Correlation Of Nucleosome Positioning With Transcription And DNA Methylation In Maize

Nucleosomes are the fundamental units of chromatin in eukaryotic cells, and play a critical role in gene regulation via modulating the DNA accessibility for regulatory proteins. It is generally accepted that pattern of nucleosome organization along the chromosome have substantial impact on the transcription of genes, but the exact role is still poorly understood. Besides influencing gene transcription, numerous lines of evidence suggest nucleosome also has effect on DNA methylation, although the mechanism of this effect remains elusive.Maize (Zea mays) is one of the most important crops in the world and a model system for plant genomics research. Here, we obtained genome-wide maps of nucleosome occupancy in both shoot and endosperm of maize by sequencing the nucleosomal DNA generated with micrococcal nuclease (MNase) digestion. The average nucleosome repeat length for shoot is ～3 bp longer than that for endosperm. Comparison of nucleosome organization in shoot and endosperm revealed that gene activation was accompanied with preferential nucleosome loss from promoter and shift of first nucleosomes downstream of transcription start site (+1 nucleosome) and upstream of transcription termination site (-1 nucleosome). Furthermore, we found intrinsically DNA-encoded nucleosome organization is correlated with the expressional tissue-specificity. Compared to tissue-specific, constitutive genes showed more pronounced 5’and 3’nucleosome depleted regions, as well as further+1 and-1 nucleosomes relative to transcription start site and transcription termination site, respectively. These characteristics can also facilitate gene expression, but this effect was not reflected in ultimate translational level as the translational efficiency of tissue-specific genes is higher than constitutive genes. Our results suggested the central role of intrinsically DNA-encoded nucleosome organization is to program the expressional tissue-specificity of genes, rather than gene expression level.Combined with MethylC-seq data, we also investigated the relationship between nucleosome positioning and DNA methylation. Overall, the methylation level of nucleosome core DNA is positively correlated with that of flanking DNA. Moreover, the nucleosome flanking DNA is enriched for CHG and CHH contexts DNA methylation in all three species, while the CG context DNA methylation is enriched in nucleosome-bound DNA in maize, but enriched in flanking DNA in rice and Arabidopsis. Intrestingly, some of nucleosomes display remarkable CG context DNA methylation difference on two sides of nucleosme center, and this nucleosomes are enriched in non-transposons region. The result implies important role of DNA methylation difference in single nucleosome. We also found nucleosomes are depleted in the flanking of differentially methylated regions between shoot and endosperm in maize, and the degree of depletion enhanced with the increase of DNA methylation difference, indicating the nucleosme might paly a role in the process of DNA demethylation.In this study, we also analyzed the time-series transcriptome data of maize embryo, endosperm and whole seed tissues, and found at least 26,105 genes, including 1,614 transcription factors, are required to program maize seed development. Combined with the published RNA-seq data, we further identified 1,258 seed-specific genes, including 418 genes displaying specificly expressed in different compartments of seed. The results should help elucidate key mechanisms and regulatory networks that underlie seed development.