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. 1991 Dec;10(13):4259–4266. doi: 10.1002/j.1460-2075.1991.tb05004.x

The temporal and spatial distribution pattern of maternal exuperantia protein: evidence for a role in establishment but not maintenance of bicoid mRNA localization.

D Marcey 1, W S Watkins 1, T Hazelrigg 1
PMCID: PMC453178  PMID: 1756733

Abstract

The exuperantia (exu) gene of Drosophila melanogaster plays a fundamental role in the establishment of polarity of the oocyte and early embryo by ensuring the proper localization of the mRNA of the bicoid (bcd) gene to anterior regions of the oocyte. We have isolated and sequenced the exu gene, sequenced its female-specific transcript and a mutant allele of exu that affects primarily exu's female germline function, and determined the temporal and spatial pattern of exu protein expression during oogenesis. The exu protein is basic, with at least one basic residue being identified as necessary for exu function in the female germline, and is present transiently during oogenesis. Our results suggest that exu is not required for the maintenance of bcd mRNA localization during late stages of oogenesis and early embryogenesis, but rather for the establishment of bcd mRNA localization in the developing oocyte. We propose that the exu protein may serve to modify a component that binds bcd mRNA or to modify the bcd message itself, or may perform a role in docking the bcd mRNA at its site of localization in the developing oocyte.

