Chromatin Loop Anchors Are Core Structural Components of the Gene Expression Machinery in Maize
Abstract Background Three-dimensional chromatin loop structures connect regulatory elements to their target genes in regions known as anchors. In complex plant genomes, such as maize, it has been proposed that loops span heterochromatic regions marked by higher repeat content, but little is known on their spatial organization and genome-wide occurrence in relation to transcriptional activity. Results Here, ultra-deep Hi-C sequencing of maize B73 leaf tissue was combined with gene expression and open chromatin sequencing for chromatin loop discovery and correlation with transcriptional activity. Chromatin loops, made of two “anchors” flanking a loop “interior”, overlap with up to 90% of high-resolution interaction domains from a previous public maize interactome dataset. A majority of all anchors are shared between multiple loops, suggesting a highly dynamic environment, with a conserved set of anchors involved in multiple interaction networks. Chromatin loop interiors are marked by higher repeat contents than the anchors flanking them. A small fraction of high-resolution interaction anchors, fully embedded in larger chromatin loops, co-locate with active genes and putative protein-binding sites. Combinatorial analysis indicate that all anchors studied here co-locate with at least 81.5% of expressed genes and 74% of open chromatin regions. Up to 63% of all unique variants derived from a prior public maize eQTL datasets overlap with Hi-C loop anchors. Anchor annotation suggests that <7% of all loops detected from one Hi-C library are potentially devoid of any genes or regulatory elements. The overall conservation and organization of chromatin loop anchors in the maize genome suggest a loop modeling system hypothesized to resemble phase separation of repeat-rich regions. Conclusions A majority of expressed genes and open chromatin regions co-locate with a conserved set of chromatin loop anchors. The results presented here will be a useful reference to further investigate the function of chromatin loop anchors and of the formation of interaction regions in the regulation of gene expression in maize.