Abstract
In Drosophila males and females mutant for the ord gene, sister chromatids prematurely disjoin in meiosis. We have isolated five new alleles of ord and analyzed them both as homozygotes and in trans to deficiencies for the locus, and we show that ord function is necessary early in meiosis of both sexes. Strong ord alleles result in chromosome nondisjunction in meiosis I that appears to be the consequence of precocious separation of the sister chromatids followed by their random segregation. Cytological analysis in males confirmed that precocious disjunction of the sister chromatids occurs in prometaphase I. This is in contrast to Drosophila mei-S332 mutants, in which precocious sister-chromatid separation also occurs, but not until late in anaphase I. All three of the new female fertile ord alleles reduce recombination, suggesting they affect homolog association as well as sister-chromatid cohesion. In addition to the effect of ord mutations on meiosis, we find that in ord(2) mutants chromosome segregation is aberrant in the mitotic divisions that produce the spermatocytes. The strongest ord alleles, ord(2) and ord(5), appear to cause defects in germline divisions in the female. These alleles are female sterile and produce egg chambers with altered nurse cell number, size, and nuclear morphology. In contrast to the effects of ord mutations on germline mitosis, all of the alleles are fully viable even when in trans to a deficiency, and thus exhibit no essential role in somatic mitosis. The ord gene product may prevent premature sister-chromatid separation by promoting cohesion of the sister chromatids in a structural or regulatory manner.
Full Text
The Full Text of this article is available as a PDF (3.6 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Baker B. S., Carpenter A. T., Esposito M. S., Esposito R. E., Sandler L. The genetic control of meiosis. Annu Rev Genet. 1976;10:53–134. doi: 10.1146/annurev.ge.10.120176.000413. [DOI] [PubMed] [Google Scholar]
- Baker B. S., Carpenter A. T., Ripoll P. The Utilization during Mitotic Cell Division of Loci Controlling Meiotic Recombination and Disjunction in DROSOPHILA MELANOGASTER. Genetics. 1978 Nov;90(3):531–578. doi: 10.1093/genetics/90.3.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beadle G. W., Ephrussi B. The Differentiation of Eye Pigments in Drosophila as Studied by Transplantation. Genetics. 1936 May;21(3):225–247. doi: 10.1093/genetics/21.3.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
- COOPER K. W. MEIOTIC CONJUNCTIVE ELEMENTS NOT INVOLVING CHIASMATA. Proc Natl Acad Sci U S A. 1964 Nov;52:1248–1255. doi: 10.1073/pnas.52.5.1248. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cooke C. A., Heck M. M., Earnshaw W. C. The inner centromere protein (INCENP) antigens: movement from inner centromere to midbody during mitosis. J Cell Biol. 1987 Nov;105(5):2053–2067. doi: 10.1083/jcb.105.5.2053. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldstein L. S. Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster. Cell. 1981 Sep;25(3):591–602. doi: 10.1016/0092-8674(81)90167-7. [DOI] [PubMed] [Google Scholar]
- Hazelrigg T., Levis R., Rubin G. M. Transformation of white locus DNA in drosophila: dosage compensation, zeste interaction, and position effects. Cell. 1984 Feb;36(2):469–481. doi: 10.1016/0092-8674(84)90240-x. [DOI] [PubMed] [Google Scholar]
- Kerrebrock A. W., Miyazaki W. Y., Birnby D., Orr-Weaver T. L. The Drosophila mei-S332 gene promotes sister-chromatid cohesion in meiosis following kinetochore differentiation. Genetics. 1992 Apr;130(4):827–841. doi: 10.1093/genetics/130.4.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koshland D., Hartwell L. H. The structure of sister minichromosome DNA before anaphase in Saccharomyces cerevisiae. Science. 1987 Dec 18;238(4834):1713–1716. doi: 10.1126/science.3317838. [DOI] [PubMed] [Google Scholar]
- Lin H. P., Church K. Meiosis in Drosophila melanogaster, III. The effect of orientation disruptor (ord) on gonial mitotic and the meiotic divisions in males. Genetics. 1982 Dec;102(4):751–770. doi: 10.1093/genetics/102.4.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maguire M. P., Paredes A. M., Riess R. W. The desynaptic mutant of maize as a combined defect of synaptonemal complex and chiasma maintenance. Genome. 1991 Dec;34(6):879–887. doi: 10.1139/g91-135. [DOI] [PubMed] [Google Scholar]
- Mason J. M. Orientation disruptor (ord): a recombination-defective and disjunction-defective meiotic mutant in Drosophila melanogaster. Genetics. 1976 Nov;84(3):545–572. doi: 10.1093/genetics/84.3.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moens P. B., Earnshaw W. C. Anti-topoisomerase II recognizes meiotic chromosome cores. Chromosoma. 1989 Nov;98(5):317–322. doi: 10.1007/BF00292383. [DOI] [PubMed] [Google Scholar]
- Murray A. W., Szostak J. W. Chromosome segregation in mitosis and meiosis. Annu Rev Cell Biol. 1985;1:289–315. doi: 10.1146/annurev.cb.01.110185.001445. [DOI] [PubMed] [Google Scholar]
- Rattner J. B., Kingwell B. G., Fritzler M. J. Detection of distinct structural domains within the primary constriction using autoantibodies. Chromosoma. 1988;96(5):360–367. doi: 10.1007/BF00330702. [DOI] [PubMed] [Google Scholar]
- Rose D., Thomas W., Holm C. Segregation of recombined chromosomes in meiosis I requires DNA topoisomerase II. Cell. 1990 Mar 23;60(6):1009–1017. doi: 10.1016/0092-8674(90)90349-j. [DOI] [PubMed] [Google Scholar]
- Sandler L., Lindsley D. L., Nicoletti B., Trippa G. Mutants affecting meiosis in natural populations of Drosophila melanogaster. Genetics. 1968 Nov;60(3):525–558. doi: 10.1093/genetics/60.3.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simpson P. Maternal-Zygotic Gene Interactions during Formation of the Dorsoventral Pattern in Drosophila Embryos. Genetics. 1983 Nov;105(3):615–632. doi: 10.1093/genetics/105.3.615. [DOI] [PMC free article] [PubMed] [Google Scholar]