Skip to main content
Genetics logoLink to Genetics
. 1999 Feb;151(2):685–695. doi: 10.1093/genetics/151.2.685

Identification of genes controlling malpighian tubule and other epithelial morphogenesis in Drosophila melanogaster.

X Liu 1, I Kiss 1, J A Lengyel 1
PMCID: PMC1460502  PMID: 9927461

Abstract

The Drosophila Malpighian tubule is a model system for studying genetic mechanisms that control epithelial morphogenesis. From a screen of 1800 second chromosome lethal lines, by observing uric acid deposits in unfixed inviable embryos, we identified five previously described genes (barr, fas, flb, raw, and thr) and one novel gene, walrus (wal), that affect Malpighian tubule morphogenesis. Phenotypic analysis of these mutant embryos allows us to place these genes, along with other previously described genes, into a genetic pathway that controls Malpighian tubule development. Specifically, wal affects evagination of the Malpighian tubule buds, fas and thr affect bud extension, and barr, flb, raw, and thr affect tubule elongation. In addition, these genes were found to have different effects on development of other epithelial structures, such as foregut and hindgut morphogenesis. Finally, from the same screen, we identified a second novel gene, drumstick, that affects only foregut and hindgut morphogenesis.

Full Text

The Full Text of this article is available as a PDF (377.4 KB).

