Abstract
In Caenorhabditis elegans triploid animals with two X chromosomes (symbolized 3A;2X) are males. However, these triploid males can be feminized by making them mutant for recessive dosage compensation mutations, by adding X chromosome duplications or by microinjecting particular DNA sequences termed feminizing elements. None of these treatments affects diploid males. This study explores several aspects of these treatments in polyploids. The dosage compensation mutants exhibit a strong maternal effect, such that reduction of any of the dosage compensation gene functions in the mother leads to sex reversal of 3A;2X animals. Likewise, all X chromosome duplications tested cause both sex reversal and intersexual development of many 3A;2X animals. Microinjected feminizing element DNA does not cause extensive sex reversal, but does result in intersexual development in 3A;2X animals. Neither X chromosome duplications nor microinjected feminizing elements show the extreme maternal effect of the dosage compensation mutants, although there is indirect evidence for a maternal effect of the feminizing elements. In particular, very little feminizing element DNA needs to be microinjected in order to feminize triploid males, far less than what is needed for stable inheritance, implying that feminizing elements can work within the mother's gonad. However, even very high concentrations of microinjected feminizing elements do not affect sex determination in diploid males, suggesting that they are not part of the numerator of the X/A ratio. In addition, no pair of X chromosome duplications feminizes diploid males, suggesting that none of these duplications contains a numerator of the X/A ratio. Instead, I infer that an X-linked locus, as yet undefined, must be present in two copies for hermaphrodite development to ensue or that the two X chromosomes might interact.
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Selected References
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- Baker B. S., Belote J. M. Sex determination and dosage compensation in Drosophila melanogaster. Annu Rev Genet. 1983;17:345–393. doi: 10.1146/annurev.ge.17.120183.002021. [DOI] [PubMed] [Google Scholar]
- Cline T. W. A female-specific lethal lesion in an X-linked positive regulator of the Drosophila sex determination gene, Sex-lethal. Genetics. 1986 Jul;113(3):641–663. doi: 10.1093/genetics/113.3.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cline T. W. Autoregulatory functioning of a Drosophila gene product that establish es and maintains the sexually determined state. Genetics. 1984 Jun;107(2):231–277. doi: 10.1093/genetics/107.2.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cline T. W. Evidence that sisterless-a and sisterless-b are two of several discrete "numerator elements" of the X/A sex determination signal in Drosophila that switch Sxl between two alternative stable expression states. Genetics. 1988 Aug;119(4):829–862. doi: 10.1093/genetics/119.4.829. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cline T. W. The Drosophila sex determination signal: how do flies count to two? Trends Genet. 1993 Nov;9(11):385–390. doi: 10.1016/0168-9525(93)90138-8. [DOI] [PubMed] [Google Scholar]
- DeLong L., Plenefisch J. D., Klein R. D., Meyer B. J. Feedback control of sex determination by dosage compensation revealed through Caenorhabditis elegans sdc-3 mutations. Genetics. 1993 Apr;133(4):875–896. doi: 10.1093/genetics/133.4.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorman M., Kuroda M. I., Baker B. S. Regulation of the sex-specific binding of the maleless dosage compensation protein to the male X chromosome in Drosophila. Cell. 1993 Jan 15;72(1):39–49. doi: 10.1016/0092-8674(93)90048-u. [DOI] [PubMed] [Google Scholar]
