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. 2009 Mar;181(3):875-87.
doi: 10.1534/genetics.108.097741. Epub 2008 Dec 22.

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, Youbin Xiang, R Scott Hawley, Caroline Ahn, Terry L Orr-Weaver
Affiliations

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 et al. Genetics. 2009 Mar.

Abstract

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.

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Figures

F<sc>igure</sc> 1.—
Figure 1.—
SC assembly is normal in condensin and passenger complex mutants. In the left panels DNA is red and C(3)G is green. The middle panels show C(3)G staining and the right, DNA. (A) Oregon R control. (B) dcap-gZ1/dcap-gK4. (C) incenpQA26 Df(2L)Exel7049/incenpQA26. (D) incenpQA26 ord10/incenpQA26. All images are at the same magnification. Bar, 5μm.
F<sc>igure</sc> 2.—
Figure 2.—
Developmental timing of SC disassembly. In the left panels DNA is red and C(3)G green; side panels show separated channels for boxed region, with C(3)G on the top. In wild-type oocytes C(3)G localizes to the meiotic chromosomes beginning in the germarium, prior to stage 2. This localization to the chromosomes, which are in a compact structure and take up only a small portion of the nucleus, is maintained through stage 4 or 5. As development continues, C(3)G begins to delocalize from the chromosomes and is seen with increasing intensity throughout the nucleus. (A–D) Display of the categories scored in Table 1. (A) C(3)G localized solely to chromosome axis (Oregon R, stage 4). (B) C(3)G dispersed on axis and spreading through nucleus (Oregon R, stage 6). (C) Trace amounts of C(3)G on chromosomes (Oregon R, stage 6). (D) No C(3)G associated with chromosomes (Oregon R, stage 8). All of the merged images are at the same magnification. Bar, 10μm.
F<sc>igure</sc> 3.—
Figure 3.—
SC dynamics and delayed disassembly in dcap-g mutants. SC structure in progressive stages of oocyte development in dcap-gK3/Df mutant oocytes. DNA is in green; C(3)G is in red in the merged images and in white in the insets. (A) In the germarium, SC assembles normally in the dcap-g mutant. (B and C) The SC is present during the pachytene stages, as in wild-type oocytes. (D) The SC aberrantly persists into stage 8. The developmental stage is shown in each panel. The merged images are at the same magnification. Bar, 20 μm; bars, 5 μm in all the enlarged insets.
F<sc>igure</sc> 4.—
Figure 4.—
The SC prematurely disassembles in incenp mutants. The SC is disassembled completely in this stage 5 oocyte from an incenpQA26 Df(2L)Exel7049/incenpQA26 female, because there is no detectable C(3)G staining on the chromosomes. The DNA is shown in red and C(3)G in green in the merged image on the left, and split channels are shown as labeled on the right. Bar in the merged image, 5 μm.
F<sc>igure</sc> 5.—
Figure 5.—
dcap-g mutant oocytes have defective metaphase I figures. (A) FISH analysis shows that in the w1118 control the chromosomes are held on the metaphase I plate, with the X chromosomes (green FISH signal) bioriented. Bar, 3 μm. (B) In dcap-gZ1/K4 mutant mature oocytes multiple chromosome masses are seen at metaphase I. The FISH probes (X, green; fourth, red) show that the homologs are not only bioriented but separated. Bar, 2 μm. (C) MEI-S332 (red) localization to the centromeres of a control Oregon R oocyte. The spindle is shown in green. (D–F) MEI-S332 localizes to the centromeres in dcap-g mutants. In all panels DNA stain is in blue. The images in C–F are at the same magnification. Bar, 5 μm.
F<sc>igure</sc> 6.—
Figure 6.—
Biorientation and segregation failure in incenp mutant oocytes. (A–C) FISH analysis of chromosome orientation. In contrast to the biorientation observed for the X bivalent (green FISH signal) in the w1118 control (A), in incenpQA26 Df(2L)Exel7049/incenpQA26 mutant oocytes the X bivalent (green) is monooriented (B and C). In these oocytes the fourth chromosomes (red) are bioriented. (D and E) Staining for MEI-S332 (red), spindle (green), and DNA (blue). MEI-S332 localizes to chromosomes in incenp mutant oocytes. Although it can localize in a pattern consistent with centromere localization (arrow in D), extra foci frequently are observed (E). (F and G) FISH analysis of chromosomes. Bivalents fail to biorient in incenpQA26 ord10/incenpQA26 oocytes. In F, the X chromosomes are bioriented (green) but the fourth chromosomes (red) monooriented, whereas the opposite is observed in G. Bars are indicated in each panel.
F<sc>igure</sc> 7.—
Figure 7.—
dcap-g and incenp mutant mothers produce embryos displaying defects in mitosis and postmeiotic chromosome structure. Early embryos stained for DNA (green, and gray) and tubulin (red). (A) Oregon R, anaphase in first mitotic division. (B) A dcap-gZ1/dcap-gK4, polyploid mass in early arrested embryo. (C) incenpQA26, chromosome bridging in first anaphase. (D) incenpQA26, chromatin bridging in early arrested embryo. (E–H) polar body rosette structures. (E) Oregon R, displays condensed arms of even length. (F) dcap-gK3, pulverized chromosomes. (G) dcap-gZ1, hypercondensed chromosomes. (H) incenpQA26, elongated and fragmented chromosomes. The images in A–D are at the same magnification. Bars, 5 μm.
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