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

• Published in: Genetics (Austin) 2009-03, Vol.181 (3), p.875-887
• Main Authors: Resnick, Tamar D, Dej, Kimberley J, Xiang, Youbin, Hawley, R. Scott, Ahn, Caroline, Orr-Weaver, Terry L
• Format: Article
• Language: English
• Subjects: Adenosine Triphosphatases - genetics; Adenosine Triphosphatases - metabolism; Alleles; Animals; Carrier Proteins - metabolism; Cell Cycle Proteins - metabolism; Cell division; chromosomal passenger complex; Chromosomal Proteins, Non-Histone - genetics; Chromosomal Proteins, Non-Histone - metabolism; chromosome segregation; condensin complex; DNA-Binding Proteins - genetics; DNA-Binding Proteins - metabolism; Drosophila - cytology; Drosophila - embryology; Drosophila - genetics; Drosophila - metabolism; Drosophila melanogaster; Drosophila Proteins - metabolism; Female; females; Infertility, Female - genetics; Investigations; Kinases; Meiosis; Metaphase; Microfilament Proteins - genetics; Microfilament Proteins - metabolism; Multiprotein Complexes - genetics; Multiprotein Complexes - metabolism; mutants; Mutation; oocytes; Oogenesis; phenotype; Prometaphase; Proteins; Roles; synaptonemal complex; Synaptonemal Complex - genetics; Synaptonemal Complex - metabolism
• ISSN: 0016-6731; 1943-2631; 1943-2631
• DOI: 10.1534/genetics.108.097741

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 incenp(QA26) 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 divisions.