Mutations in the Chromosomal Passenger Complex and the Condensin Complex Differentially Affect Synaptonemal Complex Disassembly and Metaphase I Configuration in Drosophila Female Meiosis by ProQuest


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									Copyright Ó 2009 by the Genetics Society of America
DOI: 10.1534/genetics.108.097741

    Mutations in the Chromosomal Passenger Complex and the Condensin
    Complex Differentially Affect Synaptonemal Complex Disassembly and
          Metaphase I Configuration in Drosophila Female Meiosis

  Tamar D. Resnick,*,1 Kimberley J. Dej,*,2 Youbin Xiang,† R. Scott Hawley,†,‡ Caroline Ahn*,3
                                 and Terry L. Orr-Weaver*,4
      *Whitehead Institute for Biomedical Research, and the Department of Biology, Massachusetts Institute of Technology, Cambridge,
               Massachusetts 02142, †Stowers Institute, Kansas City, Missouri 64110 and the ‡Department of Physiology,
                                     Kansas University Medical Center, Kansas City, Kansas 66160
                                                    Manuscript received October 18, 2008
                                                 Accepted for publication December 21, 2008

               Production of haploid gametes relies on the specially regulated meiotic cell cycle. Analyses of the role of
             essential mitotic regulators in meiosis have been hampered by a shortage of appropriate alleles in
             metazoans. We characterized female-sterile alleles of the condensin complex component dcap-g and used
             them to define roles for condensin in Drosophila female meiosis. In mitosis, the condensin complex is
             required for sister-chromatid resolution and contributes to chromosome condensation. In meiosis, we
             demonstrate a role for dcap-g in disassembly of the synaptonemal complex and for proper retention of the
             chromosomes in a metaphase I-arrested state. The chromosomal passenger complex also is known to have
             mitotic roles in chromosome condensation and is required in some systems for localization of the
             condensin complex. We used the QA26 allele of passenger component incenp to investigate the role of the
             passenger complex in oocyte meiosis. Strikingly, in incenpQA26 mutants maintenance of the synaptonemal
             complex is disrupted. In contrast to the dcap-g mutants, the incenp mutation leads to a failure of paired
             homologous chromosomes to biorient, such that bivalents frequently orient toward only one pole in
             prometaphase and metaphase I. We show that incenp interacts genetically with ord, suggesting an
             important functional relationship between them in meiotic chromosome dynamics. The dcap-g and incenp
             mutations cause maternal effect lethality, with embryos from mutant mothers arrested in the initial mitotic

O      RGANISMS that undergo sexual reproduction
        utilize a specialized cell cycle, meiosis, to generate
haploid gametes. Precise partitioning of the genome in
                                                                            allow homologs to remain physically attached after SC
                                                                            disassembly and to thereby coordinate their movements.
                                                                               In meiosis I, homologs biorient on the spindle while
meiosis is essential so that diploidy is reestablished upon                 sister chromatids coorient toward a single pole (re-
fertilization, which is critical for embryonic development                  viewed in Petronczki et al. 2003). Release of cohesion
(Hassold and Hunt 2001). Meiosis employs distinct                           distal to the chiasmata at the onset of anaphase I allows
regulatory mechanisms such that the DNA is replicated                       homologs to move apart; maintenance of centromere
exactly once and then divided twice without an additional                   cohesion holds sister chromatids together as they travel
intervening round of replication.                                           toward a single spindle pole. The enduring attachment
   In preparation for meiotic divisons, homologs pair                       between sister chromatids is essential for them to biorient
and, in many systems, a proteinaceous structure, the                        on the spindle in meiosis II. Centromere cohesion is
synaptonemal complex (SC), forms an axis between                            severed at the onset of anaphase II and sister chromatids
homologs and regulates meiotic recombination (Page                          segregate, in a manner more similar to mitosis.
and Hawley 2003). Crossover events generate covalent                           Progression through the meiotic program relies criti-
linkages between homologs. These, in combination                            cally on activity of both meiosis-specific factors and
with sister-chromatid cohesion distal to the chiasmata                      proteins that are also essential in mitosis. Study of the
(the physical structures resulting from crossing over),                     meiotic roles of proteins required in mitosis has been
                                                                            hampered by a shortage of alleles weak enough to allow
   Present address: Department of Genetics, Cell Biology, and Develop-      development of an animal, but strong enough to reveal
ment, University of Minnesota, Minneapolis, MN 55455.                       meiotic phenotypes. The condensin complex and the
   Present address: Department of Biology, McMaster University, Hamilton,   chromosomal passenger complex are important regula-
ON L8S 4K1, Canada.
   Present address: Harvard School of Dental Medicine, Boston, MA 02115.
                                                                            tors of chromosome dynamics in mitosis, but their roles
   Corresponding author: Whitehead 
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