Title: Chromoanagenesis from radiation-induced genome damage in Populus

Journal Article · · PLoS Genetics

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.

Research Organization:
Univ. of California, Davis, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
SC0007183
OSTI ID:
1850992
Journal Information:
PLoS Genetics, Journal Name: PLoS Genetics Journal Issue: 8 Vol. 17; ISSN 1553-7404
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

References (32)

Radiation induced mutations for plant selection journal June 1995
Chromoplexy: A New Category of Complex Rearrangements in the Cancer Genome journal May 2013
Massive Genomic Rearrangement Acquired in a Single Catastrophic Event during Cancer Development journal January 2011
Chromosome Catastrophes Involve Replication Mechanisms Generating Complex Genomic Rearrangements journal September 2011
Criteria for Inference of Chromothripsis in Cancer Genomes journal March 2013
Punctuated Evolution of Prostate Cancer Genomes journal April 2013
DNA breaks and chromosome pulverization from errors in mitosis journal January 2012
Chromoanagenesis and cancer: mechanisms and consequences of localized, complex chromosomal rearrangements journal November 2012
Chromothripsis and cancer: causes and consequences of chromosome shattering journal September 2012
Physiological status of plant tissue affects the frequency and types of mutations induced by carbon-ion irradiation in Arabidopsis journal January 2018
Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri journal March 2018
A comprehensive genomic scan reveals gene dosage balance impacts on quantitative traits in Populus trees journal June 2019
Fast and accurate short read alignment with Burrows-Wheeler transform journal May 2009
The Sequence Alignment/Map format and SAMtools journal June 2009
Gametocidal Genes Induce Chromosome Breakage in the Interphase Prior to the First Mitotic Cell Division of the Male Gametophyte in Wheat journal June 1998
Chromoanasynthesis: another way for the formation of complex chromosomal abnormalities in human reproduction journal July 2018
An ion beam–induced Arabidopsis mutant with marked chromosomal rearrangement journal June 2017
Genome-wide analysis of mutations in mutant lineages selected following fast-neutron irradiation mutagenesis of Arabidopsis thaliana journal April 2012
Catastrophic Unbalanced Genome Rearrangements Cause Somatic Loss of Berry Color in Grapevine journal August 2017
Efficient Genome-Wide Detection and Cataloging of EMS-Induced Mutations Using Exome Capture and Next-Generation Sequencing journal April 2014
A System for Dosage-Based Functional Genomics in Poplar journal August 2015
Genome-Scale Sequence Disruption Following Biolistic Transformation in Rice and Maize journal January 2019
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) journal September 2006
Mechanisms generating cancer genome complexity from a single cell division error journal April 2020
The Mechanism of Double-Strand DNA Break Repair by the Nonhomologous DNA End-Joining Pathway journal June 2010
BLAST+: architecture and applications journal January 2009
Mechanisms of chromosomal rearrangement in the human genome journal January 2010
Chromosome-breakage genomic instability and chromothripsis in breast cancer journal January 2014
Chromoanagenesis: a piece of the macroevolution scenario journal January 2020
Phenotypic Consequences of Aneuploidy in Arabidopsis thaliana journal December 2010
Chromothripsis-like chromosomal rearrangements induced by ionizing radiation using proton microbeam irradiation system journal February 2016
Frequency, Origins, and Evolutionary Role of Chromosomal Inversions in Plants journal March 2020