repetitive nucleosome subunits. Nucleosome distribution patterns, which contain information on epigenetic controls, are dynamically affected by ATP-dependent chromatin remodeling factors (remodelers). However, whether plants have specific nucleosome distribution patterns and how plant remodelers contribute to the pattern formation are not clear. In this study we used the micrococcal nuclease digestion followed by deep sequencing (MNase-seq) assay to show the genome-wide nucleosome pattern in Arabidopsis thaliana. We demonstrated that the nucleosome distribution patterns of Arabidopsis are associated with the gene expression level, and have several specific characteristics that are different from those of animals and yeast. In addition, we found that remodelers in the A. thaliana imitation switch (AtISWI) subfamily are important for the formation of the nucleosome distribution pattern. Double mutations in the AtISWI genes, CHROMATIN REMODELING 11 (CHR11) and CHR17, resulted in the loss of the evenly spaced nucleosome pattern in gene bodies, but did not affect nucleosome density, supporting a previous idea that the primary role of ISWI is to slide nucleosomes in gene bodies for pattern formation.

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).…”

Genome-Wide Nucleosome Occupancy and Positioning and Their Impact on Gene Expression and Evolution in Plants

“…Some sequences, such as the poly(dA:dT) sequences, which are intrinsically stiff, are enriched in linker sequences (Mavrich et al, 2008a(Mavrich et al, , 2008bLocke et al, 2010;Valouev et al, 2011) and nucleosome-depleted regions, such as promoters (Segal and Widom, 2009;Raveh-Sadka et al, 2012). However, several factors can override the sequence-based nucleosome positioning, including RNA Polymerase II (Pol II) transcription, recruitment of ATP-dependent chromatin remodelers, and the presence of histone variants and histone modifications (Bell et al, 2011;Struhl and Segal, 2013;Li et al, 2014). Therefore, nucleosome occupancy and positioning are dynamic processes during development as well as in response to environmental cues.…”