Selected References

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

  1. Bhat M. A., Philp A. V., Glover D. M., Bellen H. J. Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with Topoisomerase II. Cell. 1996 Dec 13;87(6):1103–1114. doi: 10.1016/s0092-8674(00)81804-8. [DOI] [PubMed] [Google Scholar]
  2. Blochlinger K., Bodmer R., Jan L. Y., Jan Y. N. Patterns of expression of cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos. Genes Dev. 1990 Aug;4(8):1322–1331. doi: 10.1101/gad.4.8.1322. [DOI] [PubMed] [Google Scholar]
  3. D'Andrea R. J., Stratmann R., Lehner C. F., John U. P., Saint R. The three rows gene of Drosophila melanogaster encodes a novel protein that is required for chromosome disjunction during mitosis. Mol Biol Cell. 1993 Nov;4(11):1161–1174. doi: 10.1091/mbc.4.11.1161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Diaz R. J., Harbecke R., Singer J. B., Pignoni F., Janning W., Lengyel J. A. Graded effect of tailless on posterior gut development: molecular basis of an allelic series of a nuclear receptor gene. Mech Dev. 1996 Jan;54(1):119–130. doi: 10.1016/0925-4773(95)00467-x. [DOI] [PubMed] [Google Scholar]
  5. Eberl D. F., Hilliker A. J. Characterization of X-linked recessive lethal mutations affecting embryonic morphogenesis in Drosophila melanogaster. Genetics. 1988 Jan;118(1):109–120. doi: 10.1093/genetics/118.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Francois V., Solloway M., O'Neill J. W., Emery J., Bier E. Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene. Genes Dev. 1994 Nov 1;8(21):2602–2616. doi: 10.1101/gad.8.21.2602. [DOI] [PubMed] [Google Scholar]
  7. Gaul U., Weigel D. Regulation of Krüppel expression in the anlage of the Malpighian tubules in the Drosophila embryo. Mech Dev. 1990 Dec;33(1):57–67. doi: 10.1016/0925-4773(90)90135-9. [DOI] [PubMed] [Google Scholar]
  8. Hacohen N., Kramer S., Sutherland D., Hiromi Y., Krasnow M. A. sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell. 1998 Jan 23;92(2):253–263. doi: 10.1016/s0092-8674(00)80919-8. [DOI] [PubMed] [Google Scholar]
  9. Hall A. Rho GTPases and the actin cytoskeleton. Science. 1998 Jan 23;279(5350):509–514. doi: 10.1126/science.279.5350.509. [DOI] [PubMed] [Google Scholar]
  10. Harbecke R., Janning W. The segmentation gene Krüppel of Drosophila melanogaster has homeotic properties. Genes Dev. 1989 Jan;3(1):114–122. doi: 10.1101/gad.3.1.114. [DOI] [PubMed] [Google Scholar]
  11. Hoch M., Broadie K., Jäckle H., Skaer H. Sequential fates in a single cell are established by the neurogenic cascade in the Malpighian tubules of Drosophila. Development. 1994 Dec;120(12):3439–3450. doi: 10.1242/dev.120.12.3439. [DOI] [PubMed] [Google Scholar]
  12. Hoch M., Pankratz M. J. Control of gut development by fork head and cell signaling molecules in Drosophila. Mech Dev. 1996 Aug;58(1-2):3–14. doi: 10.1016/s0925-4773(96)00541-2. [DOI] [PubMed] [Google Scholar]
  13. Häcker U., Perrimon N. DRhoGEF2 encodes a member of the Dbl family of oncogenes and controls cell shape changes during gastrulation in Drosophila. Genes Dev. 1998 Jan 15;12(2):274–284. doi: 10.1101/gad.12.2.274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jack J., Myette G. The genes raw and ribbon are required for proper shape of tubular epithelial tissues in Drosophila. Genetics. 1997 Sep;147(1):243–253. doi: 10.1093/genetics/147.1.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kerber B., Fellert S., Hoch M. Seven-up, the Drosophila homolog of the COUP-TF orphan receptors, controls cell proliferation in the insect kidney. Genes Dev. 1998 Jun 15;12(12):1781–1786. doi: 10.1101/gad.12.12.1781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kispert A., Herrmann B. G., Leptin M., Reuter R. Homologs of the mouse Brachyury gene are involved in the specification of posterior terminal structures in Drosophila, Tribolium, and Locusta. Genes Dev. 1994 Sep 15;8(18):2137–2150. doi: 10.1101/gad.8.18.2137. [DOI] [PubMed] [Google Scholar]
  17. Lekven A. C., Tepass U., Keshmeshian M., Hartenstein V. faint sausage encodes a novel extracellular protein of the immunoglobulin superfamily required for cell migration and the establishment of normal axonal pathways in the Drosophila nervous system. Development. 1998 Jul;125(14):2747–2758. doi: 10.1242/dev.125.14.2747. [DOI] [PubMed] [Google Scholar]
  18. Leptin M. Drosophila gastrulation: from pattern formation to morphogenesis. Annu Rev Cell Dev Biol. 1995;11:189–212. doi: 10.1146/annurev.cb.11.110195.001201. [DOI] [PubMed] [Google Scholar]
  19. Liu S., Jack J. Regulatory interactions and role in cell type specification of the Malpighian tubules by the cut, Krüppel, and caudal genes of Drosophila. Dev Biol. 1992 Mar;150(1):133–143. doi: 10.1016/0012-1606(92)90013-7. [DOI] [PubMed] [Google Scholar]
  20. Meadows L. A., Gell D., Broadie K., Gould A. P., White R. A. The cell adhesion molecule, connectin, and the development of the Drosophila neuromuscular system. J Cell Sci. 1994 Jan;107(Pt 1):321–328. doi: 10.1242/jcs.107.1.321. [DOI] [PubMed] [Google Scholar]
  21. Noselli S. JNK signaling and morphogenesis in Drosophila. Trends Genet. 1998 Jan;14(1):33–38. doi: 10.1016/S0168-9525(97)01320-6. [DOI] [PubMed] [Google Scholar]
  22. Philp A. V., Axton J. M., Saunders R. D., Glover D. M. Mutations in the Drosophila melanogaster gene three rows permit aspects of mitosis to continue in the absence of chromatid segregation. J Cell Sci. 1993 Sep;106(Pt 1):87–98. doi: 10.1242/jcs.106.1.87. [DOI] [PubMed] [Google Scholar]
  23. Rehorn K. P., Thelen H., Michelson A. M., Reuter R. A molecular aspect of hematopoiesis and endoderm development common to vertebrates and Drosophila. Development. 1996 Dec;122(12):4023–4031. doi: 10.1242/dev.122.12.4023. [DOI] [PubMed] [Google Scholar]
  24. Singer J. B., Harbecke R., Kusch T., Reuter R., Lengyel J. A. Drosophila brachyenteron regulates gene activity and morphogenesis in the gut. Development. 1996 Dec;122(12):3707–3718. doi: 10.1242/dev.122.12.3707. [DOI] [PubMed] [Google Scholar]
  25. Stratmann R., Lehner C. F. Separation of sister chromatids in mitosis requires the Drosophila pimples product, a protein degraded after the metaphase/anaphase transition. Cell. 1996 Jan 12;84(1):25–35. doi: 10.1016/s0092-8674(00)80990-3. [DOI] [PubMed] [Google Scholar]
  26. Tepass U., Theres C., Knust E. crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell. 1990 Jun 1;61(5):787–799. doi: 10.1016/0092-8674(90)90189-l. [DOI] [PubMed] [Google Scholar]
  27. Török T., Tick G., Alvarado M., Kiss I. P-lacW insertional mutagenesis on the second chromosome of Drosophila melanogaster: isolation of lethals with different overgrowth phenotypes. Genetics. 1993 Sep;135(1):71–80. doi: 10.1093/genetics/135.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES