Abstract
In recombination-proficient organisms, chiasmata appear to mediate associations between homologs at metaphase of meiosis I. It is less clear how homolog associations are maintained in organisms that lack recombination, such as male Drosophila. In lieu of chiasmata and synaptonemal complexes, there must be molecules that balance poleward forces exerted across homologous centromeres. Here we describe the genetic and cytological characterization of four EMS-induced mutations in teflon (tef), a gene involved in this process in Drosophila melanogaster. All four alleles are male specific and cause meiosis I-specific nondisjunction of the autosomes. They do not measurably perturb sex chromosome segregation, suggesting that there are differences in the genetic control of autosome and sex chromosome segregation in males. Meiotic transmission of univalent chromosomes is unaffected in tef mutants, implicating the tef product in a pairing-dependent process. The segregation of translocations between sex chromosomes and autosomes is altered in tef mutants in a manner that supports this hypothesis. Consistent with these genetic observations, cytological examination of meiotic chromosomes suggests a role of tef in regulating or mediating pairing of autosomal bivalents at meiosis I. We discuss implications of this finding in regard to the evolution of heteromorphic sex chromosomes and the mechanisms that ensure chromosome disjunction in the absence of recombination.
Full Text
The Full Text of this article is available as a PDF (249.1 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ault J. G., Lin H. P., Church K. Meiosis in Drosophila melanogaster. IV. The conjunctive mechanism of the XY bivalent. Chromosoma. 1982;86(3):309–317. doi: 10.1007/BF00292259. [DOI] [PubMed] [Google Scholar]
- Ault J. G., Rieder C. L. Meiosis in Drosophila males. I. The question of separate conjunctive mechanisms for the XY and autosomal bivalents. Chromosoma. 1994 Sep;103(5):352–356. doi: 10.1007/BF00417883. [DOI] [PubMed] [Google Scholar]
- Baker B. S., Carpenter A. T. Genetic analysis of sex chromosomal meiotic mutants in Drosophilia melanogaster. Genetics. 1972 Jun;71(2):255–286. doi: 10.1093/genetics/71.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
- COOPER K. W. Cytogenetic analysis of major heterochromatic elements (especially Xh and Y) in Drosophila melanogaster, and the theory of "heterochromatin". Chromosoma. 1959;10:535–588. doi: 10.1007/BF00396588. [DOI] [PubMed] [Google Scholar]
- Cenci G., Bonaccorsi S., Pisano C., Verni F., Gatti M. Chromatin and microtubule organization during premeiotic, meiotic and early postmeiotic stages of Drosophila melanogaster spermatogenesis. J Cell Sci. 1994 Dec;107(Pt 12):3521–3534. doi: 10.1242/jcs.107.12.3521. [DOI] [PubMed] [Google Scholar]
- Clarkson M., Saint R. A His2AvDGFP fusion gene complements a lethal His2AvD mutant allele and provides an in vivo marker for Drosophila chromosome behavior. DNA Cell Biol. 1999 Jun;18(6):457–462. doi: 10.1089/104454999315178. [DOI] [PubMed] [Google Scholar]
- Fang J. S., Jagiello G. M. Unique state of sexual dimorphism of crossing-over in diplotene spermatocytes and oocytes of Mesocricetus brandti, a species with neonatal oogenesis. Biol Reprod. 1991 Sep;45(3):447–454. doi: 10.1095/biolreprod45.3.447. [DOI] [PubMed] [Google Scholar]
- Hilliker A. J., Holm D. G., Appels R. The relationship between heterochromatic homology and meiotic segregation of compound second autosomes during spermatogenesis in Drosophila melanogaster. Genet Res. 1982 Apr;39(2):157–168. doi: 10.1017/s0016672300020851. [DOI] [PubMed] [Google Scholar]
