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Fused sister kinetochores initiate the reductional division in meiosis I

Nature Cell Biology volume 11, pages 1103–1108 (2009)Cite this article

Abstract

During meiosis I the genome is reduced to the haploid content by a coordinated reductional division event. Homologous chromosomes align, recombine and segregate while the sister chromatids co-orient and move to the same pole1,2. Several data suggest that sister kinetochores co-orient early in metaphase I and that sister chromatid cohesion (which requires Rec8 and Shugoshin) supports monopolar orientation. Nevertheless, it is unclear how the sister kinetochores function as single unit during this period. A gene (monopolin)3 with a co-orienting role was identified in Saccharomyces cerevisiae; however, it does not have the same function in fission yeast4 and no similar genes have been found in other species. Here we pursue this issue using knockdown mutants of the core kinetochore protein MIS12 (minichromosome instability 12). MIS12 binds to base of the NDC80 complex, which in turn binds directly to microtubules5,6,7. In maize plants with systemically reduced levels of MIS12, a visible MIS12–NDC80 bridge between sister kinetochores at meiosis I is broken. Kinetochores separate and orient randomly in metaphase I, causing chromosomes to stall in anaphase due to normal cohesion, marked by Shugoshin, between the chromatids. The data establish that sister kinetochores in meiosis I are fused by a shared microtubule-binding face and that this direct linkage is required for reductional division.

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Figure 1: Meiosis I.
Figure 2: Wild-type MIS12 staining.
Figure 3: Meiotic defects in Mis12 RNAi cell lines.
Figure 4: Shugoshin (SGO) stains pericentromeric regions and remains in place when sister kinetochores separate in Mis12 RNAi mutants.

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Acknowledgements

We thank X. Zhang for her support and help with RT-PCR and image analysis, H. Tang for help with statistics, R. Wang for providing Shugoshin antibodies, A. Luce for technical support and C. Topp and L. Kanizay for helpful comments. This study was supported by a grant from the National Science Foundation to R.K.D. (0421671).

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Authors and Affiliations

  1. Department of Plant Biology, University of Georgia, Athens, 30602, GA, USA

    Xuexian Li & R. Kelly Dawe

  2. Department of Genetics, University of Georgia, Athens, 30602, GA, USA

    R. Kelly Dawe

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  1. Xuexian Li
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X.L. performed experimental work and data analysis. R.K.D. focused on planning and interpretation.

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Correspondence to R. Kelly Dawe.

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Li, X., Dawe, R. Fused sister kinetochores initiate the reductional division in meiosis I. Nat Cell Biol 11, 1103–1108 (2009). https://doi.org/10.1038/ncb1923

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