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Loss of centromere function drives karyotype evolution in closely related Malassezia species

  1. Sundar Ram Sankaranarayanan
  2. Giuseppe Ianiri
  3. Marco A Coelho
  4. Md Hashim Reza
  5. Bhagya C Thimmappa
  6. Promit Ganguly
  7. Rakesh Netha Vadnala
  8. Sheng Sun
  9. Rahul Siddharthan
  10. Christian Tellgren-Roth
  11. Thomas L Dawson
  12. Joseph Heitman  Is a corresponding author
  13. Kaustuv Sanyal  Is a corresponding author
  1. Jawaharlal Nehru Centre for Advanced Scientific Research, India
  2. Duke University Medical Center, United States
  3. The Institute of Mathematical Sciences (HBNI), India
  4. Uppsala University, Sweden
  5. Agency for Science, Technology and Research, Singapore
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Cite this article as: eLife 2020;9:e53944 doi: 10.7554/eLife.53944

Abstract

Genomic rearrangements associated with speciation often result in chromosome number variation among closely related species. Malassezia species show variable karyotypes ranging between 6 and 9 chromosomes. Here, we experimentally identified all 8 centromeres in M. sympodialis as 3 to 5 kb long kinetochore-bound regions spanning an AT-rich core and depleted of the canonical histone H3. Centromeres of similar sequence features were identified as CENP-A-rich regions in Malassezia furfur with 7 chromosomes, and histone H3 depleted regions in Malassezia slooffiae and Malassezia globosa with 9 chromosomes each. Analysis of synteny conservation across centromeres with newly generated chromosome-level genome assemblies suggests two distinct mechanisms of chromosome number reduction from an inferred 9-chromosome ancestral state: (a) chromosome breakage followed by loss of centromere DNA and (b) centromere inactivation accompanied by changes in DNA sequence following chromosome-chromosome fusion. We propose AT-rich centromeres drive karyotype diversity in the Malassezia species complex through breakage and inactivation.

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Author details

  1. Sundar Ram Sankaranarayanan

    Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  2. Giuseppe Ianiri

    Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3278-8678
  3. Marco A Coelho

    Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Md Hashim Reza

    Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  5. Bhagya C Thimmappa

    Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  6. Promit Ganguly

    Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  7. Rakesh Netha Vadnala

    The Institute of Mathematical Sciences (HBNI), Chennai, India
    Competing interests
    The authors declare that no competing interests exist.
  8. Sheng Sun

    Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Rahul Siddharthan

    The Institute of Mathematical Sciences (HBNI), Chennai, India
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2233-0954
  10. Christian Tellgren-Roth

    Department of Immunology, Genetics and Pathology, Uppsala University, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  11. Thomas L Dawson

    Skin Research Institute Singapore, Agency for Science, Technology and Research, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  12. Joseph Heitman

    Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, United States
    For correspondence
    heitm001@duke.edu
    Competing interests
    The authors declare that no competing interests exist.
  13. Kaustuv Sanyal

    Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India
    For correspondence
    sanyal@jncasr.ac.in
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6611-4073

Funding

Tata Innovation Fellowship (BT/HRT/35/01/03/2017)

  • Kaustuv Sanyal

Department of Biotechnology , Ministry of Science and Technology (BT/INF/22/SP27679/2018)

  • Kaustuv Sanyal

National Institutes of Health (R37 award-AI39115-21; R01 award-AI50113-15)

  • Joseph Heitman

Agency for Science, Technology and Research (H18/01a0/016)

  • Thomas L Dawson

Jawaharlal Nehru Centre for Advanced Scientific Research (Graduate student fellowship)

  • Sundar Ram Sankaranarayanan

Science and Engineering Research Board (PDF/2016/002858)

  • Md Hashim Reza

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

Reviewing Editor

  1. Wolf-Dietrich Heyer, University of California, Davis, United States

Publication history

  1. Received: November 26, 2019
  2. Accepted: January 20, 2020
  3. Accepted Manuscript published: January 20, 2020 (version 1)

Copyright

© 2020, Sankaranarayanan 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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