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Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I

Nature Cell Biology volume 5, pages 480–485 (2003)Cite this article

Abstract

During meiosis, two rounds of chromosome segregation occur after a single round of DNA replication, producing haploid progeny from diploid progenitors. Three innovations in chromosome behaviour during meiosis I accomplish this unique division. First, crossovers between maternal and paternal sister chromatids (detected cytologically as chiasmata) bind replicated maternal and paternal chromosomes together. Second, sister kinetochores attach to microtubules from the same pole (mono-polar orientation), causing maternal and paternal centromere pairs (and not sister chromatids) to be separated. Third, sister chromatid cohesion near centromeres is preserved at anaphase I when cohesion along chromosome arms is destroyed. The finding that destruction of mitotic cohesion is regulated by Polo-like kinases1,2 prompted us to investigate the meiotic role of the yeast Polo-like kinase Cdc5. We show here that cells lacking Cdc5 synapse homologues and initiate recombination normally, but fail to efficiently resolve recombination intermediates as crossovers. They also fail to properly localize the Lrs4 (ref. 3) and Mam1 (ref. 4) monopolin proteins, resulting in bipolar orientation of sister kinetochores. Cdc5 is thus required both for the formation of chiasmata and for cosegregation of sister centromeres at meiosis I.

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Figure 1: Expression of Cdc5 during meiosis.
Figure 2: Cdc5 is required for meiosis I.
Figure 3: Cdc5 is required to prevent bi-orientation of sister kinetochores at meiosis I.
Figure 4: Strains lacking Cdc5 are specifically defective in crossover product formation.

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Acknowledgements

We thank the Nasmyth group and F. Klein, S. Hauf, M. Winey and N. Hunter for discussions, F.Klein for help with chromosome spreads, H. Tkadletz for help preparing figures, and K. Rabitsch and D. Schoffnegger for promoter replacement reagents. We thank A. Amon and B. Lee for communicating unpublished results and providing the Pclb2-CDC20 strain. R.K.C. was sponsored by the Damon Runyon Cancer Research Foundation. Research in the Nasmyth laboratory is supported by Boehringer Ingelheim International and the Austrian Industrial Research Promotion Fund.

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Authors and Affiliations

  1. Research Institute of Molecular Pathology (IMP), Vienna, A-1030, Austria

    Rosemary K. Clyne, Vittorio L. Katis & Kim Nasmyth

  2. Laboratory of Biochemistry, Center for Cancer Research, National Cancer Institute, Bethesda, 20892-4255, MD, USA

    Lea Jessop & Michael Lichten

  3. Department of Biochemistry and Biophysics, University of California, San Francisco, 94143-0448, CA, USA

    Kirsten R. Benjamin & Ira Herskowitz

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  1. Rosemary K. Clyne
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Correspondence to Kim Nasmyth.

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Supplementary information

Supplementary Figures

Figure S1. Rec8 chromatin association and homologue synapsis during pachytene. (PDF 89 kb)

Figure S2. A Cdc5-dependent form of Rec8 accumulates in metaphase I.

Supplementary Table

Table 1. Genotypes of strains described in this study. (DOC 26 kb)

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Clyne, R., Katis, V., Jessop, L. et al. Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I. Nat Cell Biol 5, 480–485 (2003). https://doi.org/10.1038/ncb977

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