Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1991 Jul 1;88(13):5824–5828. doi: 10.1073/pnas.88.13.5824

Zygotic genes that mediate torso receptor tyrosine kinase functions in the Drosophila melanogaster embryo.

T R Strecker 1, M L Yip 1, H D Lipshitz 1
PMCID: PMC51970  PMID: 1905816

Abstract

The developmental signal that specifies the fates of cells at the anterior and posterior termini of the Drosophila embryo is transmitted by the torso receptor tyrosine kinase. This paper presents the results of a genetic interaction test for zygotic loci that act downstream of torso in the terminal genetic hierarchy. Tests of 26 zygotic mutants with defects in terminal development indicate that at least 14 reside in this hierarchy. The phenotypes associated with these genes fall into three classes, each of which represents a distinct aspect of terminal development and evolution. Four of the genes have been molecularly cloned and their products include an intercellular communication factor and three kinds of transcription factors.

Full text

PDF
5824

Images in this article

5826Image
on p.5826

Selected References

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

  1. Ambrosio L., Mahowald A. P., Perrimon N. Requirement of the Drosophila raf homologue for torso function. Nature. 1989 Nov 16;342(6247):288–291. doi: 10.1038/342288a0. [DOI] [PubMed] [Google Scholar]
  2. Carroll S. B., Scott M. P. Localization of the fushi tarazu protein during Drosophila embryogenesis. Cell. 1985 Nov;43(1):47–57. doi: 10.1016/0092-8674(85)90011-x. [DOI] [PubMed] [Google Scholar]
  3. Casanova J. Pattern formation under the control of the terminal system in the Drosophila embryo. Development. 1990 Oct;110(2):621–628. doi: 10.1242/dev.110.2.621. [DOI] [PubMed] [Google Scholar]
  4. Casanova J., Struhl G. Localized surface activity of torso, a receptor tyrosine kinase, specifies terminal body pattern in Drosophila. Genes Dev. 1989 Dec;3(12B):2025–2038. doi: 10.1101/gad.3.12b.2025. [DOI] [PubMed] [Google Scholar]
  5. Degelmann A., Hardy P. A., Mahowald A. P. Genetic analysis of two female-sterile loci affecting eggshell integrity and embryonic pattern formation in Drosophila melanogaster. Genetics. 1990 Oct;126(2):427–434. doi: 10.1093/genetics/126.2.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Degelmann A., Hardy P. A., Perrimon N., Mahowald A. P. Developmental analysis of the torso-like phenotype in Drosophila produced by a maternal-effect locus. Dev Biol. 1986 Jun;115(2):479–489. doi: 10.1016/0012-1606(86)90268-x. [DOI] [PubMed] [Google Scholar]
  7. Eldon E. D., Pirrotta V. Interactions of the Drosophila gap gene giant with maternal and zygotic pattern-forming genes. Development. 1991 Feb;111(2):367–378. doi: 10.1242/dev.111.2.367. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Irish V. F., Gelbart W. M. The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo. Genes Dev. 1987 Oct;1(8):868–879. doi: 10.1101/gad.1.8.868. [DOI] [PubMed] [Google Scholar]
  10. Jürgens G. Head and tail development of the Drosophila embryo involves spalt, a novel homeotic gene. EMBO J. 1988 Jan;7(1):189–196. doi: 10.1002/j.1460-2075.1988.tb02799.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Klingler M., Erdélyi M., Szabad J., Nüsslein-Volhard C. Function of torso in determining the terminal anlagen of the Drosophila embryo. Nature. 1988 Sep 15;335(6187):275–277. doi: 10.1038/335275a0. [DOI] [PubMed] [Google Scholar]
  12. Lehmann R., Nüsslein-Volhard C. hunchback, a gene required for segmentation of an anterior and posterior region of the Drosophila embryo. Dev Biol. 1987 Feb;119(2):402–417. doi: 10.1016/0012-1606(87)90045-5. [DOI] [PubMed] [Google Scholar]
  13. Macdonald P. M., Struhl G. A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature. 1986 Dec 11;324(6097):537–545. doi: 10.1038/324537a0. [DOI] [PubMed] [Google Scholar]
  14. Mayer U., Nüsslein-Volhard C. A group of genes required for pattern formation in the ventral ectoderm of the Drosophila embryo. Genes Dev. 1988 Nov;2(11):1496–1511. doi: 10.1101/gad.2.11.1496. [DOI] [PubMed] [Google Scholar]
