Abstract
In a variety of tissues in eukaryotes, multipotential stem cells are responsible for maintaining a germinal population and generating a differentiated progeny. The Drosophila germline is one such tissue where a continuous supply of eggs or sperm relies on the normal functioning of stem cells. Recent studies have implicated a possible role for the posterior determinant gene nanos (nos) in stem cells. Here, I report that nanos is required in the Drosophila female germline as well as in the male germline. In the female, nos is required for the functioning of stem cells. In nos mutants, while the stem cells are specified, these cells divide only a few times at the most and then degenerate. The loss of germline stem cells in nos mutant mothers appears to be due to a progressive degeneration of the plasma membrane. Furthermore, following germ cell loss, the germaria in the nos mutant mothers appear to carry on massive mitochondrial biogenesis activity. Thus, the syncytia of such germaria are filled with mitochondria. In the male germline, the male fertility assay indicates that nos appears to be also required for the maintenance of stem cells. In these mutant males, spermatogenesis is progressively affected and these males eventually become sterile. These results indicate novel requirements for nos in the Drosophila germline.
Full Text
The Full Text of this article is available as a PDF (1.1 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Attardi G., Schatz G. Biogenesis of mitochondria. Annu Rev Cell Biol. 1988;4:289–333. doi: 10.1146/annurev.cb.04.110188.001445. [DOI] [PubMed] [Google Scholar]
- BROWN E. H., KING R. C. STUDIES ON THE EVENTS RESULTING IN THE FORMATION OF AN EGG CHAMBER IN DROSOPHILA MELANOGASTER. Growth. 1964 Mar;28:41–81. [PubMed] [Google Scholar]
- Bhat K. M., Farkas G., Karch F., Gyurkovics H., Gausz J., Schedl P. The GAGA factor is required in the early Drosophila embryo not only for transcriptional regulation but also for nuclear division. Development. 1996 Apr;122(4):1113–1124. doi: 10.1242/dev.122.4.1113. [DOI] [PubMed] [Google Scholar]
- Bhat K. M., Schedl P. Establishment of stem cell identity in the Drosophila germline. Dev Dyn. 1997 Dec;210(4):371–382. doi: 10.1002/(SICI)1097-0177(199712)210:4<371::AID-AJA2>3.0.CO;2-D. [DOI] [PubMed] [Google Scholar]
- Bhat K. M., Schedl P. Requirement for engrailed and invected genes reveals novel regulatory interactions between engrailed/invected, patched, gooseberry and wingless during Drosophila neurogenesis. Development. 1997 May;124(9):1675–1688. doi: 10.1242/dev.124.9.1675. [DOI] [PubMed] [Google Scholar]
- 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. 1993 Jul;118(3):797–812. doi: 10.1242/dev.118.3.797. [DOI] [PubMed] [Google Scholar]
- Curtis D., Apfeld J., Lehmann R. nanos is an evolutionarily conserved organizer of anterior-posterior polarity. Development. 1995 Jun;121(6):1899–1910. doi: 10.1242/dev.121.6.1899. [DOI] [PubMed] [Google Scholar]
- Dalby B., Glover D. M. Discrete sequence elements control posterior pole accumulation and translational repression of maternal cyclin B RNA in Drosophila. EMBO J. 1993 Mar;12(3):1219–1227. doi: 10.1002/j.1460-2075.1993.tb05763.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dexter T. M., Spooncer E. Growth and differentiation in the hemopoietic system. Annu Rev Cell Biol. 1987;3:423–441. doi: 10.1146/annurev.cb.03.110187.002231. [DOI] [PubMed] [Google Scholar]
- Forbes A., Lehmann R. Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development. 1998 Feb;125(4):679–690. doi: 10.1242/dev.125.4.679. [DOI] [PubMed] [Google Scholar]
- Forristall C., Pondel M., Chen L., King M. L. Patterns of localization and cytoskeletal association of two vegetally localized RNAs, Vg1 and Xcat-2. Development. 1995 Jan;121(1):201–208. doi: 10.1242/dev.121.1.201. [DOI] [PubMed] [Google Scholar]
- Gavis E. R., Lehmann R. Localization of nanos RNA controls embryonic polarity. Cell. 1992 Oct 16;71(2):301–313. doi: 10.1016/0092-8674(92)90358-j. [DOI] [PubMed] [Google Scholar]
- Hall P. A., Watt F. M. Stem cells: the generation and maintenance of cellular diversity. Development. 1989 Aug;106(4):619–633. doi: 10.1242/dev.106.4.619. [DOI] [PubMed] [Google Scholar]
