Catastrophic chromosomal restructuring during genome elimination in plants

  1. Ek Han Tan
  2. Isabelle M Henry
  3. Maruthachalam Ravi
  4. Keith R Bradnam
  5. Terezie Mandakova
  6. Mohan P A Marimuthu
  7. Ian Korf
  8. Martin A Lysak
  9. Luca Comai  Is a corresponding author
  10. Simon W L Chan
  1. University of California, Davis, United States
  2. Indian Institute of Science Education and Research, India
  3. Masaryk University, Czech Republic

Abstract

Genome instability is associated with mitotic errors and cancer. This phenomenon can lead to deleterious rearrangements, but also genetic novelty, and many questions regarding its genesis, fate and evolutionary role remain unanswered. Here, we describe extreme chromosomal restructuring during genome elimination, a process resulting from hybridization of Arabidopsis plants expressing different centromere histones H3. Shattered chromosomes are formed from the genome of the haploid inducer, consistent with genomic catastrophes affecting a single, laggard chromosome compartmentalized within a micronucleus. Analysis of breakpoint junctions implicates breaks followed by repair through non-homologous end joining (NHEJ) or stalled fork repair. Furthermore, mutation of required NHEJ factor DNA Ligase 4 results in enhanced haploid recovery. Lastly, heritability and stability of a rearranged chromosome suggest a potential for enduring genomic novelty. These findings provide a tractable, natural system towards investigating the causes and mechanisms of complex genomic rearrangements similar to those associated with several human disorders.

Article and author information

Author details

  1. Ek Han Tan

    Department of Plant Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Isabelle M Henry

    Department of Plant Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Maruthachalam Ravi

    School of Biology, Indian Institute of Science Education and Research, Thiruvananthapuram, India
    Competing interests
    The authors declare that no competing interests exist.
  4. Keith R Bradnam

    Genome Center, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Terezie Mandakova

    Central European Institute of Technology, Masaryk University, Brno, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  6. Mohan P A Marimuthu

    Department of Plant Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Ian Korf

    Genome Center, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Martin A Lysak

    Central European Institute of Technology, Masaryk University, Brno, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  9. Luca Comai

    Department of Plant Biology, University of California, Davis, Davis, United States
    For correspondence
    lcomai@ucdavis.edu
    Competing interests
    The authors declare that no competing interests exist.
  10. Simon W L Chan

    Department of Plant Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Bernard de Massy, Institute of Human Genetics, CNRS UPR 1142, France

Publication history

  1. Received: January 16, 2015
  2. Accepted: May 14, 2015
  3. Accepted Manuscript published: May 15, 2015 (version 1)
  4. Version of Record published: June 10, 2015 (version 2)
  5. Version of Record updated: April 19, 2017 (version 3)

Copyright

© 2015, Tan et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Ek Han Tan
  2. Isabelle M Henry
  3. Maruthachalam Ravi
  4. Keith R Bradnam
  5. Terezie Mandakova
  6. Mohan P A Marimuthu
  7. Ian Korf
  8. Martin A Lysak
  9. Luca Comai
  10. Simon W L Chan
(2015)
Catastrophic chromosomal restructuring during genome elimination in plants
eLife 4:e06516.
https://doi.org/10.7554/eLife.06516

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