Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis


Although assembly of acentrosomal meiotic spindles has been extensively studied1, little is known about the segregation of chromosomes on these spindles. Here, we show in Caenorhabditis elegans oocytes that the kinetochore protein, KNL-1, directs assembly of meiotic kinetochores that orient chromosomes. However, in contrast to mitosis, chromosome separation during meiotic anaphase is kinetochore-independent. Before anaphase, meiotic kinetochores and spindle poles disassemble along with the microtubules on the poleward side of chromosomes. During anaphase, microtubules then form between the separating chromosomes. Functional analysis implicated a set of proteins that localize to a ring-shaped domain between kinetochores during pre-anaphase spindle assembly and anaphase separation. These proteins are localized by the chromosomal passenger complex, which regulates the loss of meiotic chromosome cohesion2,3,4. Thus, meiotic segregation in C. elegans is a two-stage process, where kinetochores orient chromosomes, but are then dispensable for their separation. We suggest that separation is controlled by a meiosis-specific chromosomal domain to coordinate cohesin removal and chromosome segregation.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it


Prices may be subject to local taxes which are calculated during checkout

Figure 1: Cup-shaped meiotic kinetochores are assembled by a KNL-1-dependent mechanism and are required for accurate meiotic chromosome segregation.
Figure 2: KNL-1 is required to orient chromosomes on the acentrosomal meiotic spindle before anaphase onset.
Figure 3: Anaphase chromosome separation on acentrosomal meiotic spindles occurs by a kinetochore-independent mechanism.
Figure 4: Proteins that localize to a ring-shaped domain between the kinetochores form linker structures during anaphase.
Figure 5: Ring domain proteins contribute to both pre-anaphase spindle assembly and anaphase separation.


  1. Dumont, J. & Brunet, S. Oogenesis: The Universal Process. (eds Verlhac, M. H. & Villeneuve, A. M.) 269–290 (Wiley-Blackwell, 2010).

    Google Scholar 

  2. Nabeshima, K., Villeneuve, A. M. & Colaiacovo, M. P. Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. J. Cell Biol. 168, 683–689 (2005).

    Article  CAS  Google Scholar 

  3. Kaitna, S., Pasierbek, P., Jantsch, M., Loidl, J. & Glotzer, M. The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous chromosomes during meiosis. Curr. Biol. 12, 798–812 (2002).

    Article  CAS  Google Scholar 

  4. Rogers, E., Bishop, J. D., Waddle, J. A., Schumacher, J. M. & Lin, R. The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. J. Cell Biol. 157, 219–229 (2002).

    Article  CAS  Google Scholar 

  5. Maddox, P. S., Oegema, K., Desai, A. & Cheeseman, I. M. “Holo”er than thou: chromosome segregation and kinetochore function in C. elegans. Chromosome Res. 12, 641–653 (2004).

    Article  CAS  Google Scholar 

  6. Monen, J., Maddox, P. S., Hyndman, F., Oegema, K. & Desai, A. Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis. Nat. Cell Biol. 7, 1248–1255 (2005).

    Article  Google Scholar 

  7. Powers, J. et al. Loss of KLP-19 polar ejection force causes misorientation and missegregation of holocentric chromosomes. J. Cell Biol. 166, 991–1001 (2004).

    Article  CAS  Google Scholar 

  8. Wignall, S. M. & Villeneuve, A. M. Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis. Nat. Cell Biol. 11, 839–844 (2009).

    Article  CAS  Google Scholar 

  9. Gilliland, W. D. et al. The Multiple Roles of Mps1 in Drosophila Female Meiosis. PLoS Genet. 3, e113 (2007).

    Article  Google Scholar 

  10. Howe, M., McDonald, K. L., Albertson, D. G. & Meyer, B. J. HIM-10 is required for kinetochore structure and function on Caenorhabditis elegans holocentric chromosomes. J. Cell Biol. 153, 1227–1238 (2001).

    Article  CAS  Google Scholar 

  11. Cheeseman, I. M. & Desai, A. Molecular architecture of the kinetochore–microtubule interface. Nat. Rev. Mol. Cell Biol. 9, 33–46 (2008).

    Article  CAS  Google Scholar 

  12. Cheeseman, I. M. et al. A conserved protein network controls assembly of the outer kinetochore and its ability to sustain tension. Genes Dev. 18, 2255–2268 (2004).

    Article  CAS  Google Scholar 

  13. Oegema, K., Desai, A., Rybina, S., Kirkham, M. & Hyman, A. A. Functional analysis of kinetochore assembly in Caenorhabditis elegans. J. Cell Biol. 153, 1209–1226 (2001).

    Article  CAS  Google Scholar 

  14. McNally, K., Audhya, A., Oegema, K. & McNally, F. J. Katanin controls mitotic and meiotic spindle length. J. Cell Biol. 175, 881–891 (2006).

