Abstract
The cytoplasmically inherited bacterium Wolbachia pipientis is a widespread parasite of arthropods that manipulates the reproductive biology of its hosts, often to their detriment, in order to foster its own transmission through egg cytoplasm1,2. Here we report that infection by Wolbachia restores fertility to Drosophila melanogaster mutant females prevented from making eggs by protein-coding lesions in Sex-lethal (Sxl), the master regulator of sex determination. Suppression of sterility by Wolbachia discriminates markedly among similar germline-specific Sxl alleles, and is not observed for mutations in other genes that produce similar ‘tumorous ovary’ phenotypes, including one that blocks Sxl germline expression. This allele and gene specificity indicates that suppression probably results from a specific interaction with Sxl protein, rather than from a bypass of the normal germline requirement for this developmental regulator or from an effect on Sxl expression. The Sxl–Wolbachia interaction provides a rare opportunity to explore host–parasite relationships at the molecular level in a model insect. Furthermore, demonstration that a parasite infection can counteract the deleterious effects of mutations in host genes illustrates how hosts might become dependent on parasites.
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References
Werren, J. H. Biology of Wolbachia. Annu. Rev. Entomol. 42, 587–609 (1997)
Knight, J. Meet the Herod bug. Nature 412, 12–14 (2001)
Werren, J. H. & O'Neill, S. L. in Influential Passengers: Inherited Microorganisms and Arthropod Reproduction (eds O'Neill, S. L., Hoffman, A. A. & Werren, J. H.) 1–41 (Oxford Univ. Press, Oxford, 1997)
Huigens, M. E. et al. Infectious parthenogenesis. Nature 405, 178–179 (2000)
Bouchon, D., Rigaud, T. & Juchault, P. Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization. Proc. R. Soc. Lond. B 265, 1081–1090 (1998)
Hurst, G. D. D., Johnson, A. P., Schulenburg, J. H. G. & Fuyama, Y. Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics 156, 699–709 (2000)
Boyle, L., O'Neill, S. L., Robertson, H. M. & Karr, T. L. Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260, 1796–1799 (1993)
Bordenstein, S. R., O'Hara, F. P. & Werren, J. H. Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409, 707–710 (2001)
Dedeine, F. et al. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc. Natl Acad. Sci. USA 98, 6247–6252 (2001)
Bourtzis, K., Nirgianaki, A., Markakis, G. & Savakis, C. Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 144, 1063–1073 (1996)
Min, K. T. & Benzer, S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Natl Acad. Sci. USA 94, 10792–10796 (1997)
Cline, T. W. & Meyer, B. J. Vive la différence: males vs females in flies vs worms. Annu. Rev. Genet. 30, 637–702 (1996)
Schupbach, T. Normal female germ cell differentiation requires the female X-chromosome to autosome ratio and expression of Sex-lethal in Drosophila melanogaster. Genetics 109, 529–548 (1985)
Cook, K. R. Regulation of Recombination and Oogenesis by the ovarian tumor, Sex-lethal, and ovo Genes of Drosophila melanogaster. Thesis no. 381, Univ. Iowa (1993)
Salz, H. K., Cline, T. W. & Schedl, P. Functional changes associated with structural alterations induced by mobilization of a P element inserted in the Sex-lethal gene of Drosophila. Genetics 117, 221–231 (1987)
Perrimon, N., Mohler, D., Engstrom, L. & Mahowald, A. P. X-linked female-sterile loci in Drosophila melanogaster. Genetics 113, 695–712 (1986)
Bopp, D., Horabin, J. I., Lersch, R. A., Cline, T. W. & Schedl, P. Expression of the Sex-lethal gene is controlled at multiple levels during Drosophila oogenesis. Development 118, 797–812 (1993)
Dines, J. L. New Aspects of Functional Complexity for the Master Regulator of Drosophila melanogaster Sex Determination Thesis no. 319, Univ. California, Berkeley (2001)
O'Neill, S. L., Giordano, R., Colbert, A. M. E., Karr, T. L. & Robertson, H. M. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl Acad. Sci. USA 89, 2699–2702 (1999)
Bopp, D., Schutt, C., Puro, J., Huang, H. & Nothiger, R. Recombination and disjunction in female germ cells of Drosophila depend on the germline activity of the gene Sex-lethal. Development 126, 5785–5794 (1999)
Dines, J., Lersch, B., Lu, B., Bell, M. & Cline, T. W. Functional specialization of SEX-LETHAL protein isoforms. Annu. Drosophila Res. Conf. Program Abs. Vol. 39, a245 (1998)
Salz, H. K. et al. The Drosophila female-specific sex-determination gene, Sex-lethal, has stage-, tissue-, and sex-specific RNAs suggesting multiple modes of regulation. Genes Dev. 3, 708–719 (1989)
Oliver, B., Perrimon, N. & Mahowald, A. P. Genetic evidence that the sans fille locus is involved in Drosophila sex determination. Genetics 120, 159–172 (1988)
Steinmann-Zwicky, M. Sex determination in Drosophila: the X-chromosomal gene liz is required for Sxl activity. EMBO J. 7, 3889–3898 (1988)
Pauli, D., Oliver, B. & Mahowald, A. P. The role of the ovarian tumor locus in Drosophila melanogaster germline sex determination. Development 119, 123–134 (1993)
Page, S. L., McKim, K. S., Deneen, B., Van Hook, T. L. & Hawley, S. R. Genetic studies of mei-P26 reveal a link between the processes that control germ cell proliferation in both sexes and those that control meiotic exchange in Drosophila. Genetics 155, 1757–1772 (2000)
Hager, J. H. & Cline, T. W. Induction of female Sex-lethal RNA splicing in male germ cells: implications for Drosophila germline sex determination. Development 124, 5033–5048 (1997)
Cline, T. W. A male-specific lethal mutation in Drosophila melanogaster that transforms sex. Dev. Biol. 72, 266–275 (1979)
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 119, 829–862 (1988)
Acknowledgements
We thank L. Sefton for generating the original suppressed Sxlf4 strain, D. Presgraves for the y w CS Wolbachia strain, and B. J. Meyer for comments on the manuscript.
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Starr, D., Cline, T. A host–parasite interaction rescues Drosophila oogenesis defects. Nature 418, 76–79 (2002). https://doi.org/10.1038/nature00843
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DOI: https://doi.org/10.1038/nature00843
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