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
. 1994 Jul 5;91(14):6634–6638. doi: 10.1073/pnas.91.14.6634

Drosophila mode of metamerization in the embryogenesis of the lepidopteran insect Manduca sexta.

R Kraft 1, H Jäckle 1
PMCID: PMC44257  PMID: 8022829

Abstract

Insect embryos have been classified as intermediate- and short-germ embryos, in which posterior segments are thought to be generated sequentially from an uncommitted growth zone, or as long-term embryos, such as Drosophila melanogaster, which develop primordia for all segments simultaneously. In Drosophila the coordinated activities among a three-tiered cascade of zygotic segmentation genes subdivide the embryo into progressively smaller units along the anterior-posterior axis. The mode of pattern specification in lepidopteran embryos has not been determined, although on morphological grounds they have been characterized as intermediate-germ insects. We have cloned orthologues of Drosophila segmentation genes from the tobacco hawkmoth Manduca sexta and have found that the blastoderm expression patterns of these genes show a molecular prepatterning typical of Drosophila. Thus, successive segment formation in Manduca embryos may not be due to sequential addition but rather may be the consequence of a lateral compression of the embryo proceeding in an anterior-to-posterior progression. These data challenge the view that the classification of insect development according to morphological criteria can serve as a reliable indicator of the molecular mechanisms underlying segmentation.