    Article  CAS  Google Scholar 

  15. Hannak, E. & Heald, R. Xorbit/CLASP links dynamic microtubules to chromosomes in the Xenopus meiotic spindle. J. Cell Biol. 172, 19–25 (2006).

    Article  CAS  Google Scholar 

  16. Brunet, S., Polanski, Z., Verlhac, M. H., Kubiak, J. Z. & Maro, B. Bipolar meiotic spindle formation without chromatin. Curr. Biol. 8, 1231–1234 (1998).

    Article  CAS  Google Scholar 

  17. Ohsugi, M. et al. Kid-mediated chromosome compaction ensures proper nuclear envelope formation. Cell 132, 771–782 (2008).

    Article  CAS  Google Scholar 

  18. Martinez-Perez, E. et al. Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev. 22, 2886–2901 (2008).

    Article  CAS  Google Scholar 

  19. de Carvalho, C. E. et al. LAB-1 antagonizes the Aurora B kinase in C. elegans. Genes Dev. 22, 2869–2885 (2008).

    Article  Google Scholar 

  20. Toth, A. et al. Functional genomics identifies monopolin: a kinetochore protein required for segregation of homologs during meiosis I. Cell 103, 1155–1168 (2000).

    Article  CAS  Google Scholar 

  21. Yokobayashi, S. & Watanabe, Y. The kinetochore protein Moa1 enables cohesion-mediated monopolar attachment at meiosis I. Cell 123, 803–817 (2005).

    Article  CAS  Google Scholar 

  22. Albertson, D. G. & Thomson, J. N. Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res. 1, 15–26 (1993).

    Article  CAS  Google Scholar 

  23. Brunet, S. et al. Kinetochore fibers are not involved in the formation of the first meiotic spindle in mouse oocytes, but control the exit from the first meiotic M phase. J. Cell Biol. 146, 1–12 (1999).

    Article  CAS  Google Scholar 

  24. Deng, M., Gao, J., Suraneni, P. & Li, R. Kinetochore-independent chromosome poleward movement during anaphase of meiosis II in mouse eggs. PLoS One 4, e5249 (2009).

    Article  Google Scholar 

  25. Jones, K. T. Meiosis in oocytes: predisposition to aneuploidy and its increased incidence with age. Hum. Reprod. Update 14, 143–158 (2008).

    Article  CAS  Google Scholar 

  26. Hunt, P. A. & Hassold, T. J. Human female meiosis: what makes a good egg go bad? Trends Genet. 24, 86–93 (2008).

    Article  CAS  Google Scholar 

  27. Praitis, V., Casey, E., Collar, D. & Austin, J. Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157, 1217–1226 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Desai, A. et al. KNL-1 directs assembly of the microtubule-binding interface of the kinetochore in C. elegans. Genes Dev. 17, 2421–2435 (2003).

    Article  CAS  Google Scholar 

  29. Gassmann, R. et al. A new mechanism controlling kinetochore-microtubule interactions revealed by comparison of two dynein-targeting components: SPDL-1 and the Rod/Zwilch/Zw10 complex. Genes Dev. 22, 2385–2399 (2008).

    Article  CAS  Google Scholar 

  30. Cheeseman, I. M., MacLeod, I., Yates, J. R. 3rd, Oegema, K. & Desai, A. The CENP-F-like proteins HCP-1 and HCP-2 target CLASP to kinetochores to mediate chromosome segregation. Curr. Biol. 15, 771–777 (2005).

    Article  CAS  Google Scholar 

  31. Edgar, L. G. Blastomere culture and analysis. Methods Cell Biol. 48, 303–321 (1995).

    Article  CAS  Google Scholar 

Download references


We are grateful to J. Canman and R. Green for critical reading of the manuscript. This work was supported by an EMBO long-term postdoctoral fellowship to J.D., grants from Human Frontiers Science Program (RGY0084) and the NIH (GM074215) to A.D., and funding from the Ludwig Institute for Cancer Research to A.D. and K.O.

Author information

Authors and Affiliations



All experimental data were generated by J.D., who also had primary responsibility for experimental design and data analysis. A.D. and K.O. contributed to experimental design and data analysis. J.D., A.D. and K.O. wrote the manuscript.

Corresponding author

Correspondence to Arshad Desai.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 1669 kb)

Supplementary Information

Supplementary Movie 1 (MOV 2004 kb)

Supplementary Information

Supplementary Movie 2 (MOV 948 kb)

Supplementary Information

Supplementary Movie 3 (MOV 331 kb)

Supplementary Information

Supplementary Movie 4 (MOV 1686 kb)

Supplementary Information

Supplementary Movie 5 (MOV 632 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dumont, J., Oegema, K. & Desai, A. A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis. Nat Cell Biol 12, 894–901 (2010).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing