Abstract
Segregation distortion is a meiotic drive system, discovered in wild populations, in which males heterozygous for an SD chromosome and a sensitive SD(+) homolog transmit the SD chromosome almost exclusively. SD represents a complex of three closely linked loci in the centromeric region of chromosome 2: Sd, the Segregation distorter gene; E(SD), the Enhancer of Segregation Distortion, required for full expression of drive; and Rsp, the target for the action of Sd, existing in a continuum of states classifiable into sensitive (Rsp(s)) and insensitive (Rsp(i)). In an SD/SD(+) male which is Sd E(SD) Rsp(i)/Sd(+) E(SD)(+) Rsp(s), the Sd and E(SD) elements act jointly to induce the dysfunction of those spermatids receiving the Rsp(s) chromosome. By manipulating the number of copies and the position of the Enhancer region, I demonstrated that: (1) E(SD), whether in its normal position or translocated to the Y chromosome, is able to enhance the degree of Sd-caused distortion in a dosage-dependent manner; (2) even in the absence of Sd, the E(SD) allele in two doses can cause significant distortion, in Sd(+) or Df(Sd)-bearing genotypes; (3) quantitative differences among Enhancers of different sources suggest allelic variation at E(SD), which could account at least in part for differences among wild SD chromosomes in strength of distortion; (4) E(SD)/E(SD)-mediated distortion, like that of Sd, is directed at the Rsp target, whether Rsp is on the second or the Y chromosome; (5) E(SD), like Sd, is suppressed by an unlinked dominant suppressor of SD action. These results show that E(SD) is independently capable of acting on Rsp and is not a simple modifier of the action of Sd. E(SD) provides an example of a trans-acting gene embedded in heterochromatin that can interact with another heterochromatic gene, Rsp, as well as parallel the effect of a euchromatic gene, Sd.
Full Text
The Full Text of this article is available as a PDF (1.9 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bonaccorsi S., Gatti M., Pisano C., Lohe A. Transcription of a satellite DNA on two Y chromosome loops of Drosophila melanogaster. Chromosoma. 1990 Aug;99(4):260–266. doi: 10.1007/BF01731701. [DOI] [PubMed] [Google Scholar]
- Brittnacher J. G., Ganetzky B. On the Components of Segregation Distortion in DROSOPHILA MELANOGASTER. II. Deletion Mapping and Dosage Analysis of the SD Locus. Genetics. 1983 Apr;103(4):659–673. doi: 10.1093/genetics/103.4.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brittnacher J. G., Ganetzky B. On the components of segregation distortion in Drosophila melanogaster. III. Nature of enhancer of SD. Genetics. 1984 Jul;107(3):423–434. doi: 10.1093/genetics/107.3.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Crow J. F. Genes that violate Mendel's rules. Sci Am. 1979 Feb;240(2):134-43, 146. doi: 10.1038/scientificamerican0279-134. [DOI] [PubMed] [Google Scholar]
- Devlin R. H., Bingham B., Wakimoto B. T. The organization and expression of the light gene, a heterochromatic gene of Drosophila melanogaster. Genetics. 1990 May;125(1):129–140. doi: 10.1093/genetics/125.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ganetzky B. On the components of segregation distortion in Drosophila melanogaster. Genetics. 1977 Jun;86(2 Pt 1):321–355. [PMC free article] [PubMed] [Google Scholar]
- Hartl D. L. Complementation analysis of male fertility among the segregation distorter chromosomes of Drosophila melanogaster. Genetics. 1973 Apr;73(4):613–629. doi: 10.1093/genetics/73.4.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hartl D. L. Genetic dissection of segregation distortion II. Mechanism of suppression of distortion by certain inversions. Genetics. 1975 Jul;(3):539–547. doi: 10.1093/genetics/80.3.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hartl D. L. Genetic dissection of segregation distortion. I. Suicide combinations of SD genes. Genetics. 1974 Mar;76(3):477–486. doi: 10.1093/genetics/76.3.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hartl D. L. Genetic dissection of segregation distortion. III. Unequal recovery of reciprocal recombinants. Genetics. 1980 Nov;96(3):685–696. doi: 10.1093/genetics/96.3.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hennig W. Y chromosome function and spermatogenesis in Drosophila hydei. Adv Genet. 1985;23:179–234. doi: 10.1016/s0065-2660(08)60513-1. [DOI] [PubMed] [Google Scholar]
- Hilliker A. J., Appels R., Schalet A. The genetic analysis of D. melanogaster heterochromatin. Cell. 1980 Oct;21(3):607–619. doi: 10.1016/0092-8674(80)90424-9. [DOI] [PubMed] [Google Scholar]