Full text

PDF
6634

Images in this article

6635Image
on p.6635
6637Image
on p.6637
6637Image
on p.6637

Selected References

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

  1. Akam M. The molecular basis for metameric pattern in the Drosophila embryo. Development. 1987 Sep;101(1):1–22. [PubMed] [Google Scholar]
  2. Baker N. E. Molecular cloning of sequences from wingless, a segment polarity gene in Drosophila: the spatial distribution of a transcript in embryos. EMBO J. 1987 Jun;6(6):1765–1773. doi: 10.1002/j.1460-2075.1987.tb02429.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carr J. N., Taghert P. H. Pair-rule expression of a cell surface molecule during gastrulation of the moth embryo. Development. 1989 Sep;107(1):143–151. doi: 10.1242/dev.107.1.143. [DOI] [PubMed] [Google Scholar]
  4. Chou Q., Russell M., Birch D. E., Raymond J., Bloch W. Prevention of pre-PCR mis-priming and primer dimerization improves low-copy-number amplifications. Nucleic Acids Res. 1992 Apr 11;20(7):1717–1723. doi: 10.1093/nar/20.7.1717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Copenhaver P. F., Taghert P. H. Development of the enteric nervous system in the moth. I. Diversity of cell types and the embryonic expression of FMRFamide-related neuropeptides. Dev Biol. 1989 Jan;131(1):70–84. doi: 10.1016/s0012-1606(89)80039-9. [DOI] [PubMed] [Google Scholar]
  6. Daga A., Tighe J. E., Calabi F. Leukaemia/Drosophila homology. Nature. 1992 Apr 9;356(6369):484–484. doi: 10.1038/356484b0. [DOI] [PubMed] [Google Scholar]
  7. French V. Insect development. The long and the short of it. Nature. 1993 Feb 4;361(6411):400–401. doi: 10.1038/361400a0. [DOI] [PubMed] [Google Scholar]
  8. Gergen J. P., Butler B. A. Isolation of the Drosophila segmentation gene runt and analysis of its expression during embryogenesis. Genes Dev. 1988 Sep;2(9):1179–1193. doi: 10.1101/gad.2.9.1179. [DOI] [PubMed] [Google Scholar]
  9. Higgins D. G., Sharp P. M. Fast and sensitive multiple sequence alignments on a microcomputer. Comput Appl Biosci. 1989 Apr;5(2):151–153. doi: 10.1093/bioinformatics/5.2.151. [DOI] [PubMed] [Google Scholar]
  10. Hülskamp M., Tautz D. Gap genes and gradients--the logic behind the gaps. Bioessays. 1991 Jun;13(6):261–268. doi: 10.1002/bies.950130602. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Kania M. A., Bonner A. S., Duffy J. B., Gergen J. P. The Drosophila segmentation gene runt encodes a novel nuclear regulatory protein that is also expressed in the developing nervous system. Genes Dev. 1990 Oct;4(10):1701–1713. doi: 10.1101/gad.4.10.1701. [DOI] [PubMed] [Google Scholar]
  13. Klingler M., Gergen J. P. Regulation of runt transcription by Drosophila segmentation genes. Mech Dev. 1993 Sep;43(1):3–19. doi: 10.1016/0925-4773(93)90019-t. [DOI] [PubMed] [Google Scholar]
  14. Knipple D. C., Seifert E., Rosenberg U. B., Preiss A., Jäckle H. Spatial and temporal patterns of Krüppel gene expression in early Drosophila embryos. Nature. 1985 Sep 5;317(6032):40–44. doi: 10.1038/317040a0. [DOI] [PubMed] [Google Scholar]
  15. Kraft R., Tardiff J., Krauter K. S., Leinwand L. A. Using mini-prep plasmid DNA for sequencing double stranded templates with Sequenase. Biotechniques. 1988 Jun;6(6):544-6, 549. [PubMed] [Google Scholar]
  16. Leptin M., Grunewald B. Cell shape changes during gastrulation in Drosophila. Development. 1990 Sep;110(1):73–84. doi: 10.1242/dev.110.1.73. [DOI] [PubMed] [Google Scholar]
  17. Mead D. A., Pey N. K., Herrnstadt C., Marcil R. A., Smith L. M. A universal method for the direct cloning of PCR amplified nucleic acid. Biotechnology (N Y) 1991 Jul;9(7):657–663. doi: 10.1038/nbt0791-657. [DOI] [PubMed] [Google Scholar]
  18. Miyoshi H., Shimizu K., Kozu T., Maseki N., Kaneko Y., Ohki M. t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10431–10434. doi: 10.1073/pnas.88.23.10431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nagy L. M., Booker R., Riddiford L. M. Isolation and embryonic expression of an abdominal-A-like gene from the lepidopteran, Manduca sexta. Development. 1991 May;112(1):119–129. doi: 10.1242/dev.112.1.119. [DOI] [PubMed] [Google Scholar]
  20. Nusse R., Varmus H. E. Wnt genes. Cell. 1992 Jun 26;69(7):1073–1087. doi: 10.1016/0092-8674(92)90630-u. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Pankratz M. J., Jäckle H. Making stripes in the Drosophila embryo. Trends Genet. 1990 Sep;6(9):287–292. doi: 10.1016/0168-9525(90)90234-w. [DOI] [PubMed] [Google Scholar]
  23. Patel N. H., Ball E. E., Goodman C. S. Changing role of even-skipped during the evolution of insect pattern formation. Nature. 1992 May 28;357(6376):339–342. doi: 10.1038/357339a0. [DOI] [PubMed] [Google Scholar]
  24. Patel N. H., Kornberg T. B., Goodman C. S. Expression of engrailed during segmentation in grasshopper and crayfish. Development. 1989 Oct;107(2):201–212. doi: 10.1242/dev.107.2.201. [DOI] [PubMed] [Google Scholar]
  25. Rijsewijk F., Schuermann M., Wagenaar E., Parren P., Weigel D., Nusse R. The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell. 1987 Aug 14;50(4):649–657. doi: 10.1016/0092-8674(87)90038-9. [DOI] [PubMed] [Google Scholar]
  26. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  27. Siegfried E., Chou T. B., Perrimon N. wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell. 1992 Dec 24;71(7):1167–1179. doi: 10.1016/s0092-8674(05)80065-0. [DOI] [PubMed] [Google Scholar]
  28. Sommer R. J., Retzlaff M., Goerlich K., Sander K., Tautz D. Evolutionary conservation pattern of zinc-finger domains of Drosophila segmentation genes. Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10782–10786. doi: 10.1073/pnas.89.22.10782. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sommer R. J., Tautz D. Involvement of an orthologue of the Drosophila pair-rule gene hairy in segment formation of the short germ-band embryo of Tribolium (Coleoptera) Nature. 1993 Feb 4;361(6411):448–450. doi: 10.1038/361448a0. [DOI] [PubMed] [Google Scholar]
  30. Sommer R., Tautz D. Segmentation gene expression in the housefly Musca domestica. Development. 1991 Oct;113(2):419–430. doi: 10.1242/dev.113.2.419. [DOI] [PubMed] [Google Scholar]
  31. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Treier M., Pfeifle C., Tautz D. Comparison of the gap segmentation gene hunchback between Drosophila melanogaster and Drosophila virilis reveals novel modes of evolutionary change. EMBO J. 1989 May;8(5):1517–1525. doi: 10.1002/j.1460-2075.1989.tb03536.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. van den Heuvel M., Nusse R., Johnston P., Lawrence P. A. Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication. Cell. 1989 Nov 17;59(4):739–749. doi: 10.1016/0092-8674(89)90020-2. [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