1. Chromosomes and Gene Expression
  2. Genetics and Genomics
Download icon

Spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres

  1. Krishnendu Guin
  2. Yao Chen
  3. Radha Mishra
  4. Siti Rawaidah B M Muzaki
  5. Bhagya C Thimmappa
  6. Caoimhe E O'Brien
  7. Geraldine Butler
  8. Amartya Sanyal  Is a corresponding author
  9. Kaustuv Sanyal  Is a corresponding author
  1. Jawaharlal Nehru Centre for Advanced Scientific Research, India
  2. Nanyang Technological University, Singapore
  3. University College Dublin, Ireland
  4. Conway Institute, University College Dublin, Ireland
Research Article
  • Cited 3
  • Views 1,358
  • Annotations
Cite this article as: eLife 2020;9:e58556 doi: 10.7554/eLife.58556

Abstract

Centromeres of Candida albicans form on unique and different DNA sequences but a closely related species, Candida tropicalis, possesses homogenized inverted repeat (HIR)-associated centromeres. To investigate the mechanism of centromere type transition, we improved the fragmented genome assembly and constructed a chromosome-level genome assembly of C. tropicalis by employing PacBio sequencing, chromosome conformation capture sequencing (3C-seq), chromoblot, and genetic analysis of engineered aneuploid strains. Further, we analyzed the 3D genome organization using 3C-seq data, which revealed spatial proximity among the centromeres as well as telomeres of seven chromosomes in C. tropicalis. Intriguingly, we observed evidence of inter-centromeric translocations in the common ancestor of C. albicans and C. tropicalis. Identification of putative centromeres in closely related Candida sojae, Candida viswanathii and Candida parapsilosis indicates loss of ancestral HIR-associated centromeres and establishment of evolutionary new centromeres (ENCs) in C. albicans. We propose that spatial proximity of the homologous centromere DNA sequences facilitated karyotype rearrangements and centromere type transitions in human pathogenic yeasts of the CUG-Ser1 clade.

Article and author information

Author details

  1. Krishnendu Guin

    Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6957-465X
  2. Yao Chen

    Nanyang Technological University, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  3. Radha Mishra

    Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  4. Siti Rawaidah B M Muzaki

    Nanyang Technological University, Singapore, Singapore
    Competing interests
    The authors declare that no competing interests exist.
  5. Bhagya C Thimmappa

    Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  6. Caoimhe E O'Brien

    University College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  7. Geraldine Butler

    Conway Institute, University College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  8. Amartya Sanyal

    Nanyang Technological University, Singapore, Singapore
    For correspondence
    asanyal@ntu.edu.sg
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2109-4478
  9. Kaustuv Sanyal

    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

Council of Scientific and Industrial Research (Shyama Prasad Mukherjee Fellowship 07/733(0181)/2013-EMR-I)

  • Krishnendu Guin

Department of Biotechnology , Ministry of Science and Technology (BT/PR27490/Med/29/1323/2018)

  • Kaustuv Sanyal

Ministry of Education - Singapore (RG39/18)

  • Amartya Sanyal

Department of Biotechnology , Ministry of Science and Technology

  • Kaustuv Sanyal

Nanyang Technological University (Nanyang Assistant Professorship grant)

  • Amartya Sanyal

Department of Biotechnology , Ministry of Science and Technology

  • Kaustuv Sanyal

Department of Biotechnology , Ministry of Science and Technology

  • Kaustuv Sanyal

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

Reviewing Editor

  1. Job Dekker, University of Massachusetts Medical School, United States

Publication history

  1. Received: May 4, 2020
  2. Accepted: May 22, 2020
  3. Accepted Manuscript published: May 29, 2020 (version 1)
  4. Version of Record published: June 12, 2020 (version 2)
  5. Version of Record updated: June 30, 2020 (version 3)

Copyright

© 2020, Guin 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.

Metrics

  • 1,358
    Page views
  • 168
    Downloads
  • 3
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

  1. Further reading

Further reading

    1. Chromosomes and Gene Expression
    Matthew G Thompson et al.
    Research Article

    Viral infection induces the expression of numerous host genes that impact the outcome of infection. Here we show that infection of human lung epithelial cells with Influenza A virus (IAV) also induces a broad program of alternative splicing of host genes. While these splicing-regulated genes are not enriched for canonical regulators of viral infection, we find that many of these genes do impact replication of IAV. Moreover, in several cases, specific inhibition of the IAV-induced splicing pattern also attenuates viral infection. We further show that approximately a quarter of the IAV-induced splicing events are regulated by hnRNP K, a host protein required for efficient splicing of the IAV M transcript in nuclear speckles. Finally, we find an increase in hnRNP K in nuclear speckles upon IAV infection, which may alter accessibility of hnRNP K for host transcripts thereby leading to a program of host splicing changes that promote IAV replication.

    1. Chromosomes and Gene Expression
    2. Genetics and Genomics
    Konstantin Riege et al.
    Tools and Resources

    The transcription factor p53 is the best-known tumor suppressor, but its sibling p63 is a master regulator of epidermis development and a key oncogenic driver in squamous cell carcinomas (SCC). Despite multiple gene expression studies becoming available, the limited overlap of reported p63-dependent genes has made it difficult to decipher the p63 gene regulatory network. Particularly, analyses of p63 response elements differed substantially among the studies. To address this intricate data situation, we provide an integrated resource that enables assessing the p63-dependent regulation of any human gene of interest. We use a novel iterative de novo motif search approach in conjunction with extensive ChIP-seq data to achieve a precise global distinction between p53 and p63 binding sites, recognition motifs, and potential co-factors. We integrate these data with enhancer:gene associations to predict p63 target genes and identify those that are commonly de-regulated in SCC representing candidates for prognosis and therapeutic interventions.