Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1999 Sep;153(1):235–250. doi: 10.1093/genetics/153.1.235

The Drosophila pumilio gene encodes two functional protein isoforms that play multiple roles in germline development, gonadogenesis, oogenesis and embryogenesis.

M Parisi 1, H Lin 1
PMCID: PMC1460748  PMID: 10471709

Abstract

The pumilio (pum) gene plays an essential role in embryonic patterning and germline stem cell (GSC) maintenance during oogenesis in Drosophila. Here we report on a phenotypic analysis using pum(ovarette) mutations, which reveals multiple functions of pum in primordial germ cell proliferation, larval ovary formation, GSC division, and subsequent oogenic processes, as well as in oviposition. Specifically, by inducing pum(-) GSC clones at the onset of oogenesis, we show that pum is directly involved in GSC division, a function that is distinct from its requirement in primordial germ cells. Furthermore, we show that pum encodes 156- and 130-kD proteins, both of which are functional isoforms. Among pum(ovarette) mutations, pum(1688) specifically eliminates the 156-kD isoform but not the 130-kD isoform, while pum(2003) and pum(4277) specifically affect the 130-kD isoform but not the 156-kD isoform. Normal doses of both isoforms are required for the zygotic function of pum, yet either isoform alone at a normal dose is sufficient for the maternal effect function of pum. A pum cDNA transgene that contains the known open reading frame encodes only the 156-kD isoform and rescues the phenotype of both pum(1688) and pum(2003) mutants. These observations suggest that the 156- and 130-kD isoforms can compensate for each other's function in a dosage-dependent manner. Finally, we present molecular evidence suggesting that the two PUM isoforms share some of their primary structures.

