Abstract
Extrachromosomal circular DNA (eccDNA) elements of chromosomal origin are known to be common in a number of eukaryotic species. However, it remains to be addressed whether genomic features such as genome size, the load of repetitive elements within a genome, and/or animal physiology affect the number of eccDNAs. Here, we investigate the distribution and numbers of eccDNAs in a condensed and less repeat-rich genome compared with the human genome, using Columba livia domestica (domestic rock pigeon) as a model organism. By sequencing eccDNA in blood and breast muscle from three pigeon breeds at various ages and with different flight behavior, we characterize 30,000 unique eccDNAs. We identify genomic regions that are likely hotspots for DNA circularization in breast muscle, including genes involved in muscle development. We find that although eccDNA counts do not correlate with the biological age in pigeons, the number of unique eccDNAs in a nonflying breed (king pigeons) is significantly higher (9-fold) than homing pigeons. Furthermore, a comparison between eccDNA from skeletal muscle in pigeons and humans reveals ∼9-10 times more unique eccDNAs per human nucleus. The fraction of eccDNA sequences, derived from repetitive elements, exist in proportions to genome content, that is, human 72.4% (expected 52.5%) and pigeon 8.7% (expected 5.5%).Overall, our results support that eccDNAs are common in pigeons, that the amount of unique eccDNA types per nucleus can differ between species as well as subspecies, and suggest that eccDNAs from repeats are found in proportions relative to the content of repetitive elements in a genome.
Highlights
It has been shown that eukaryotic nuclear DNA can excise from chromosomes and form circular molecules that are retained within the cell
DNA was collected from pigeons of different age: 6 weeks up to 8 years, and different breeds: the highly active homing pigeon (n 1⁄4 11, flying; n 1⁄4 4, preflying), the flightless king pigeon (n 1⁄4 10, caged), and the Danish Suabian breed with poor flight ability (n 1⁄4 2, caged)
High confidence Extrachromosomal circular DNA (eccDNA) were recorded based on following criteria: 1) a minimum of two sequencing reads identified at the circular DNA junctions, 2) the locus had more than 80% read coverage, and 3) at least 10% of the region was covered by reads with high mapping quality ($unique sequence)
Summary
It has been shown that eukaryotic nuclear DNA can excise from chromosomes and form circular molecules that are retained within the cell These extrachromosomal circular DNA (eccDNA) elements can, in certain cases, replicate and propagate in cells as semistable genetic elements (Kanda et al 2001; Gresham et al 2010; Vogt et al 2014; Meng et al 2015; Shoura et al 2017; Turner et al 2017) and have so far been found in all eukaryotic species studied to date (Gaubatz 1990; Paulsen et al 2018 for reviews). Evol. 12(2):3762–3777. doi:10.1093/gbe/evz281 Advance Access publication December 27, 2019
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