Chromoanagenesis from radiation-induced genome damage in Populus

Abstract

Chromoanagenesis is a genomic catastrophe that results in chromosomal shattering and reassembly. These extreme single chromosome events were first identified in cancer, and have since been observed in other systems, but have so far only been formally documented in plants in the context of haploid induction crosses. The frequency, origins, consequences, and evolutionary impact of such major chromosomal remodeling in other situations remain obscure. Here, we demonstrate the occurrence of chromoanagenesis in poplar (Populus sp.) trees produced from gamma-irradiated pollen. Specifically, in this population of siblings carrying indel mutations, two individuals exhibited highly frequent copy number variation (CNV) clustered on a single chromosome, one of the hallmarks of chromoanagenesis. Using short-read sequencing, we confirmed the presence of clustered segmental rearrangement. Independently, we identified and validated novel DNA junctions and confirmed that they were clustered and corresponded to these rearrangements. Our reconstruction of the novel sequences suggests that the chromosomal segments have reorganized randomly to produce a novel rearranged chromosome but that two different mechanisms might be at play. Our results indicate that gamma irradiation can trigger chromoanagenesis, suggesting that this may also occur when natural or induced mutagens cause DNA breaks. We further demonstrate that such events can be tolerated in poplar, and even replicated clonally, providing an attractive system for more in-depth investigations of their consequences.

Chromoanagenesis in the asy1 meiotic mutant of Arabidopsis

“…Statistical analysis suggested that breakpoint loci were significantly associated with gene-rich regions for both 1kb and 10kb window sizes (p-value < 0.001) (Fig.1F, 1G). These results are consistent with previously documented chromoanagenesis events in plants, which also exhibited higher than expected frequency of breakpoints occurrence in genic regions [7, 10]. In addition to gene density, we also characterized the potential enrichment of other genomic features, including chromatin states, transposable elements, or replication origins.…”

“…The annotation files of various genomic features of Arabidopsis thaliana (TAIR10) was acquired from the GitHub repository (https://github.com/KorfLab/FRAG_project) associated with the breakpoint analysis previously performed on aneuploid Arabidopsis [7]. Statistical analysis was performed as previously described [10]. The megaspore mother cell from asy1 homozygous mutant exhibits chromosome mis-segregation during female meiosis.…”

Detection and characterization of genome-wide mutations in M1 vegetative cells of gamma-irradiated Arabidopsis

“…These results also demonstrated that analyzing the M1 genome for mutations is conducive to detecting and characterizing large DNA alterations. Very recently, Guo et al (2021) [ 41 ] conducted WGS analysis on F1 poplar plants obtained with gamma-irradiated pollen. Although the authors focused on specific chromosomes with highly complex segmental rearrangements formed by “chromoanagenesis [ 42 ]”, they detected a number of Mb-ordered deletions and duplications, implying that their system, similar to our own, was well suited for detecting large DNA alterations.…”

Frequency and Spectrum of Mutations Induced by Gamma Rays Revealed by Phenotype Screening and Whole-Genome Re-Sequencing in Arabidopsis thaliana

“…The genome mutation profile is another important index for evaluating the mutagenic effects of gamma rays. In the last 10 years, the availability of next-generation sequencing (NGS) technology has greatly propelled the understanding of the genome-wide characteristics of mutations induced by gamma rays [ 10 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 ]. The first attempt was made by Henry.…”

“…The insertions and deletions (InDels) mutations were detected in approximately 500 F 1 seedlings produced by pollinating Populus deltoides with gamma rays-irradiated Populus nigra pollen based on HiSeq2000 and HiSeq2500 platform [ 30 ]. Very recently, using whole-genome sequencing analysis, they have demonstrated that gamma rays can trigger chromoanagenesis in poplar plants [ 29 ]. Datta established a low-coverage whole-genome sequencing approach to recover the large genomic InDels (ranging from 0.3 to 3.8 Mb) and copy number variation caused by gamma rays in triploid bananas [ 39 ].…”