- Hilliker A. J. Genetic analysis of the centromeric heterochromatin of chromosome 2 of Drosophila melanogaster: deficiency mapping of EMS-induced lethal complementation groups. Genetics. 1976 Aug;83(4):765–782. doi: 10.1093/genetics/83.4.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hiraizumi Y., Martin D. W., Eckstrand I. A. A Modified Model of Segregation Distortion in DROSOPHILA MELANOGASTER. Genetics. 1980 Jul;95(3):693–706. doi: 10.1093/genetics/95.3.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hiraizumi Y., Nakazima K. Deviant sex ratio associated with segregation distortion in Drosophila melanogaster. Genetics. 1967 Apr;55(4):681–697. doi: 10.1093/genetics/55.4.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hiraizumi Y., Thomas A. M. Suppressor Systems of Segregation Distorter (SD) Chromosomes in Natural Populations of DROSOPHILA MELANOGASTER. Genetics. 1984 Feb;106(2):279–292. doi: 10.1093/genetics/106.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hiraizumi Y, Crow J F. Heterozygous Effects on Viability, Fertility, Rate of Development, and Longevity of Drosophila Chromosomes That Are Lethal When Homozygous. Genetics. 1960 Aug;45(8):1071–1083. doi: 10.1093/genetics/45.8.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lyon M. F. Male sterility of the mouse t-complex is due to homozygosity of the distorter genes. Cell. 1986 Jan 31;44(2):357–363. doi: 10.1016/0092-8674(86)90770-1. [DOI] [PubMed] [Google Scholar]
- Lyon M. F. Transmission ratio distortion in mouse t-haplotypes is due to multiple distorter genes acting on a responder locus. Cell. 1984 Jun;37(2):621–628. doi: 10.1016/0092-8674(84)90393-3. [DOI] [PubMed] [Google Scholar]
- Lyttle T. W. Additive Effects of Multiple SEGREGATION DISTORTER ( SD) Chromosomes on Sperm Dysfunction in DROSOPHILA MELANOGASTER. Genetics. 1986 Sep;114(1):203–216. doi: 10.1093/genetics/114.1.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lyttle T. W., Brittnacher J. G., Ganetzky B. Detection of Rsp and modifier variation in the meiotic drive system Segregation distorter (SD) of Drosophila melanogaster. Genetics. 1986 Sep;114(1):183–202. doi: 10.1093/genetics/114.1.183. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lyttle T. W. Chromosomal Control of Fertility in DROSOPHILA MELANOGASTER . I. Rescue of T(Y;A)/bb Male Sterility by Chromosome Rearrangement. Genetics. 1984 Mar;106(3):423–434. doi: 10.1093/genetics/106.3.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lyttle T. W. The effect of novel chromosome position and variable dose on the genetic behavior of the Responder (Rsp) element of the Segregation distorter (SD) system of Drosophila melanogaster. Genetics. 1989 Apr;121(4):751–763. doi: 10.1093/genetics/121.4.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marchant G. E., Holm D. G. Genetic analysis of the heterochromatin of chromosome 3 in Drosophila melanogaster. I. Products of compound-autosome detachment. Genetics. 1988 Oct;120(2):503–517. doi: 10.1093/genetics/120.2.503. [DOI] [PMC free article] [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]
- Miklos G. L. An investigation of the components of Segregation-Distorter systems in Drosophila melanogaster. Genetics. 1972 Mar;70(3):405–418. doi: 10.1093/genetics/70.3.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miklos G. L., Smith-White S. An analysis of the instability of segregation-distorter in Drosophila melanogaster. Genetics. 1971 Feb;67(2):305–317. doi: 10.1093/genetics/67.2.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pimpinelli S., Dimitri P. Cytogenetic analysis of segregation distortion in Drosophila melanogaster: the cytological organization of the Responder (Rsp) locus. Genetics. 1989 Apr;121(4):765–772. doi: 10.1093/genetics/121.4.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pimpinelli S., Sullivan W., Prout M., Sandler L. On biological functions mapping to the heterochromatin of Drosophila melanogaster. Genetics. 1985 Apr;109(4):701–724. doi: 10.1093/genetics/109.4.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sandler L., Hiraizumi Y. MEIOTIC DRIVE IN NATURAL POPULATIONS OF DROSOPHILA MELANOGASTER. II. GENETIC VARIATION AT THE SEGREGATION-DISTORTER LOCUS. Proc Natl Acad Sci U S A. 1959 Sep;45(9):1412–1422. doi: 10.1073/pnas.45.9.1412. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sandler L, Hiraizumi Y. Meiotic Drive in Natural Populations of Drosophila Melanogaster. V. on the Nature of the Sd Region. Genetics. 1960 Dec;45(12):1671–1689. doi: 10.1093/genetics/45.12.1671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silver L. M., Remis D. Five of the nine genetically defined regions of mouse t haplotypes are involved in transmission ratio distortion. Genet Res. 1987 Feb;49(1):51–56. doi: 10.1017/s0016672300026720. [DOI] [PubMed] [Google Scholar]
- Sullivan W., Pimpinelli S. The genetic factors altered in homozygous abo stocks of Drosophila melanogaster. Genetics. 1986 Nov;114(3):885–895. doi: 10.1093/genetics/114.3.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Temin R. G., Marthas M. Factors Influencing the Effect of Segregation Distortion in Natural Populations of DROSOPHILA MELANOGASTER. Genetics. 1984 Jul;107(3):375–393. doi: 10.1093/genetics/107.3.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tokuyasu K. T., Peacock W. J., Hardy R. W. Dynamics of spermiogenesis in Drosophila melanogaster. VII. Effects of segregation distorter (SD) chromosome. J Ultrastruct Res. 1977 Jan;58(1):96–107. doi: 10.1016/s0022-5320(77)80011-7. [DOI] [PubMed] [Google Scholar]
- Wu C. I., Lyttle T. W., Wu M. L., Lin G. F. Association between a satellite DNA sequence and the Responder of Segregation Distorter in D. melanogaster. Cell. 1988 Jul 15;54(2):179–189. doi: 10.1016/0092-8674(88)90550-8. [DOI] [PubMed] [Google Scholar]