Abstract
The repeated rDNA array gives rise to the nucleolus, an organelle that is central to cellular processes as varied as stress response, cell cycle regulation, RNA modification, cell metabolism, and genome stability. The rDNA array is also responsible for the production of more than 70% of all cellular RNAs (the ribosomal RNAs). The rRNAs are produced from two sets of loci: the 5S rDNA array resides exclusively on human chromosome 1 while the 45S rDNA arrays reside on the short arm of five human acrocentric chromosomes. These critical genome elements have remained unassembled and have been excluded from all Hi-C analyses to date. Here we built the first high resolution map of 5S and 45S rDNA array contacts with the rest of the genome combining over 15 billion Hi-C reads from several experiments. The data enabled sufficiently high coverage to map rDNA-genome interactions with 1MB resolution and identify rDNA-gene contacts. The map showed that the 5S and 45S arrays display preferential contact at common sites along the genome but are not themselves sufficiently close to yield 5S-45S Hi-C contacts. Ribosomal DNA contacts are enriched in segments of closed, repressed, and late replicating chromatin, as well as CTCF binding sites. Finally, we identified functional categories whose dispersed genes coalesced in proximity to the rDNA arrays or instead avoided proximity with the rDNA arrays. The observations further our understanding of the spatial localization of rDNA arrays and their contribution to the architecture of the cell nucleus.
Highlights
Ribosomal RNAs are essential components of the cell, and are encoded in the 5S and 45S ribosomal DNA arrays of higher eukaryotes [1,2,3,4]
The repeated ribosomal DNA array gives rise to the nucleolus, an organelle that is involved in key cellular processes such as stress response, cell cycle regulation, RNA modification, and production of more than 70% of all cellular RNAs
We mined 5,356,990,189 high quality Hi-C reads in LCL to identify 13,528,436 reads with at least one end mapped to the 45S ribosomal DNA (rDNA) and 105,147 reads with at least one end mapped to the 5S rDNA (S1 and S2 Tables)
Summary
Ribosomal RNAs (rRNAs) are essential components of the cell, and are encoded in the 5S and 45S ribosomal DNA (rDNA) arrays of higher eukaryotes [1,2,3,4]. The 5S rDNA array resides on chromosome 1 and encodes the 5S rRNA, whereas the 45S rDNA array resides on five human acrocentric chromosomes and encodes the 18S, 5.8S, and 28S rRNA components of the ribosome [5,6,7]. Proximity to the nucleolus can in some cases promote inactivation of certain RNA polymerase II transcribed genes [9], the observation has not been systematically tested across the genome. Studies of nuclear architecture have largely excluded analyses of spatial interactions with the 5S and 45S rDNA arrays
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