The telomere bouquet regulates meiotic centromere assembly

Michael Klutstein, Alex Fennell, Alfonso Fernández-Álvarez, Julia Promisel Cooper*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

50 Scopus citations

Abstract

The role of the conserved meiotic telomere bouquet has been enigmatic for over a century. We showed previously that disruption of the fission yeast bouquet impairs spindle formation in approximately half of meiotic cells. Surprisingly, bouquet-deficient meiocytes with functional spindles harbour chromosomes that fail to achieve spindle attachment. Kinetochore proteins and the centromeric histone H3 variant Cnp1 fail to localize to those centromeres that exhibit spindle attachment defects in the bouquet's absence. The HP1 orthologue Swi6 also fails to bind these centromeres, suggesting that compromised pericentromeric heterochromatin underlies the kinetochore defects. We find that centromeres are prone to disassembly during meiosis, but this is reversed by localization of centromeres to the telomere-proximal microenvironment, which is conducive to heterochromatin formation and centromere reassembly. Accordingly, artificially tethering a centromere to a telomere rescues the tethered centromere but not other centromeres. These results reveal an unanticipated level of control of centromeres by telomeres.

Original languageAmerican English
Pages (from-to)458-469
Number of pages12
JournalNature Cell Biology
Volume17
Issue number4
DOIs
StatePublished - 30 Apr 2015

Bibliographical note

Funding Information:
We thank our current and former laboratory members for discussions and advice, and R. Allshire (Wellcome Trust, University of Edinburgh, UK), M. Sato (University of Tokyo, Japan), T. Toda (Cancer Research UK, UK) and Y. Watanabe (University of Tokyo, Japan) for strains and reagents. We thank M. Lichten, S. Grewal and their laboratory members for discussion and help with reagents and equipment during our recent move. This work was supported by the National Institutes of Health, Cancer Research UK, the European Research Council, and a Marie Curie fellowship to M.K.

Publisher Copyright:
© 2015 Macmillan Publishers Limited.

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