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Selected References

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

  1. Bandziulis R. J., Swanson M. S., Dreyfuss G. RNA-binding proteins as developmental regulators. Genes Dev. 1989 Apr;3(4):431–437. doi: 10.1101/gad.3.4.431. [DOI] [PubMed] [Google Scholar]
  2. Berleth T., Burri M., Thoma G., Bopp D., Richstein S., Frigerio G., Noll M., Nüsslein-Volhard C. The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J. 1988 Jun;7(6):1749–1756. doi: 10.1002/j.1460-2075.1988.tb03004.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cohen S. M., Jürgens G. Mediation of Drosophila head development by gap-like segmentation genes. Nature. 1990 Aug 2;346(6283):482–485. doi: 10.1038/346482a0. [DOI] [PubMed] [Google Scholar]
  4. Dalton D., Chadwick R., McGinnis W. Expression and embryonic function of empty spiracles: a Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev. 1989 Dec;3(12A):1940–1956. doi: 10.1101/gad.3.12a.1940. [DOI] [PubMed] [Google Scholar]
  5. Dreyfuss G., Swanson M. S., Piñol-Roma S. Heterogeneous nuclear ribonucleoprotein particles and the pathway of mRNA formation. Trends Biochem Sci. 1988 Mar;13(3):86–91. doi: 10.1016/0968-0004(88)90046-1. [DOI] [PubMed] [Google Scholar]
  6. Driever W., Nüsslein-Volhard C. A gradient of bicoid protein in Drosophila embryos. Cell. 1988 Jul 1;54(1):83–93. doi: 10.1016/0092-8674(88)90182-1. [DOI] [PubMed] [Google Scholar]
  7. Driever W., Nüsslein-Volhard C. The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell. 1988 Jul 1;54(1):95–104. doi: 10.1016/0092-8674(88)90183-3. [DOI] [PubMed] [Google Scholar]
  8. Driever W., Nüsslein-Volhard C. The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. Nature. 1989 Jan 12;337(6203):138–143. doi: 10.1038/337138a0. [DOI] [PubMed] [Google Scholar]
  9. Driever W., Thoma G., Nüsslein-Volhard C. Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen. Nature. 1989 Aug 3;340(6232):363–367. doi: 10.1038/340363a0. [DOI] [PubMed] [Google Scholar]
  10. Finkelstein R., Perrimon N. The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature. 1990 Aug 2;346(6283):485–488. doi: 10.1038/346485a0. [DOI] [PubMed] [Google Scholar]
  11. Hazelrigg T., Watkins W. S., Marcey D., Tu C., Karow M., Lin X. R. The exuperantia gene is required for Drosophila spermatogenesis as well as anteroposterior polarity of the developing oocyte, and encodes overlapping sex-specific transcripts. Genetics. 1990 Nov;126(3):607–617. doi: 10.1093/genetics/126.3.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ingham P. W. The molecular genetics of embryonic pattern formation in Drosophila. Nature. 1988 Sep 1;335(6185):25–34. doi: 10.1038/335025a0. [DOI] [PubMed] [Google Scholar]
  13. Lawrence J. B., Singer R. H. Intracellular localization of messenger RNAs for cytoskeletal proteins. Cell. 1986 May 9;45(3):407–415. doi: 10.1016/0092-8674(86)90326-0. [DOI] [PubMed] [Google Scholar]
  14. MacDonald P. M. bicoid mRNA localization signal: phylogenetic conservation of function and RNA secondary structure. Development. 1990 Sep;110(1):161–171. doi: 10.1242/dev.110.1.161. [DOI] [PubMed] [Google Scholar]
  15. Macdonald P. M., Struhl G. cis-acting sequences responsible for anterior localization of bicoid mRNA in Drosophila embryos. Nature. 1988 Dec 8;336(6199):595–598. doi: 10.1038/336595a0. [DOI] [PubMed] [Google Scholar]
  16. Melton D. A. Translocation of a localized maternal mRNA to the vegetal pole of Xenopus oocytes. Nature. 1987 Jul 2;328(6125):80–82. doi: 10.1038/328080a0. [DOI] [PubMed] [Google Scholar]
  17. Query C. C., Bentley R. C., Keene J. D. A common RNA recognition motif identified within a defined U1 RNA binding domain of the 70K U1 snRNP protein. Cell. 1989 Apr 7;57(1):89–101. doi: 10.1016/0092-8674(89)90175-x. [DOI] [PubMed] [Google Scholar]
  18. Robertson H. M., Preston C. R., Phillis R. W., Johnson-Schlitz D. M., Benz W. K., Engels W. R. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 1988 Mar;118(3):461–470. doi: 10.1093/genetics/118.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rogers S., Wells R., Rechsteiner M. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science. 1986 Oct 17;234(4774):364–368. doi: 10.1126/science.2876518. [DOI] [PubMed] [Google Scholar]
  20. Rosenberg A. H., Lade B. N., Chui D. S., Lin S. W., Dunn J. J., Studier F. W. Vectors for selective expression of cloned DNAs by T7 RNA polymerase. Gene. 1987;56(1):125–135. doi: 10.1016/0378-1119(87)90165-x. [DOI] [PubMed] [Google Scholar]
  21. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schupbach T., Wieschaus E. Germline autonomy of maternal-effect mutations altering the embryonic body pattern of Drosophila. Dev Biol. 1986 Feb;113(2):443–448. doi: 10.1016/0012-1606(86)90179-x. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Seeger M. A., Kaufman T. C. Molecular analysis of the bicoid gene from Drosophila pseudoobscura: identification of conserved domains within coding and noncoding regions of the bicoid mRNA. EMBO J. 1990 Sep;9(9):2977–2987. doi: 10.1002/j.1460-2075.1990.tb07490.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Spradling A. C., Rubin G. M. Transposition of cloned P elements into Drosophila germ line chromosomes. Science. 1982 Oct 22;218(4570):341–347. doi: 10.1126/science.6289435. [DOI] [PubMed] [Google Scholar]
  26. St Johnston D., Driever W., Berleth T., Richstein S., Nüsslein-Volhard C. Multiple steps in the localization of bicoid RNA to the anterior pole of the Drosophila oocyte. Development. 1989;107 (Suppl):13–19. doi: 10.1242/dev.107.Supplement.13. [DOI] [PubMed] [Google Scholar]
  27. Stephenson E. C., Chao Y. C., Fackenthal J. D. Molecular analysis of the swallow gene of Drosophila melanogaster. Genes Dev. 1988 Dec;2(12A):1655–1665. doi: 10.1101/gad.2.12a.1655. [DOI] [PubMed] [Google Scholar]
  28. Struhl G., Struhl K., Macdonald P. M. The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell. 1989 Jun 30;57(7):1259–1273. doi: 10.1016/0092-8674(89)90062-7. [DOI] [PubMed] [Google Scholar]
  29. Yisraeli J. K., Sokol S., Melton D. A. The process of localizing a maternal messenger RNA in Xenopus oocytes. Development. 1989;107 (Suppl):31–36. doi: 10.1242/dev.107.Supplement.31. [DOI] [PubMed] [Google Scholar]

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