- Karpen G. H., Spradling A. C. Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P element insertional mutagenesis. Genetics. 1992 Nov;132(3):737–753. doi: 10.1093/genetics/132.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lin H. P., Ault J. G., Church K. Meiosis in Drosophila melanogaster. I. Chromosome identification and kinetochore microtubule numbers during the first and second meiotic divisions in males. Chromosoma. 1981;83(4):507–521. doi: 10.1007/BF00328276. [DOI] [PubMed] [Google Scholar]
- Lindsley D L, Sandler L. The Meiotic Behavior of Grossly Deleted X Chromosomes in Drosophila Melanogaster. Genetics. 1958 May;43(3):547–563. doi: 10.1093/genetics/43.3.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lucchesi J. C. On the origin of sex chromosomes. Bioessays. 1999 Mar;21(3):188–190. doi: 10.1002/(SICI)1521-1878(199903)21:3<188::AID-BIES2>3.0.CO;2-7. [DOI] [PubMed] [Google Scholar]
- McKee B. D., Karpen G. H. Drosophila ribosomal RNA genes function as an X-Y pairing site during male meiosis. Cell. 1990 Apr 6;61(1):61–72. doi: 10.1016/0092-8674(90)90215-z. [DOI] [PubMed] [Google Scholar]
- McKee B. D., Lumsden S. E., Das S. The distribution of male meiotic pairing sites on chromosome 2 of Drosophila melanogaster: meiotic pairing and segregation of 2-Y transpositions. Chromosoma. 1993 Feb;102(3):180–194. doi: 10.1007/BF00387733. [DOI] [PubMed] [Google Scholar]
- Merrill C. J., Chakravarti D., Habera L., Das S., Eisenhour L., McKee B. D. Promoter-containing ribosomal DNA fragments function as X-Y meiotic pairing sites in D. melanogaster males. Dev Genet. 1992;13(6):468–484. doi: 10.1002/dvg.1020130609. [DOI] [PubMed] [Google Scholar]
- Merrill P. T., Sweeton D., Wieschaus E. Requirements for autosomal gene activity during precellular stages of Drosophila melanogaster. Development. 1988 Nov;104(3):495–509. doi: 10.1242/dev.104.3.495. [DOI] [PubMed] [Google Scholar]
- Orr-Weaver T. L. Meiosis in Drosophila: seeing is believing. Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10443–10449. doi: 10.1073/pnas.92.23.10443. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parry D. M., Sandler L. The genetic identification of a heterochromatic segment on the X chromosome of Drosophila melanogaster. Genetics. 1974 Jul;77(3):535–539. doi: 10.1093/genetics/77.3.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pisano C., Bonaccorsi S., Gatti M. The kl-3 loop of the Y chromosome of Drosophila melanogaster binds a tektin-like protein. Genetics. 1993 Mar;133(3):569–579. doi: 10.1093/genetics/133.3.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rasmussen S. W. Meiosis in Bombyx mori females. Philos Trans R Soc Lond B Biol Sci. 1977 Mar 21;277(955):343–350. doi: 10.1098/rstb.1977.0022. [DOI] [PubMed] [Google Scholar]
- Rasmussen S. W. Ultrastructural studies of spermatogenesis in Drosophila melanogaster Meigen. Z Zellforsch Mikrosk Anat. 1973 Jun 20;140(1):125–144. doi: 10.1007/BF00307062. [DOI] [PubMed] [Google Scholar]
- Ren X., Eisenhour L., Hong C., Lee Y., McKee B. D. Roles of rDNA spacer and transcription unit-sequences in X-Y meiotic chromosome pairing in Drosophila melanogaster males. Chromosoma. 1997 Jun;106(1):29–36. doi: 10.1007/s004120050221. [DOI] [PubMed] [Google Scholar]
- Robbins L. G. Are unpaired chromosomes spermicidal?: A maximum-likelihood analysis of segregation and meiotic drive in Drosophila melanogaster males deficient for the ribosomal-dna. Genetics. 1999 Jan;151(1):251–262. doi: 10.1093/genetics/151.1.251. [DOI] [PMC free article] [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]
- Williams B. C., Gatti M., Goldberg M. L. Bipolar spindle attachments affect redistributions of ZW10, a Drosophila centromere/kinetochore component required for accurate chromosome segregation. J Cell Biol. 1996 Sep;134(5):1127–1140. doi: 10.1083/jcb.134.5.1127. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wolf K. W. How meiotic cells deal with non-exchange chromosomes. Bioessays. 1994 Feb;16(2):107–114. doi: 10.1002/bies.950160207. [DOI] [PubMed] [Google Scholar]