Full Text

The Full Text of this article is available as a PDF (645.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barker D. D., Wang C., Moore J., Dickinson L. K., Lehmann R. Pumilio is essential for function but not for distribution of the Drosophila abdominal determinant Nanos. Genes Dev. 1992 Dec;6(12A):2312–2326. doi: 10.1101/gad.6.12a.2312. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Chou T. B., Perrimon N. Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics. 1992 Jul;131(3):643–653. doi: 10.1093/genetics/131.3.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cox D. N., Chao A., Baker J., Chang L., Qiao D., Lin H. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 1998 Dec 1;12(23):3715–3727. doi: 10.1101/gad.12.23.3715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Deng W., Lin H. Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of a polarized microtubule array for oocyte specification in Drosophila. Dev Biol. 1997 Sep 1;189(1):79–94. doi: 10.1006/dbio.1997.8669. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Godt D., Laski F. A. Mechanisms of cell rearrangement and cell recruitment in Drosophila ovary morphogenesis and the requirement of bric à brac. Development. 1995 Jan;121(1):173–187. doi: 10.1242/dev.121.1.173. [DOI] [PubMed] [Google Scholar]
  8. Hay B., Jan L. Y., Jan Y. N. Localization of vasa, a component of Drosophila polar granules, in maternal-effect mutants that alter embryonic anteroposterior polarity. Development. 1990 Jun;109(2):425–433. doi: 10.1242/dev.109.2.425. [DOI] [PubMed] [Google Scholar]
  9. Holland P. V., Purcell R. H., Smith H., Alter H. J. Subtyping of hepatitis-associated antigen (HB-Ag); simplified technique with counterelectrophoresis. J Immunol. 1972 Sep;109(3):420–425. [PubMed] [Google Scholar]
  10. Horowitz H., Berg C. A. Aberrant splicing and transcription termination caused by P element insertion into the intron of a Drosophila gene. Genetics. 1995 Jan;139(1):327–335. doi: 10.1093/genetics/139.1.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Jaglarz M. K., Howard K. R. Primordial germ cell migration in Drosophila melanogaster is controlled by somatic tissue. Development. 1994 Jan;120(1):83–89. doi: 10.1242/dev.120.1.83. [DOI] [PubMed] [Google Scholar]
  13. King F. J., Lin H. Somatic signaling mediated by fs(1)Yb is essential for germline stem cell maintenance during Drosophila oogenesis. Development. 1999 May;126(9):1833–1844. doi: 10.1242/dev.126.9.1833. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. Lin H. The self-renewing mechanism of stem cells in the germline. Curr Opin Cell Biol. 1998 Dec;10(6):687–693. doi: 10.1016/s0955-0674(98)80108-7. [DOI] [PubMed] [Google Scholar]
  17. Lin H., Yue L., Spradling A. C. The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development. 1994 Apr;120(4):947–956. doi: 10.1242/dev.120.4.947. [DOI] [PubMed] [Google Scholar]
  18. Macdonald P. M. The Drosophila pumilio gene: an unusually long transcription unit and an unusual protein. Development. 1992 Jan;114(1):221–232. doi: 10.1242/dev.114.1.221. [DOI] [PubMed] [Google Scholar]
  19. Manseau L. J., Schüpbach T. The egg came first, of course! Anterior-posterior pattern formation in Drosophila embryogenesis and oogenesis. Trends Genet. 1989 Dec;5(12):400–405. doi: 10.1016/0168-9525(89)90198-4. [DOI] [PubMed] [Google Scholar]
  20. Moore L. A., Broihier H. T., Van Doren M., Lunsford L. B., Lehmann R. Identification of genes controlling germ cell migration and embryonic gonad formation in Drosophila. Development. 1998 Feb;125(4):667–678. doi: 10.1242/dev.125.4.667. [DOI] [PubMed] [Google Scholar]
  21. Nakamura A., Amikura R., Mukai M., Kobayashi S., Lasko P. F. Requirement for a noncoding RNA in Drosophila polar granules for germ cell establishment. Science. 1996 Dec 20;274(5295):2075–2079. doi: 10.1126/science.274.5295.2075. [DOI] [PubMed] [Google Scholar]
  22. Nüsslein-Volhard C., Frohnhöfer H. G., Lehmann R. Determination of anteroposterior polarity in Drosophila. Science. 1987 Dec 18;238(4834):1675–1681. doi: 10.1126/science.3686007. [DOI] [PubMed] [Google Scholar]
  23. Rørth P. A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12418–12422. doi: 10.1073/pnas.93.22.12418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schüpbach T., Roth S. Dorsoventral patterning in Drosophila oogenesis. Curr Opin Genet Dev. 1994 Aug;4(4):502–507. doi: 10.1016/0959-437x(94)90064-a. [DOI] [PubMed] [Google Scholar]
  25. Struhl G. Differing strategies for organizing anterior and posterior body pattern in Drosophila embryos. Nature. 1989 Apr 27;338(6218):741–744. doi: 10.1038/338741a0. [DOI] [PubMed] [Google Scholar]
  26. Wharton R. P., Sonoda J., Lee T., Patterson M., Murata Y. The Pumilio RNA-binding domain is also a translational regulator. Mol Cell. 1998 May;1(6):863–872. doi: 10.1016/s1097-2765(00)80085-4. [DOI] [PubMed] [Google Scholar]
  27. Wharton R. P., Struhl G. RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos. Cell. 1991 Nov 29;67(5):955–967. doi: 10.1016/0092-8674(91)90368-9. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Williamson A., Lehmann R. Germ cell development in Drosophila. Annu Rev Cell Dev Biol. 1996;12:365–391. doi: 10.1146/annurev.cellbio.12.1.365. [DOI] [PubMed] [Google Scholar]
  30. Wreden C., Verrotti A. C., Schisa J. A., Lieberfarb M. E., Strickland S. Nanos and pumilio establish embryonic polarity in Drosophila by promoting posterior deadenylation of hunchback mRNA. Development. 1997 Aug;124(15):3015–3023. doi: 10.1242/dev.124.15.3015. [DOI] [PubMed] [Google Scholar]
  31. Zaccai M., Lipshitz H. D. Differential distributions of two adducin-like protein isoforms in the Drosophila ovary and early embryo. Zygote. 1996 May;4(2):159–166. doi: 10.1017/s096719940000304x. [DOI] [PubMed] [Google Scholar]
  32. Zamore P. D., Bartel D. P., Lehmann R., Williamson J. R. The PUMILIO-RNA interaction: a single RNA-binding domain monomer recognizes a bipartite target sequence. Biochemistry. 1999 Jan 12;38(2):596–604. doi: 10.1021/bi982264s. [DOI] [PubMed] [Google Scholar]
  33. Zamore P. D., Williamson J. R., Lehmann R. The Pumilio protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins. RNA. 1997 Dec;3(12):1421–1433. [PMC free article] [PubMed] [Google Scholar]
  34. Zhang N., Zhang J., Cheng Y., Howard K. Identification and genetic analysis of wunen, a gene guiding Drosophila melanogaster germ cell migration. Genetics. 1996 Jul;143(3):1231–1241. doi: 10.1093/genetics/143.3.1231. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES