Polo-like kinase Cdc5 regulates Spc72 recruitment to spindle pole body in the methylotrophic yeast Ogataea polymorpha

  1. Hiromi Maekawa  Is a corresponding author
  2. Annett Neuner
  3. Diana Rüthnick
  4. Elmar Schiebel
  5. Gislene Pereira
  6. Yoshinobu Kaneko
  1. Osaka University, Japan
  2. Universität Heidelberg, Germany
  3. University of Heidelberg, Germany

Abstract

Cytoplasmic microtubules (cMT) control mitotic spindle positioning in many organisms, and are therefore pivotal for successful cell division. Despite its importance, the temporal control of cMT formation remains poorly understood. Here we show that unlike the best-studied yeast Saccharomyces cerevisiae, position of pre-anaphase nucleus is not strongly biased toward bud neck in Ogataea polymorpha and the regulation of spindle positioning becomes active only shortly before anaphase. This is likely due to the unstable property of cMTs compared to those in S. cerevisiae. Furthermore, we show that cMT nucleation/anchoring is restricted at the level of recruitment of the γ-tubulin complex receptor, Spc72, to spindle pole body (SPB), which is regulated by the polo-like kinase Cdc5. Additionally, electron microscopy revealed that the cytoplasmic side of SPB is structurally different between G1 and anaphase. Thus, polo-like kinase dependent recruitment of γ-tubulin receptor to SPBs determines the timing of spindle orientation in O. polymorpha.

Data availability

The following previously published data sets were used
    1. Maekawa H
    2. Kaneko Y
    (2014) Opolymorpha_4329
    Publicly available at the DNA Data Bank of Japan (accession no. DF933569-DF933585).

Article and author information

Author details

  1. Hiromi Maekawa

    Graduate School of Engineering, Osaka University, Suita, Japan
    For correspondence
    hmaekawa@agr.kyushu-u.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0175-1610
  2. Annett Neuner

    Zentrum für Molekulare Biologie (ZMBH), Universität Heidelberg, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Diana Rüthnick

    Zentrum für Molekulare Biologie (ZMBH), Universität Heidelberg, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Elmar Schiebel

    Zentrum für Molekulare Biologie (ZMBH), Universität Heidelberg, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Gislene Pereira

    Centre for Organismal Studies (COS), University of Heidelberg, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6519-4737
  6. Yoshinobu Kaneko

    Graduate School of Engineering, Osaka University, Suita, Japan
    Competing interests
    The authors declare that no competing interests exist.

Funding

Institute for Fermentation, Osaka (the Endowed Chair Program)

  • Yoshinobu Kaneko

Japan Society for the Promotion of Science (JP24570214)

  • Hiromi Maekawa

Deutsche Forschungsgemeinschaft (PE1883)

  • Gislene Pereira

Deutsche Forschungsgemeinschaft (SFB873)

  • Gislene Pereira

Deutsche Forschungsgemeinschaft (SFB1036)

  • Gislene Pereira

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

Reviewing Editor

  1. Anna Akhmanova, Utrecht University, Netherlands

Publication history

  1. Received: December 19, 2016
  2. Accepted: August 17, 2017
  3. Accepted Manuscript published: August 30, 2017 (version 1)
  4. Version of Record published: October 3, 2017 (version 2)

Copyright

© 2017, Maekawa 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. Hiromi Maekawa
  2. Annett Neuner
  3. Diana Rüthnick
  4. Elmar Schiebel
  5. Gislene Pereira
  6. Yoshinobu Kaneko
(2017)
Polo-like kinase Cdc5 regulates Spc72 recruitment to spindle pole body in the methylotrophic yeast Ogataea polymorpha
eLife 6:e24340.
https://doi.org/10.7554/eLife.24340

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