- Henikoff S., Eghtedarzadeh M. K. Conserved arrangement of nested genes at the Drosophila Gart locus. Genetics. 1987 Dec;117(4):711–725. doi: 10.1093/genetics/117.4.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herman R. K., Kari C. K., Hartman P. S. Dominant X-chromosome nondisjunction mutants of Caenorhabditis elegans. Genetics. 1982 Nov;102(3):379–400. doi: 10.1093/genetics/102.3.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herman R. K., Kari C. K. Recombination between small X chromosome duplications and the X chromosome in Caenorhabditis elegans. Genetics. 1989 Apr;121(4):723–737. doi: 10.1093/genetics/121.4.723. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herman R. K., Madl J. E., Kari C. K. Duplications in Caenorhabditis elegans. Genetics. 1979 Jun;92(2):419–435. doi: 10.1093/genetics/92.2.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hodgkin J., Horvitz H. R., Brenner S. Nondisjunction Mutants of the Nematode CAENORHABDITIS ELEGANS. Genetics. 1979 Jan;91(1):67–94. doi: 10.1093/genetics/91.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hodgkin J. Primary sex determination in the nematode C. elegans. Development. 1987;101 (Suppl):5–16. doi: 10.1242/dev.101.Supplement.5. [DOI] [PubMed] [Google Scholar]
- Hodgkin J. Sex determination and dosage compensation in Caenorhabditis elegans. Annu Rev Genet. 1987;21:133–154. doi: 10.1146/annurev.ge.21.120187.001025. [DOI] [PubMed] [Google Scholar]
- Jeppesen P., Turner B. M. The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell. 1993 Jul 30;74(2):281–289. doi: 10.1016/0092-8674(93)90419-q. [DOI] [PubMed] [Google Scholar]
- Kuroda M. I., Kernan M. J., Kreber R., Ganetzky B., Baker B. S. The maleless protein associates with the X chromosome to regulate dosage compensation in Drosophila. Cell. 1991 Sep 6;66(5):935–947. doi: 10.1016/0092-8674(91)90439-6. [DOI] [PubMed] [Google Scholar]
- Lucchesi J. C., Manning J. E. Gene dosage compensation in Drosophila melanogaster. Adv Genet. 1987;24:371–429. doi: 10.1016/s0065-2660(08)60013-9. [DOI] [PubMed] [Google Scholar]
- Madl J. E., Herman R. K. Polyploids and sex determination in Caenorhabditis elegans. Genetics. 1979 Oct;93(2):393–402. doi: 10.1093/genetics/93.2.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McCoubrey W. K., Nordstrom K. D., Meneely P. M. Microinjected DNA from the X chromosome affects sex determination in Caenorhabditis elegans. Science. 1988 Nov 25;242(4882):1146–1151. doi: 10.1126/science.2973125. [DOI] [PubMed] [Google Scholar]
- Mello C. C., Kramer J. M., Stinchcomb D., Ambros V. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991 Dec;10(12):3959–3970. doi: 10.1002/j.1460-2075.1991.tb04966.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meneely P. M., Nordstrom K. D. X chromosome duplications affect a region of the chromosome they do not duplicate in Caenorhabditis elegans. Genetics. 1988 Jun;119(2):365–375. doi: 10.1093/genetics/119.2.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meneely P. M., Wood W. B. An autosomal gene that affects X chromosome expression and sex determination in Caenorhabditis elegans. Genetics. 1984 Jan;106(1):29–44. doi: 10.1093/genetics/106.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nonet M. L., Meyer B. J. Early aspects of Caenorhabditis elegans sex determination and dosage compensation are regulated by a zinc-finger protein. Nature. 1991 May 2;351(6321):65–68. doi: 10.1038/351065a0. [DOI] [PubMed] [Google Scholar]
- Palmer M. J., Mergner V. A., Richman R., Manning J. E., Kuroda M. I., Lucchesi J. C. The male-specific lethal-one (msl-1) gene of Drosophila melanogaster encodes a novel protein that associates with the X chromosome in males. Genetics. 1993 Jun;134(2):545–557. doi: 10.1093/genetics/134.2.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parkhurst S. M., Ish-Horowicz D. Common denominators for sex. Curr Biol. 1992 Dec;2(12):629–631. doi: 10.1016/0960-9822(92)90097-t. [DOI] [PubMed] [Google Scholar]
- Plenefisch J. D., DeLong L., Meyer B. J. Genes that implement the hermaphrodite mode of dosage compensation in Caenorhabditis elegans. Genetics. 1989 Jan;121(1):57–76. doi: 10.1093/genetics/121.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tartof K. D., Henikoff S. Trans-sensing effects from Drosophila to humans. Cell. 1991 Apr 19;65(2):201–203. doi: 10.1016/0092-8674(91)90153-p. [DOI] [PubMed] [Google Scholar]
- Turner B. M., Birley A. J., Lavender J. Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell. 1992 Apr 17;69(2):375–384. doi: 10.1016/0092-8674(92)90417-b. [DOI] [PubMed] [Google Scholar]
- Villeneuve A. M., Meyer B. J. The regulatory hierarchy controlling sex determination and dosage compensation in Caenorhabditis elegans. Adv Genet. 1990;27:117–188. doi: 10.1016/s0065-2660(08)60025-5. [DOI] [PubMed] [Google Scholar]