Dynamics of extrachromosomal circular DNA in rice

Abstract

The genome’s dynamic nature, exemplified by elements like extrachromosomal circular DNA (eccDNA), is crucial for biodiversity and adaptation. Yet, the role of eccDNA in plants, particularly rice, remains underexplored. Here, we identify 25,598 eccDNAs, unveiling the widespread presence of eccDNA across six rice tissues and revealing its formation as a universal and random process. Interestingly, we discover that direct repeats play a pivotal role in eccDNA formation, pointing to a unique origin mechanism. Despite eccDNA’s prevalence in coding sequences, its impact on gene expression is minimal, implying its roles beyond gene regulation. We also observe the association between eccDNA’s formation and minor chromosomal deletions, providing insights of its possible function in regulating genome stability. Further, we discover eccDNA specifically accumulated in rice leaves, which may be associated with DNA damage caused by environmental stressors like intense light. In summary, our research advances understanding of eccDNA’s role in the genomic architecture and offers valuable insights for rice cultivation and breeding.

Unveiling eccDNA Dynamics in Rice: Insights into Adaptation to Nutritional Stress

“…Although a few eccDNAs were over 37 kb, the average size across all the treatments was approximately 500 bp. This size distribution was similar to that observed in other organisms, such as human cells 11 , Arabidopsis 15 , and the short-read sequencing analysis from rice 17 (Supplementary Fig. 4a).…”

“…1a), consistent with the study on rice eccDNAs using short Illumina reads 17 . However, likely due to the analysis of samples subjected to nutritional treatment and the long read sequencing platform used, we identi ed a 4-fold higher number of distinct eccDNAs in rice shoots (96757) than that previously reported (22183) 17 . Additionally, we observed a high percentage of eccDNAs mapping to CDS regions (Fig.…”

“…Our Nanopore sequencing data uncover their size distribution, with most eccDNAs ranging between 200 bp and 600 bp (Fig. 1a), consistent with the study on rice eccDNAs using short Illumina reads 17 . However, likely due to the analysis of samples subjected to nutritional treatment and the long read sequencing platform used, we identi ed a 4-fold higher number of distinct eccDNAs in rice shoots (96757) than that previously reported (22183) 17 .…”

“…The presence of eccDNAs has been reported in several plant species 14 , including Arabidopsis (Arabidopsis thaliana) 15 , sugarcane (Saccharum o cinarum) 16 , and rice (Oryza sativa) 17 . A notable example of the functional role of eccDNAs in plants is glyphosate resistance 18 in the noxious weed Amaranthus palmeri, which is due to eccDNA increased copy number of the gene encoding the target enzyme of this herbicide, 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) 19 .…”

“…High TE-derived eccDNA loads in Arabidopsis ddm1 mutants suggested a role of eccDNAs in genome instability by altering DNA repair pathways 23 . Recently, dynamic analysis in rice also revealed important information on eccDNA origin 17 . Although increasing data on the functional role of eccDNAs on adaptive mechanisms and genome evolution has been recently reported, the role of eccDNAs in plant adaptation to environmental pressures, including nutritional stresses, remains largely unexplored 7 .…”