- Hülskamp M., Pfeifle C., Tautz D. A morphogenetic gradient of hunchback protein organizes the expression of the gap genes Krüppel and knirps in the early Drosophila embryo. Nature. 1990 Aug 9;346(6284):577–580. doi: 10.1038/346577a0. [DOI] [PubMed] [Google Scholar]
- Hülskamp M., Schröder C., Pfeifle C., Jäckle H., Tautz D. Posterior segmentation of the Drosophila embryo in the absence of a maternal posterior organizer gene. Nature. 1989 Apr 20;338(6217):629–632. doi: 10.1038/338629a0. [DOI] [PubMed] [Google Scholar]
- Irish V., Lehmann R., Akam M. The Drosophila posterior-group gene nanos functions by repressing hunchback activity. Nature. 1989 Apr 20;338(6217):646–648. doi: 10.1038/338646a0. [DOI] [PubMed] [Google Scholar]
- Kloc M., Etkin L. D. Two distinct pathways for the localization of RNAs at the vegetal cortex in Xenopus oocytes. Development. 1995 Feb;121(2):287–297. doi: 10.1242/dev.121.2.287. [DOI] [PubMed] [Google Scholar]
- Kobayashi S., Yamada M., Asaoka M., Kitamura T. Essential role of the posterior morphogen nanos for germline development in Drosophila. Nature. 1996 Apr 25;380(6576):708–711. doi: 10.1038/380708a0. [DOI] [PubMed] [Google Scholar]
- Koch E. A., King R. C. The origin and early differentiation of the egg chamber of Drosophila melanogaster. J Morphol. 1966 Jul;119(3):283–303. doi: 10.1002/jmor.1051190303. [DOI] [PubMed] [Google Scholar]
- Lantz V., Ambrosio L., Schedl P. The Drosophila orb gene is predicted to encode sex-specific germline RNA-binding proteins and has localized transcripts in ovaries and early embryos. Development. 1992 May;115(1):75–88. doi: 10.1242/dev.115.1.75. [DOI] [PubMed] [Google Scholar]
- Lantz V., Chang J. S., Horabin J. I., Bopp D., Schedl P. The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev. 1994 Mar 1;8(5):598–613. doi: 10.1101/gad.8.5.598. [DOI] [PubMed] [Google Scholar]
- Lasko P. F., Ashburner M. Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development. Genes Dev. 1990 Jun;4(6):905–921. doi: 10.1101/gad.4.6.905. [DOI] [PubMed] [Google Scholar]
- Lehmann R., Nüsslein-Volhard C. The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo. Development. 1991 Jul;112(3):679–691. doi: 10.1242/dev.112.3.679. [DOI] [PubMed] [Google Scholar]
- Lin H., Spradling A. C. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development. 1997 Jun;124(12):2463–2476. doi: 10.1242/dev.124.12.2463. [DOI] [PubMed] [Google Scholar]
- Lin H., Spradling A. C. Germline stem cell division and egg chamber development in transplanted Drosophila germaria. Dev Biol. 1993 Sep;159(1):140–152. doi: 10.1006/dbio.1993.1228. [DOI] [PubMed] [Google Scholar]
- McKearin D. M., Spradling A. C. bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev. 1990 Dec;4(12B):2242–2251. doi: 10.1101/gad.4.12b.2242. [DOI] [PubMed] [Google Scholar]
- Mosquera L., Forristall C., Zhou Y., King M. L. A mRNA localized to the vegetal cortex of Xenopus oocytes encodes a protein with a nanos-like zinc finger domain. Development. 1993 Jan;117(1):377–386. doi: 10.1242/dev.117.1.377. [DOI] [PubMed] [Google Scholar]
- Rinaldi A. M., De Leo G., Arzone A., Salcher I., Storace A., Mutolo V. Biochemical and electron microscopic evidence that cell nucleus negatively controls mitochondrial genomic activity in early sea urchin development. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1916–1920. doi: 10.1073/pnas.76.4.1916. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schüpbach T., Wieschaus E. Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations. Genetics. 1989 Jan;121(1):101–117. doi: 10.1093/genetics/121.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schüpbach T., Wieschaus E. Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics. 1991 Dec;129(4):1119–1136. doi: 10.1093/genetics/129.4.1119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Struhl G., Johnston P., Lawrence P. A. Control of Drosophila body pattern by the hunchback morphogen gradient. Cell. 1992 Apr 17;69(2):237–249. doi: 10.1016/0092-8674(92)90405-2. [DOI] [PubMed] [Google Scholar]
- Tautz D. Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres. Nature. 1988 Mar 17;332(6161):281–284. doi: 10.1038/332281a0. [DOI] [PubMed] [Google Scholar]
- Wieschaus E., Szabad J. The development and function of the female germ line in Drosophila melanogaster: a cell lineage study. Dev Biol. 1979 Jan;68(1):29–46. doi: 10.1016/0012-1606(79)90241-0. [DOI] [PubMed] [Google Scholar]
