Orderly assembly underpinning built-in asymmetry in the yeast centrosome duplication cycle requires cyclin-dependent kinase

  1. Marco Geymonat
  2. Qiuran Peng
  3. Zhiang Guo
  4. Zulin Yu
  5. Jay R Unruh
  6. Sue L Jaspersen  Is a corresponding author
  7. Marisa Segal  Is a corresponding author
  1. University of Cambridge, United Kingdom
  2. Stowers Institute for Medical Research, United States

Abstract

Asymmetric astral microtubule organization drives the polarized orientation of the S. cerevisiae mitotic spindle and primes the invariant inheritance of the old spindle pole body (SPB, the yeast centrosome) by the bud. This model has anticipated analogous centrosome asymmetries featured in self-renewing stem cell divisions. We previously implicated Spc72, the cytoplasmic receptor for the gamma-tubulin nucleation complex, as the most upstream determinant linking SPB age, functional asymmetry and fate. Here we used structured illumination microscopy and biochemical analysis to explore the asymmetric landscape of nucleation sites inherently built into the spindle pathway and under the control of cyclin-dependent kinase (CDK). We show that CDK enforces Spc72 asymmetric docking by phosphorylating Nud1/centriolin. Furthermore, CDK-imposed order in the construction of the new SPB promotes the correct balance of nucleation sites between the nuclear and cytoplasmic faces of the SPB. Together these contributions by CDK inherently link correct SPB morphogenesis, age and fate.

Data availability

Original data has been made available via the Stowers institutional server at ftp://odr.stowers.org/LIBPB-1526For phosphoproteomic datasets cited in this manuscript, complete details are included in the citation and reference list. The datasets are accessible as supplemental material at the journal sites.

Article and author information

Author details

  1. Marco Geymonat

    Department of Genetics, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8792-0517
  2. Qiuran Peng

    Genetics, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4761-0944
  3. Zhiang Guo

    Genetics, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Zulin Yu

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Jay R Unruh

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Sue L Jaspersen

    Stowers Institute for Medical Research, Kansas City, United States
    For correspondence
    slj@stowers.org
    Competing interests
    The authors declare that no competing interests exist.
  7. Marisa Segal

    Genetics, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    ms433@hermes.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1848-9388

Funding

NIH -NIGMS (RO1GM121443)

  • Sue L Jaspersen

CSC Cambridge International Scholarship

  • Qiuran Peng
  • Marisa Segal

CSC Cambridge International Scholarship

  • Zhiang Guo
  • Marisa Segal

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

Reviewing Editor

  1. Jens Lüders, Institute for Research in Biomedicine, Spain

Publication history

  1. Received: May 22, 2020
  2. Accepted: August 21, 2020
  3. Accepted Manuscript published: August 27, 2020 (version 1)
  4. Version of Record published: September 3, 2020 (version 2)

Copyright

© 2020, Geymonat 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. Marco Geymonat
  2. Qiuran Peng
  3. Zhiang Guo
  4. Zulin Yu
  5. Jay R Unruh
  6. Sue L Jaspersen
  7. Marisa Segal
(2020)
Orderly assembly underpinning built-in asymmetry in the yeast centrosome duplication cycle requires cyclin-dependent kinase
eLife 9:e59222.
https://doi.org/10.7554/eLife.59222
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