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Astral microtubules monitor metaphase spindle alignment in fission yeast

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Abstract

Segregating genetic material along the longest axis of the cell ensures that there is a sufficient distance between daughter chromosomes at the point of cytokinesis. Monitoring the orientation of the mitotic spindle can be subjected to cell cycle controls. In the fission yeast Schizosaccharomyces pombe, the existence of such a cell-cycle checkpoint has been proposed to delay the metaphase to anaphase transition when spindle poles are not properly oriented with respect to the actomyosin ring1. Here we show, by using a fission yeast mutant compromised in its assembly of astral microtubules, that in the absence of astral microtubules short metaphase spindles are unable to orient themselves with respect to the long axis of the cell and are delayed in spindle elongation. This astral defect engages a spindle orientation checkpoint because deletion of the transcription factor Atf1, which is involved in maintaining this checkpoint, allows misaligned asterless metaphase spindles to elongate. We propose that astral microtubules are involved directly in monitoring orientation of the metaphase spindle and in controlling the timing of elongation in fission yeast.

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Figure 1: S. pombe mutants lacking Mia1 are deficient in astral microtubule function and have a high number of short misoriented spindles.
Figure 2: mia1Δ cells are delayed in orienting metaphase spindles along the long axis of the cell.
Figure 3: mia1Δ mutant cells are delayed in mitosis with fully extended metaphase spindles and high concentrations of cyclin, but have wild-type rates of spindle assembly and anaphase elongation.
Figure 4: mia1Δatf1Δ spindles start elongating irrespective of their angle of alignment with the long axis of the cell.

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Acknowledgements

We thank Y. Hiraoka, J. Millar, A. Decottignies and K. Gull for materials and reagents; G. Jedd for comments on the manuscript; and members of the fungal laboratories, especially V. Rajagopalan, V. Wachtler, N. Naqvi and K. Wong for discussions. Our research was supported by A*STAR Singapore and Temasek Life Sciences Laboratory.

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Authors and Affiliations

  1. Temasek Life Sciences Laboratory and Institute of Molecular Agrobiology, 1 Research Link, The National University of Singapore, 117604, Singapore

    Snezhana Oliferenko & Mohan K. Balasubramanian

Authors
  1. Snezhana Oliferenko
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  2. Mohan K. Balasubramanian
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Correspondence to Snezhana Oliferenko.

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The authors declare no competing financial interests.

Supplementary information

Supplementary figure and table

Figure S1 Mia1+ gene from S. pombe has an overall sequence homology to the hypothetical protein NCU01413.1from N. crassa. (PDF 214 kb)

Supplementary table 1

Movie 1

A time-lapse sequence of spindle dynamics in α-tubulin-EGFP expressing wild type S. pombe. (MOV 900 kb)

Movie 2

A time-lapse sequence of spindle dynamics in α-tubulin-EGFP expressing mia1Δ S. pombe cell. (MOV 1291 kb)

Movie 3

A time-lapse sequence of spindle dynamics, visualized using a Sid2p-EGFP expressed in wild type S. pombe. (MOV 672 kb)

Movie 4

A time-lapse sequence of spindle dynamics, visualized using a Sid2p-EGFP expressed in mia1Δ cell. (MOV 1068 kb)

Movie 5

A time-lapse sequence of spindle dynamics in α-tubulin-EGFP-expressing mia1Δatf1Δ cell. (MOV 926 kb)

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Oliferenko, S., Balasubramanian, M. Astral microtubules monitor metaphase spindle alignment in fission yeast. Nat Cell Biol 4, 816–820 (2002). https://doi.org/10.1038/ncb861

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  • DOI: https://doi.org/10.1038/ncb861

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