Dynamic turnover of centromeres drives karyotype evolution in Drosophila

  1. Ryan Bracewell
  2. Kamalakar Chatla
  3. Matthew J Nalley
  4. Doris Bachtrog  Is a corresponding author
  1. University of California, Berkeley, United States

Abstract

Centromeres are the basic unit for chromosome inheritance, but their evolutionary dynamics is poorly understood. We generate high-quality reference genomes for multiple Drosophila obscura group species to reconstruct karyotype evolution. All chromosomes in this lineage were ancestrally telocentric and the creation of metacentric chromosomes in some species was driven by de novo seeding of new centromeres at ancestrally gene-rich regions, independently of chromosomal rearrangements. The emergence of centromeres resulted in a drastic size increase due to repeat accumulation, and dozens of genes previously located in euchromatin are now embedded in pericentromeric heterochromatin. Metacentric chromosomes secondarily became telocentric in the pseudoobscura subgroup through centromere repositioning and a pericentric inversion. The former (peri)centric sequences left behind shrunk dramatically in size after their inactivation, yet contain remnants of their evolutionary past, including increased repeat-content and heterochromatic environment. Centromere movements are accompanied by rapid turnover of the major satellite DNA detected in (peri)centromeric regions.

Data availability

All sequencing data and assemblies have been deposited in GenBank (see Table S1 for all data and accession numbers).

The following data sets were generated

Article and author information

Author details

  1. Ryan Bracewell

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Kamalakar Chatla

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Matthew J Nalley

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Doris Bachtrog

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    dbachtrog@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9724-9467

Funding

National Institutes of Health (R01GM076007)

  • Doris Bachtrog

National Institutes of Health (R01 GM101255)

  • Doris Bachtrog

National Institutes of Health (R01GM093182)

  • Doris Bachtrog

National Institutes of Health (5F32GM123764-02)

  • Ryan Bracewell

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Steven Henikoff, Fred Hutchinson Cancer Research Center, United States

Publication history

  1. Received: June 3, 2019
  2. Accepted: September 12, 2019
  3. Accepted Manuscript published: September 16, 2019 (version 1)
  4. Version of Record published: October 16, 2019 (version 2)

Copyright

© 2019, Bracewell 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. Ryan Bracewell
  2. Kamalakar Chatla
  3. Matthew J Nalley
  4. Doris Bachtrog
(2019)
Dynamic turnover of centromeres drives karyotype evolution in Drosophila
eLife 8:e49002.
https://doi.org/10.7554/eLife.49002

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