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SYSTEMS BIOLOGY, MOLECULAR BIOLOGY, AND GENE REGULATION

Arabidopsis Separase Functions beyond the Removal of Sister Chromatid Cohesion during Meiosis^1,[OA]

Department of Chemistry and Biochemistry, Miami University, Oxford, Ohio 45056

Separase is a capase family protease that is required for the release of sister chromatid cohesion during meiosis and mitosis. Proteolytic cleavage of the -kleisin subunit of the cohesin complex at the metaphase-to-anaphase transition is essential for the proper segregation of chromosomes. In addition to its highly conserved role in cleaving the -kleisin subunit, separase appears to have acquired additional diverse activities in some organisms, including involvement in mitotic and meiotic anaphase spindle assembly and elongation, interphase spindle pole body positioning, and epithelial cell reorganization. Results from the characterization of Arabidopsis (Arabidopsis thaliana) separase (ESP) demonstrated that meiotic expression of ESP RNA interference blocked the proper removal of cohesin from chromosomes and resulted in the presence of a mixture of fragmented chromosomes and intact bivalents. The presence of large numbers of intact bivalents raised the possibility that separase may also have multiple roles in Arabidopsis. In this report, we show that meiotic expression of ESP RNA interference blocks the removal of cohesin during both meiosis I and II, results in alterations in nonhomologous centromere association, disrupts the radial microtubule system after telophase II, and affects the proper establishment of nuclear cytoplasmic domains, resulting in the formation of multinucleate microspores.

² Present address: Genetics and Biochemistry Branch, The National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, 5 Memorial Road, Building 5/209, Bethesda, MD 20892.

³ Present address: Department of Biochemistry and Molecular Biology, Mayo Clinic College of Medicine, Rochester, MN 55905.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Christopher A. Makaroff (makaroca{at}muohio.edu).

^[OA] Open access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.109.140699

^* Corresponding author; e-mail makaroca{at}muohio.edu.

Received May 1, 2009; accepted June 28, 2009; published July 10, 2009.