  15. Mohler J., Eldon E. D., Pirrotta V. A novel spatial transcription pattern associated with the segmentation gene, giant, of Drosophila. EMBO J. 1989 May;8(5):1539–1548. doi: 10.1002/j.1460-2075.1989.tb03538.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Muriel W. J., Cole J., Lehmann A. R. Molecular analysis of ouabain-resistant mutants of the mouse lymphoma cell line L5178Y. Mutagenesis. 1987 Sep;2(5):383–389. doi: 10.1093/mutage/2.5.383. [DOI] [PubMed] [Google Scholar]
  17. Nüsslein-Volhard C., Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature. 1980 Oct 30;287(5785):795–801. doi: 10.1038/287795a0. [DOI] [PubMed] [Google Scholar]
  18. Parks S., Wieschaus E. The Drosophila gastrulation gene concertina encodes a G alpha-like protein. Cell. 1991 Jan 25;64(2):447–458. doi: 10.1016/0092-8674(91)90652-f. [DOI] [PubMed] [Google Scholar]
  19. Pignoni F., Baldarelli R. M., Steingrímsson E., Diaz R. J., Patapoutian A., Merriam J. R., Lengyel J. A. The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily. Cell. 1990 Jul 13;62(1):151–163. doi: 10.1016/0092-8674(90)90249-e. [DOI] [PubMed] [Google Scholar]
  20. Sprenger F., Stevens L. M., Nüsslein-Volhard C. The Drosophila gene torso encodes a putative receptor tyrosine kinase. Nature. 1989 Apr 6;338(6215):478–483. doi: 10.1038/338478a0. [DOI] [PubMed] [Google Scholar]
  21. St Johnston R. D., Gelbart W. M. Decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J. 1987 Sep;6(9):2785–2791. doi: 10.1002/j.1460-2075.1987.tb02574.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Stevens L. M., Frohnhöfer H. G., Klingler M., Nüsslein-Volhard C. Localized requirement for torso-like expression in follicle cells for development of terminal anlagen of the Drosophila embryo. Nature. 1990 Aug 16;346(6285):660–663. doi: 10.1038/346660a0. [DOI] [PubMed] [Google Scholar]
  23. Strecker T. R., Halsell S. R., Fisher W. W., Lipshitz H. D. Reciprocal effects of hyper- and hypoactivity mutations in the Drosophila pattern gene torso. Science. 1989 Feb 24;243(4894 Pt 1):1062–1066. doi: 10.1126/science.2922596. [DOI] [PubMed] [Google Scholar]
  24. Strecker T. R., Kongsuwan K., Lengyel J. A., Merriam J. R. The zygotic mutant tailless affects the anterior and posterior ectodermal regions of the Drosophila embryo. Dev Biol. 1986 Jan;113(1):64–76. doi: 10.1016/0012-1606(86)90108-9. [DOI] [PubMed] [Google Scholar]
  25. Strecker T. R., Lengyel J. A. Anterior-posterior pattern formation: an evolutionary perspective on genes specifying terminal domains. Bioessays. 1988 Jul;9(1):3–7. doi: 10.1002/bies.950090102. [DOI] [PubMed] [Google Scholar]
  26. Strecker T. R., Merriam J. R., Lengyel J. A. Graded requirement for the zygotic terminal gene, tailless, in the brain and tail region of the Drosophila embryo. Development. 1988 Apr;102(4):721–734. doi: 10.1242/dev.102.4.721. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Weigel D., Jürgens G., Klingler M., Jäckle H. Two gap genes mediate maternal terminal pattern information in Drosophila. Science. 1990 Apr 27;248(4954):495–498. doi: 10.1126/science.2158673. [DOI] [PubMed] [Google Scholar]
  29. Wieschaus E., Nusslein-Volhard C., Kluding H. Krüppel, a gene whose activity is required early in the zygotic genome for normal embryonic segmentation. Dev Biol. 1984 Jul;104(1):172–186. doi: 10.1016/0012-1606(84)90046-0. [DOI] [PubMed] [Google Scholar]
  30. Zusman S. B., Sweeton D., Wieschaus E. F. short gastrulation, a mutation causing delays in stage-specific cell shape changes during gastrulation in Drosophila melanogaster. Dev Biol. 1988 Oct;129(2):417–427. doi: 10.1016/0012-1606(88)90389-2. [DOI] [PubMed] [Google Scholar]
  31. Zusman S. B., Wieschaus E. F. Requirements for zygotic gene activity during gastrulation in Drosophila melanogaster. Dev Biol. 1985 Oct;111(2):359–371. doi: 10.1016/0012-1606(85)90490-7. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES